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Research

An Update on Biotechnological Approaches for Improving Abiotic Stress Tolerance in Tomato Shashank K. Pandey, Akula Nookaraju, Chandrama P. Upadhyaya, Mayank A. Gururani, Jelli Venkatesh, Doo-Hwan Kim, and Se Won Park*

ABSTRACT Tomato (Solanum lycopersicum L.) is the second most important vegetable crop in the world after potato (Solanum tuberosum L.), and its productivity is influenced by different abiotic stresses. Though cultivated tomato is moderately tolerant to various abiotic stresses, the crop losses due to unfavorable environmental conditions can be unpredictably severe. So far, several efforts have been made to improve abiotic stress tolerance in cultivated tomato through cultural practices, breeding techniques, and biotechnological approaches. Introgression of abiotic stress tolerance to cultivated tomato from more tolerant wild relatives through classical breeding has been attempted with limited success. However, genetic engineering based on the introgression of genes that are known to be involved in stress response and putative stress tolerance could provide powerful tools for improving abiotic stress tolerance in tomato coupled with the growing knowledge of stress physiology. The present review summarizes the current status and future directions on the use of biotechnological approaches to improve abiotic stress tolerance in tomato.

Dep. of Molecular Biotechnology, Konkuk Univ., Seoul 143 701, Korea. S.K. Pandey and A. Nookaraju contributed equally to this work. Received 5 Oct. 2010. *Corresponding author (sewpark@konkuk. ac.kr). Co-corresponding author D.-H. Kim ([email protected]). Abbreviations: ABA, abscisic acid; ABREs, ABA-responsive elements; ACC, 1-aminocyclopropane-1-carboxylate; AMF, arbuscular mycorrhizal fungi; APX, ascorbate peroxidase; AQP, aquaporin; AREB, ABAresponse element binding factor (ABF); AsA, ascorbic acid; BADH, betaine aldehyde dehydrogenase; BIBAC, binary bacterial artificial chromosome; bZIP, basic-domain leucine zipper; CBF, CSL family of DNA-binding proteins; CDPK, calcium-dependent protein kinase; DREB, dehydration response element binding factor; DRE/CRT, dehydration-responsive elements/C-repeat; ER, endoplasmic reticulum; ERF, ethylene-responsive transcription factor; GB, glycine betaine; GSH, glutathione; HSP, heat shock protein; JA, jasmonic acid; LEA, late embryogenesis-associated; MAPK, mitogen activated protein kinase; mt1D, mannitol-1-phosphate dehydrogenase; PPO, polyphenol oxidase; PR, pathogenesis-related; PS, photosystem; ROS, reactive oxygen species; SA, salicylic acid; SAP, stressassociated protein; SOD, superoxide dismutase.

T

omato (Solanum lycopersicum L.) is the second most important vegetable crop in the world after potato (Solanum tuberosum L.) in terms of per capita consumption. Being a tropical plant, tomato is well adapted to almost all climatic regions of the world and is cultivated in an area of 4.8 million ha worldwide with a production of ca. 136.2 million Mg (FAOSTAT, 2010). The production of tomato is influenced by several biotic and abiotic factors. While biotic stress responses are well investigated in plants, the responses to abiotic stress are more complex and not clearly understood (Hazen et al., 2003; Kawaguchi et al., 2003, 2004). Abiotic stress is a broad term, which includes multiple stresses such as high temperature, chilling,

Published in Crop Sci. 51:1–22 (2011). doi: 10.2135/cropsci2010.10.0579 Published online DATE. © Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher. crop science, vol. 51, september– october 2011

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excessive light, drought, water logging, wounding, and exposure to ozone, UV-B irradiation, osmotic shock, and salinity. Tomato is highly sensitive to chilling or cold stress, which inhibits seed germination during early stages of plant growth (Foolad and Lin, 2000, 2001), whereas in later stages it affects reproductive development causing homeotic floral transformations (Lozano et al., 1998). Fruit set also decreases due to poor pollen germination (Fernandez-Munoz et al., 1995) and fruits at ripening stage suffer chilling injury (Jackman et al., 1989; Sharom et al., 1994). Soil salinity related to excess amounts (0.20–0.25%) of sodium, calcium, magnesium, chlorides, sulfates, or carbonates is primarily caused by irrigation disturbances. Soil salinity severely inhibits seed germination and early seedling growth in susceptible tomato cultivars (Cook, 1979; Foolad and Jones, 1991). High soil salinity causes oxidative stress leading to disruption of the chloroplast thylakoidal and stromal membranes, cell membrane damage by membrane peroxidation, protein denaturation, and DNA damage (Benavides et al., 2000; Fidalgo et al., 2004; Rahnama and Ebrahimzadeh, 2005). Water deficit leads to decreased cell turgidity, stomatal closure, growth inhibition, and decreased respiration and photosynthesis (Holmberg and Bulow, 1998; Venema et al., 2005). Adverse effects of drought are augmented by high temperature and cause disintegration of polyribosomes, leading to alteration of polypeptide synthesis (Angeloni and Potts, 1986). Water logging results in a gradual increase of lipid peroxidation and in vivo hydrogen peroxide (H2O2) concentration in roots of tomato, leading to severe oxidative damage (Ahsan et al., 2007).

responsive elements/C-repeat (DRE/CRT), ABA-responsive elements (ABREs), and/or MYB/MYC recognition elements, which are regulated by DREB1A (dehydration response element binding factors) and CBF (CSL family of DNA-binding proteins), basic-domain leucine zipper (bZIP), and MYC/MYB factors, respectively. The DRE/CRT elements regulate gene expression in response to dehydration (salt, drought, and cold stresses), while ABRE and MYB/ MYC elements control gene expression in response to ABA under abiotic stresses (Thomashow, 1999; Shinozaki and Yamaguchi-Shinozaki, 2000) (Fig. 1). Stress-induced gene expression can be broadly categorized into three groups. The first group includes genes encoding proteins with known enzymatic or structural functions, the second group includes regulatory proteins and transcription factors and the third group includes proteins with unknown function(s) (Shinozaki and Yamaguchi-Shinozaki, 1997). Stress-induced proteins such as water channel proteins, key enzymes for synthesis of osmolytes or osmoprotectants (proline, mannitol, betaine, sugars, and polyamines), LEA proteins, proteinases, channel proteins, molecular chaperones, detoxification enzymes, and transport proteins (Bohnert and Jensen, 1996; Bray, 1997) are some of the examples of the first group of proteins. The second category of stress-inducible genes comprises regulatory genes involved in plant tolerance to abiotic stresses, which include transcription factors, protein kinases, phospholipase C, and 14-3-3 protein (Shinozaki and Yamaguchi-Shinozaki, 1997). Many of these genes show enhanced expression under abiotic stress and impart stress tolerance to plants.

PHYSIOLOGY OF ABIOTIC STRESS TOLERANCE

STRATEGIES EMPLOYED TO ENHANCE ABIOTIC STRESS TOLERANCE IN TOMATO

Plants respond to different abiotic stresses by exhibiting complex and quantitative traits involving the expression of many genes that trigger tolerance mechanisms (Blum, 1988; Zhu et al., 1997; Subudhi et al., 2000). An efficient approach toward increasing stress tolerance requires a thorough understanding of the functions of these stress-inducible genes and molecular mechanisms that condition abiotic stress tolerance. In general, the first step in any abiotic stress response is the perception of stress signals by cell wall receptors followed by signal transduction events involving second messengers like cytosolic Ca2+, abscisic acid (ABA), and kinases leading to activation of specific transcription factors and cis-acting elements. These transcription factors and cis-acting elements modulate the expression of stress-response genes leading to the synthesis of stress-related gene products and subsequent manifestation of stress tolerance. Many stress-related genes regulated at the transcriptional level show altered mRNA expression in response to abiotic stresses (Shinozaki and YamaguchiShinozaki, 1997; Cheong et al., 2002; Shinozaki et al., 2003). Promoters of many stress-related genes such as late embryogenesis-associated (LEA) genes contain dehydration 2

Recent advances in molecular genetic techniques, including genetic transformation, molecular marker mapping, and quantitative trait loci analysis have contributed significantly to a better understanding of the genetic, physiological, and biochemical basis of plant tolerance to abiotic stresses and have facilitated the development of plants with enhanced tolerance. Here we summarize various strategies employed to improve resistance in tomato for different abiotic stresses.

In Vitro Screening of Tomato for Abiotic Stress Tolerance Screening of a few plant cells and tissues under in vitro conditions instead of screening a large population of plants in fields offers a convenient and quick method for detecting variations in abiotic stress tolerance in crop plants. There are several reports on the development of cell lines with increased tolerance to drought in tomato (Cano et al., 1998; Kulkarni and Deshpande, 2007; Singh and Sharma, 2008). Cano et al. (1998) screened cultivated and wild tomato species in vitro for salt tolerance using shoot apices. There were

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crop science, vol. 51, september– october 2011

Cultural Strategies Several studies have suggested that plants naturally exhibit various physiological and biochemical mechanisms to respond and adapt to stresses through production of signal molecules such as ABA, Ca2+, jasmonic acid (JA), ethylene, and salicylic acid (SA), which function as signal transducers or messengers of environmental stresses and trigger defense responses. These defense responses are displayed by activation of genes coding for osmoprotectants and other functional proteins. There are several reports on use of these signal molecules and osmoprotectants in tomato that showed enhanced tolerance to various abiotic stresses (Mäkelä et al., 1998, 1999; Park et al., 2006; Flors et al., 2007). Reduced accumulation of ABA by exogenous application of gibberellic acid to tomato plants grown under salt stress resulted in reduced stomatal resistance and enhanced water use leading to enhanced salt stress (Maggio et al., 2010). Foliar application of glycine betaine (GB) to tomato plants during the vegetative stage enhanced stomatal conductance and protein and chlorophyll contents while decreasing photo-respiration under salt stress (Mäkelä et al., 1998, 1999). Similarly, Park et al. (2006) reported the exogenous application of GB improved chilling tolerance in tomato by protecting macromolecules and membranes directly and by inducing H2O2–mediated antioxidant mechanisms. Supplementation of ascorbic acid (AsA) in the rooting medium was found to enhance the tolerance of tomato seedlings to oxidative stress induced by NaCl (300 mM) (Shalata and Neumann, 2001). Enhanced salt tolerance in the tomato seedlings was proposed to be mediated through quenching of reactive oxygen species (ROS) by AsA. In another study, tomato plants treated with adipic acid monoethylester and 1,3-diaminepropane exhibited increased salt stress tolerance with a faster and stronger reduction of water potential and enhanced proline accumulation (Flors et al., 2007). Oxidative membrane damage and ethylene emission were both reduced in 1,3-diaminepropane–treated plants probably due to increases in the levels of nonenzymatic antioxidants as well as peroxidase activity. In another study, application of silica at the root zone imparted salinity crop science, vol. 51, september– october 2011

Figure 1. Abiotic signal perception, transduction and induction of stress induced genes in plants. ABA-independent DREB2 and ABA-dependent CBF4 transcription factors transactivate DRE/ CRT cis-elements in the promoters of LEA type genes. ABAdependent pathways regulate LEA type genes through MYC/ MYB and bZIP type transcription factors. CBFs bind to CRT/ DRE cis-elements on the promoter of LEA-type genes and induce expression of these genes. ABA, abscisic acid; bZIP, basic-domain leucine zipper; CBF, CSL family of DNA-binding proteins; CRT/DRE, dehydration responsive elements/C-repeat; DREB, dehydration response element binding factors; LEA, late embryogenesis-associated; MYC/MYB.

tolerance to tomato plants grown under high salt conditions (Romero-Aranda et al., 2006). The enhanced salt tolerance in this study was attributed to the deposition of silicate crystals in the epidermal cells forming a barrier to water loss through cuticle. A wound-inducible signal peptide systemin was found to be involved in salt tolerance in tomato plants (Capiati et al., 2006), and the systemin along with JA was suggested to increase salt stress tolerance in parallel with a Ca2+-dependent protein kinase, LeCDPK-1, which induces downstream signaling leading to cross tolerance of both wound and salt stress. These results clearly suggested a potent role of Ca2+ and JA in tolerance to salinity in tomato.

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significant differences observed in rooting characteristics between cultivated and wild species, suggesting that rooting parameters are the most useful traits for rapid evaluation and screening of tomato species and segregating populations. Kulkarni and Deshpande (2007) screened Indian tomato accessions in vitro for drought tolerance using polyethylene glycol. Similar screening of tomato cultivars were reported with Iranian cultivars of tomato by Aazami et al. (2010). These in vitro studies were further complemented with field evaluation. It has also been suggested that the repeated in vitro culture of tomato cell lines on the medium containing the stress-inducing agent allowed for generation of drought-tolerant plants (Abdel-Raheem et al., 2007; Singh and Sharma, 2008).


Another way to reduce crop losses due to salinity is the use of salt-resistant rootstocks. Several attempts have been made to improve salt stress tolerance in tomato by grafting on resistant rootstocks (Santa-Cruz et al., 2001, 2002; Estan et al., 2005). Fruit yield at 50 mM NaCl stress increased in plants of tomato ‘Moneymaker’ grafted onto ‘Pera’ and ‘Rajda’ compared with self-grafted tomato plants (Santa-Cruz et al., 2001; Martinez-Rodriguez et al., 2008). Similarly, grafting of ‘Jaquar’ shoots on salt-resistant rootstocks Radja, Pera, and the hybrid ‘Volgogradskij’ × Pera increased tomato fruit yield by 80% compared with Jaquar plants on their own rootstock (Estan et al., 2005). This strategy could also provide plant breeders with the possibility of combining good shoot characters with good root characters in cultivated tomato and for studying the contribution of genes transcribed in roots toward the performance of the shoot (Zijlstra et al., 1994; Pardo et al., 1998). It is well known that aquaporins (AQPs) significantly contribute to water movement in plants and are regulated both at transcriptional and enzymatic levels by phosphorylation as short-term responses to stresses like drought and salinity (Maurel et al., 1995; Johansson et al., 1996). The expression of AQP genes was enhanced on colonization of tomato leaves by arbuscular mycorrhizal fungi (AMF) under salt stress (Ouziad et al., 2006). This study suggests that AMF influence AQP expression in tomato plants under salt stress. Similarly, plant growth–promoting rhizobacteria found in association with crop plants grown under chronically stressful conditions such as high salinity could provide a significant benefit to the plants. These bacteria can either directly or indirectly facilitate rooting (Mayak et al., 1999) and aid in growth of plants (Glick, 1995). They also aid in plant growth by providing plants with fixed nitrogen, phytohormones, iron, and soluble phosphates. Some bacteria are also known to synthesize 1-aminocyclopropane-1-carboxylate (ACC) deaminase to metabolize ACC, a precursor of ethylene (Jacobson et al., 1994; Glick, 1995), which reduces inhibition of root growth by ethylene. The plant growth-promoting bacterium Achromobacter piechaudii, which has ACC deaminase activity, promoted the growth of tomato seedlings under salt stress (172 mM NaCl) (Mayak et al., 2004). Plant growth–promoting rhizobacteria and AMF have also been found to influence lycopene content, antioxidant activity, and potassium content in tomato (Ordookhani et al., 2010).

Biotechnological Approaches Limited variation exists within the cultivated tomato for abiotic stress tolerance; however, several wild relatives of tomato, including L. chilense Dunal, L. hirsutum Humb. and Bonpl., S. peruvianum L., and S. pennellii Correll (Miller and Tanksley, 1990; Breto et al., 1993) have been found to be good sources of abiotic stress tolerance, which can be exploited in breeding programs for introgression of abiotic stress tolerance into cultivated tomato (Foolad, 2007). In 4

addition, advances in plant genetic transformation techniques have facilitated progress in the identification of genes, enzymes, or compounds contributing to plant tolerance to various abiotic stresses. Genetic engineering approaches for developing abiotic stress tolerant tomatoes are considered to be an attractive alternative to conventional breeding. Manipulating the production of such enzymes or compounds through transgenic approaches has resulted in the development of plants with enhanced abiotic stress tolerance in several plant species including tomato.

Factors Influencing Efficient Transformation in Tomato Toward the improvement of tomato through genetic engineering, reliable regeneration and transformation procedures are essential. Over the past two decades a number of techniques have been employed for the introduction of foreign DNA into plant cells of monocotyledon and dicotyledonous plants. For tomato, genetic transformation via Agrobacterium is certainly an important tool to facilitate genetic improvement along with other methods such as particle bombardment and Agro-infiltration. Since the first report of tomato transformation by McCormick et al. (1986), numerous publications on the transformation of various tomato genotypes have been reported (summarized in Table 1). In spite of numerous efforts to improve transformation efficiencies (Hamza and Chupeau, 1993; Hu and Phillips, 2001; Cortina and Culianez-Macia, 2004), advances in this area have been limited due to low efficiency and genotype dependency of in vitro plant regeneration of tomato. Many procedures have relied on cumbersome feeder layers (with petunia [Petunia × hybrida], tomato, or tobacco [Nicotiana tabacum L.]), time-consuming media formulations or successive subcultures, and no simplified procedure for tomato transformation exists. Therefore, development of an efficient and genotype-independent tomato regeneration and transformation method is crucial for tomato improvement. Transformation efficiency in tomato is influenced by many factors including cultivar (Hamza and Chupeau, 1993; Agharbaoui et al., 1995; Ellul et al., 2003;), explant type (McCormick et al., 1986; Fillati et al., 1987; Sigareva et al., 2004), explant age (Davis et al., 1991a; Hamza and Chupeau, 1993), phytohormones (McCormick et al., 1986; Pfitzner, 1998), bacterial contamination (Ling et al., 1998; Ieamkhang and Chatchawankanphanich, 2005) and Agrobacterium virulence gene inducers (Stachel et al., 1986). Regeneration and transformation studies have primarily been focused on tomato species S. lycopersicum (Abu-El-Heba et al., 2008; Hasan et al., 2008; Kaur and Bansal, 2010), studies have also been reported for other tomato species such as S. pennellii (van Eck et al., 1995), S. peruvianum (Hamza and Chupeau, 1993), and L. chilense (Agharbaoui et al., 1995). A range of explants have been used for developing transgenic plants in tomato including leaves (Agharbaoui et al., 1995),

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Table 1. Summary of research accomplishments toward the optimization of conditions for successful genetic transformation of tomato. Transformation system

Agrobacterium strains

Vectors and marker gene(s) used

Tissue type

Transformation efficiency/result

S. lycopersicum cultivars and F1 hybrids

Agrobacteriummediated

A. tumefaciens strain GV3111SE and A208 (host C58C1)

Ti plasmids pTi6S3SE and pTiT37SE(ASE) containing NPTII gene

Leaves, cotyledons & hypocotyls

Transgenic plantlets showed kanamycin resistance

McCormick et al., 1986

S. lycopersicum Red Cherry, Improved Pearson, UC-82, Heinz 2152, and ONT 7710 S. lycopersicum, L. hirsutum × S. lycopersicum (KNVF rootstock) and S. peruvianum


A. tumefaciens strain LBA4404; A. rhizogenes strain A4

Binary vector pARC8 containing NPTII gene

Cotyledons

Transgenic plantlets showed kanamycin resistance

Shahin et al., 1986


A4T (containing Ri plasmid vector pRiA4)

pAMNeo10 containing chimeric kanamycin resistance gene

Stem explants

Transformed roots and regenerated shoots showed kanamycin resistance

Morgan et al., 1987

S. lycopersicum (VF36) × S. pennellii (LA716)


A. tumefaciens strain C58C1

Binary vector pGV3850 containing NPTII gene

Stem internodes

Transformation frequency, 34%

Chyi and Phillips, 1987

S. lycopersicum Ohio 7870, UCD 82b, Roma


A. tumefaciens strains A6, A66, A281

Ti plasmids pTiA6, pTiA66 and pTiBo542

Cotyledons and leaves

Factors such as cultivar, leaf age, bacterial strain and concentration were optimized

Davis et al., 1991a

S. lycopersicum Ohio 7870


A. tumefaciens strain A281

Ti plasmid producing agropine

Cotyledons

Acetosyringone and tomato wound-inducible factor enhanced the transformation frequency

Davis et al., 1991b

S. lycopersicum Mill. Ailsa Craig


A. tumefaciens strain C58C1

Binary vector pGSFR1161 containing NPTII gene

Cotyledons and hypocotyls

Acetosyringone enhanced the transformation process

Katia et al., 1993

S. lycopersicum Moneymaker


A. tumefaciens strains MOG101, MOG301, EHA105

Binary vectors pMOG410 (GUS), pMOG539, pMOG549, pMOG609 containing NPTII gene

Cotyledons

Average transformation frequency, ~9%

van Roekel et al., 1993

S. lycopersicum UC82B, Monalbo, Castone, Ferline and S. peruvianum CMV sel. INRA


ND†

Binary vector p35SGUSINT containing NPTII and GUS genes

Cotyledons

Transformation frequency, 8% (Monalbo) and 14% (UC82B)

Hamza and Chupeau, 1993

S. lycopersicum VFNT cherry and S. pennellii

Particle bombardment

ND

Cell Plasmids pBI121, pBI410, pBI426, and pCOR2410T-31 suspensions carrying Yeast Artificial Chromosome (YAC) and NPTII and GUS genes

Stable transformation revealed by GUS expression and kanamycin resistant calli

van Eck et al., 1995

L. chilense LA1930 and LA2747


A. tumefaciens strain LBA4404

Binary vector pBin 19 containing NPTII gene

Leaf discs

Agharbaoui et al., 1995







Binary vector pBI21 containing NPTII and GUS genes Transformation vector SLJ 44024 containing NPTII gene

Cotyledons and hypocotyls Cotyledons

Transformation frequency, 56% (LA2747) and 25% (LA1930) Transformation frequency, 10.6% Superiority of ticarcillin/ potassium clavulanate for removing Agrobacterium contamination and enhancing transformation

Ling et al., 1998

S. lycopersicum UC82


A. tumefaciens C58C1 (pGV2260)

Binary vector pBI121 containing NPTII and GUS genes

Cotyledons


Hu and Phillips, 2001



A. tumefaciens strains LBA4404, UIA143, MOG101 and GV3101

Ti plasmids pAL4404, pMOG101, pMP90, pMOG101

Cotyledons and hypocotyls

Frary and Hamilton, 2001

S. lycopersicum Micro-Tom, Red Cherry, Rubion, Piedmont, and E6203




Leaves, cotyledons and hypocotyls

Agrobacterium strains with virG and virG + virE helper plasmids effected the most efficient transfer of 150 kb of human gDNA Transformation efficiency, >20%


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Reference

Frary and Earle, 1996

Park et al., 2003

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Cultivar(s)/ accession

Table 1. Continued.


Cultivar(s)/ accession

Transformation system

Agrobacterium strains

Vectors and marker gene(s) used

Tissue type

Transformation efficiency/result

Reference

S. lycopersicum p73, UC82b and inbred lines LP0, LP2, and LP4



Modified pBin 19 vectors harboring HAL3, TAS14, and pVDH303 containing NPTII and GUS genes

Cotyledons

Transformation efficiency ranged from 1.8 to 11.3%

Ellul et al., 2003

S. lycopersicum (elite lines SG048, 00-5223-1, and 00-0498-B)



Binary vectors pNOV2147 and pNOV7100 with PMI gene

Cotyledons petioles, hypocotyls, and leaves

Transformation frequencies ranged from 2.0 to 15.5%

Sigareva et al., 2004

S. lycopersicum Momotaro, UC-97 and Edkawi


A. rhizogenes strain DCAR-2


Hypocotyls

Regenerated hairy roots at a frequency of 54 to 67%

Moghaieb et al., 2004

S. lycopersicum UC82B



Cotyledons

Transformation frequency, 12.5%

S. lycopersicum VF 134-1-2


A. tumefaciens strain AGL1

Binary vector pBIN19 containing NPTII gene Binary vector pCambia2311 containing NPTII gene

S. lycopersicum Lichun



Binary vector pTOK233 with NPTII and GUS genes

Cotyledons, hypocotyls

Transgenic shoots showed resistance to kanamycin

Wu et al., 2006

S. lycopersicum Micro-Tom


A. tumefaciens C58C1

pIG121Hm containing NPTII and GUS genes

Cotyledons


Sun et al., 2006

S. lycopersicum Micro-Tom


A. tumefaciens strain EHA105

Binary vectors contained NPTII gene

Cotyledons

Maximum transformation frequency, 20.87%

Qiu et al., 2007

S. lycopersicum CastleRock

Agrobacteriummediated and biolistic gun method

A. tumefaciens LBA4404




S. lycopersicum

Agro-infiltration

S. lycopersicum Zhongshu No. 4

Cortina and CulianezMacia, 2004 Cotyledons Superiority of augmentin Ieamkhang over cefotaxime for and Chatcharemoving Agrobacterium wankancontamination with improved phanich, 2005 transformation

Plasmid pISV2678 Hypocotyls Transformation frequency, harboring bar and NPTII with part of 30% (Agrobacterium-medigenes; pMONRTG cotyledon ated) and 26.5% (Biolistic harboring the GUS gene gun method) (Biolistic gun method) Binary vector pCB3160 conModified Transformation frequency taining NPTII and cotyledonary ranged from 0.4 to 9.0% PMI genes leaves

Abu-El-Heba et al., 2008

A. tumefaciens strain EHA 105

pROKIIGUSINT AP1 carrying GUS and NPTII genes


A. tumefaciens |strain LBA4404

Binary vector pBI21 with NPTII and GUS genes

S. lycopersicum Rio Grande



S. lycopersicum Pusa Ruby, Sioux, Arka Vikas


S. lycopersicum Roma and Riogrande S. lycopersicum Mill. Pusa Ruby, Pusa Uphar, and DT-39

Fresh, healthy & mature fruits Cotyledons

Transformation frequency ranged from 54 to 68.0%

Hasan et al., 2008

Transformation frequency, 44.7%

Gao et al., 2009

Binary vector pCB 302.2 harboring bar gene

Cotyledons, leaves

Transformation frequency ranged from 14 to 30%

Khoudi et al., 2009

A. tumefaciens strain AGL1

Binary vector pCTBE2L, pRINASE2L, pCTBE2L, pCTBE2L

Cotyledons

Transformation frequency ranged from 41.4%

Sharma et al., 2009


A. tumefaciens strain EHA101

Binary vector pTCL5 containing HPT and GUS gene

Hypocotyls & leaf disks

Transformation efficiency, 24% (Riogrande) and 8% (Roma)

Chaudhry and Rashid, 2010


A. tumefaciens strain GV3101

Binary vector pBI101 containing NPTII gene

Cotyledons

Transformation frequency, >37%

Kaur and Bansal, 2010

cotyledons (Shahin et al., 1986; Davis et al., 1991a; Cortina and Culianez-Macia, 2004; Kaur and Bansal, 2010), hypocotyls (Moghaieb et al., 2004), petioles (Sigareva et al., 2004), and internodes (Chyi and Phillips, 1987). Among them, cotyledons have been frequently used because of the availability of seeds, reproducibility of sterilization and germination conditions, and the possibility of controlling the developmental stage (Sigareva et al., 2004). Agrobacterium-mediated transformation methods have been used in almost all cases except for a couple of instances (van Eck et al., 1995; Abu-ElHeba et al., 2008). Van Eck et al. (1995) used cell suspensions 6

Briza et al., 2008

of S. lycopersicum cv. VFNT Cherry and S. pennellii for developing transgenic tissues using particle bombardment. However, stable transformation efficiency was found to be higher in Agrobacterium-mediated transformation as compared with particle bombardment (Abu-El-Heba et al., 2008). Recently, Hasan et al. (2008) reported a novel Agro-infiltration method for transformation of tomato fruits and found a high transformation efficiency of 54 to 68% in seeds as confirmed by b-glucuronidase (GUS) expression and germination on kanamycin medium. Agrobacterium rhizogenes has also been used to transform of tomato through the generation of hairy

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Genetic Engineering Approaches Recently, transgenic approaches have been employed to produce plants with enhanced tolerance to various abiotic stresses by overexpressing genes involved in different tolerance-related physiological mechanisms (Zhang et al., 2005; Park et al., 2006; Zhou et al., 2007; Cheng et al., 2009). These include genes encoding enzymes in the synthesis of solutes such as mannitol (Thomas et al., 1995), GB ( Jia et al., 2002; Zhou et al., 2007), and polyamines (Cheng et al., 2009), which contribute to osmoregulation and impart tolerance to abiotic stresses. Transgenic tomato plants have been produced that express different vacuolar crop science, vol. 51, september– october 2011

antiport proteins that facilitate exclusion of toxic ions from the cell cytosol (Zhang and Blumwald, 2001) and detoxification enzymes that reduce oxidative stress (Wang et al., 2006). Transgenic tomato plants overexpressing these genes were reported to grow, flower, and produce fruits in stress conditions, whereas the control plants did not survive. A survey of transformation studies aimed to manipulate the expression of various genes conferring tolerance to abiotic stresses in tomato is listed in Table 2.

Genes Encoding Functional and Structural Proteins Polyamines Polyamines are small ubiquitous compounds that have been implicated in the regulation of many physiological processes and a variety of stress responses in plants (Bouchereau et al., 1999; Yang et al., 2007). The polyamines spermidine, spermine, and putrescine accumulate under abiotic stress conditions, and their enhanced levels play an important role in the protective response of plants to different abiotic stresses (Rajam et al., 1998; Kumar et al., 2006). The polyamines play a key role in osmotic adjustment, membrane stability, free-radical scavenging, and regulation of stomatal opening (Liu et al., 2007). Reports also suggest the interaction of polyamines with ABA, ROS, nitric oxide, Ca2+ homeostasis, and ion channel signaling during abiotic stress response in plants (Alcázar et al., 2010). Overexpression of yeast S-adenosylmethionine decarboxylase in tomato resulted in enhanced accumulation of polyamines in transgenic plants that showed enhanced tolerance to high temperature stress (Cheng et al., 2009). The increase in polyamine levels was associated with enhanced activities of antioxidant enzymes and protection of membrane from lipid peroxidation. Glycine Betaine Glycine betaine is a quaternary ammonium compound that occurs naturally in a wide variety of plants, animals, and microorganisms (Rhodes and Hanson, 1993). Betaine regulates osmotic pressure and protects enzyme activities (Rhodes and Hanson, 1993). Elevated levels of GB were observed in many plant species in response to abiotic stresses (Rhodes and Hanson, 1993). Proposed roles for GB include stabilizing complex proteins and membranes, protecting transcriptional and translational machineries, and intervening as a molecular chaperone in the refolding of enzymes (reviewed in Sakamoto and Murata, 2000; Chen and Murata, 2002). In addition, GB may indirectly induce H2O2–mediated signaling pathways such as enhanced catalase activity (Park et al., 2006). Its amount and localization in different subcellular compartments determine the extent of plant tolerance to various abiotic stresses. The role of GB in tomato tolerance to drought, salinity, and cold has been well established by foliar application of GB to tomato plants (Mäkelä et al., 1998, 1999; Park et al., 2006).

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roots (Moghaieb et al., 2004) and subsequently regeneration of transgenic plants from hairy roots (Shahin et al., 1986). Most initial transformation studies in tomato used neomycin phosphotransferase (NPT II conferring resistance to kanamycin) and GUS as reporter genes to establish adequate protocols (Table 1). In later studies, other genes such as hygromycin phosphotransferase (HPT) gene (Chaudhry and Rashid, 2010), bialaphos resistance (bar) gene (Abu-El-Heba et al., 2008; Khoudi et al., 2009), and phosphomannose isomerase (pmi) gene (Briza et al., 2008) have also been used for optimizing transformation in tomato. For removal of Agrobacterium contamination during subculture of transgenic tissues and shoots, cefotaxime has been most commonly used, although it has also been reported that ticarcillin/ potassium clavulanate was superior for removing Agrobacterium contamination and enhancing transformation (Ling et al., 1998). In another study, augmentin was found superior to cefotaxime and timentin for removing Agrobacterium contamination and improving transformation efficiency (Ieamkhang and Chatchawankanphanich, 2005). Efficiency of binary bacterial artificial chromosome (BIBAC) vectors for Agrobacterium-mediated stable transfer of high molecular weight DNA into tomato plants was found to be positively influenced by the presence of additional copies of virG, virE1, and virE2 genes (Frary and Hamilton, 2001). In addition, the presence of a helper plasmid containing extra copies of virG was obligatory for obtaining tomato transformants with the BIBAC. This method was found to be the most efficient for transfer of high molecular weight DNA (150 kb) into the plant genome. Addition of acetosyringone to the co-cultivation media has been reported to increase the transformation frequency in tomato (Katia et al., 1993; Cortina and Culianez-Macia, 2004; Chaudhry and Rashid, 2010). Davis et al. (1991b) reported enhanced transformation efficiency in tomato with the addition of acetosyringone and a tomato woundinducible factor. Alternatively, feeder cells from species like tobacco (Fillati et al., 1987; Hamza and Chupeau, 1993; Frary and Earle, 1996), tomato (Agharbaoui et al., 1995), and petunia (van Roekel et al., 1993) have also been used for improving the efficiency of transformation of tomato.

Table 2. List of accomplishments for genetic engineering of tomato toward abiotic stress tolerance. Gene


S-adenosyl-l-methionine decarboxylase (SAMDC) Betaine aldehyde dehydrogenase (BADH)

Gene function

Gene source

Transgenic performance

Genes encoding functional and structural proteins Polyamines biosynthesis Yeast Tolerance to high temperature stress Glycine betaine accumulation Sorghum, Arabidopsis Maintenance of osmotic hortensis potential under cold and salt stress Glycine betaine accumulation Enhanced synthesis of trehalose Glutathione biosynthesis

Arthrobacter globiformis Yeast

Imparted chilling tolerance Imparted drought tolerance

Mus musculus

Imparted chilling tolerance

Mannitol synthesis

Escherichia coli

Osmotin accumulation

Tobacco

Omega-3 fatty acid desaturase (LeFAD3) LeFAD3

Increased level of 18:3 fatty acid Increased degree of fatty acid saturation

Tomato

Enhanced tolerance to chilling, drought and salinity stresses Tolerance to salt and drought stress Enhanced tolerance to chilling stress Alleviated photoinhibition of photosystem (PS)II and enhanced tolerance to heat stress

Fatty acid desaturase (FAD3, FAD7)

Altered ratio of 18:3/18:2 in leaves and fruits

Brassica napus (FAD3), Solanum tuberosum (FAD7)

Choline oxidase (codA) Trehalose-6-phosphate synthase (TPS1) Glutathione peroxidase (GPX) Mannitol-1-phosphate dehydrogenase (mt1D) Osmotin

1-aminocyclo-propane-1carboxylate (ACC) deaminase Yeast HAL1 Yeast HAL2 Vacuolar Na+/H+ antiport Aquaporin (NtAQP1)

Ascorbate peroxidase (APX) Catalase (katE)

Superoxide dismutases (FeSOD) Polyphenol oxidase (PPO)

Heat shock protein (HSP) Endoplasmic reticulum small heat shock protein (ER-sHSP) ABA responsive element binding protein (SlAREB) ABRE binding factor (ABF4) Capsicum annuum pathogeninduced factor 1 (CAP1F1) CBF1 gene

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Tomato

Enhanced tolerance to chilling stress

Genes regulating phytohormone levels Reduced ethylene Soil bacterium Enterobacter Tolerance to water logging biosynthesis cloacae UW4 Genes encoding ion transport proteins (halotolerant genes) Yeast Enhanced salt tolerance Altered Na+ and K+ homeostasis Altered Na+ and Yeast Enhanced salt tolerance K+ homeostasis Enhanced Na+ Arabidopsis Imparted salt tolerance accumulation in leaves Role in plant water Tobacco Enhanced salt tolerance balance Genes encoding enzymes in antioxidant system Pea Resistance to heat (40°C) and Detoxification of H2O2 UV-B stress Degradation of H2O2 to E. coli Tolerance to the photowater and oxygen oxidative stresses imposed by drought and chilling stress Dismutation of superoxide Arabidopsis Tolerance to salt stress radicals to H2O2 and oxygen Potato Increased water stress Photoreduction of O2 by PSI tolerance Molecular chaperones (heat shock proteins) Temperature-responsive Arabidopsis Tolerance to extreme stress mechanism temperatures Temperature-responsive Tomato Enhanced tolerance to tunicastress mechanism mycin-induced ER stress Regulatory genes controlling stress tolerance Regulation of stress-related Tomato Increased tolerance to genes water deficit and salinity ABRE-binding factor Arabidopsis Drought tolerance Transcription of stressrelated gene Expression of COR genes

Pepper Arabidopsis

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Enhanced tolerance to cold stress Resistance to water deficit

References Cheng et al., 2009 Moghaieb et al., 2000; Jia et al., 2002; Zhou et al., 2007 Park et al., 2004 Cortina and Culianez-Macia, 2005 Herbette et al., 2005 Khare et al., 2010 Goel et al., 2010 Yu et al., 2009 Wang et al. (2010).

Domínguez et al., 2010

Grichko and Glick, 2001

Gisbert et al., 2000 Arrillaga et al., 1998 Zhang and Blumwald, 2001 Sade et al., 2010

Wang et al., 2006 Mohamed et al., 2003

Serenko et al., 2009 Thipyapong et al., 2004

Lurie, 1998 Zhao et al., 2007

Hsieh et al., 2010 Na, 2005 Seong et al., 2007 Hsieh et al., 2002; Lee et al., 2003


Table 2. Continued. Rice Osmyb4 gene Ankyrin repeat domain zinc finger (CaKR1) Type I inositol 5 polyphosphatase (5PTse)

Gene function

Gene source

Transcription of stressrelated gene Influence antioxidant system

Transgenic performance

Rice Pepper

Involved in inositol 1,4,5 trisphosphate (IP3) signaling

Tomato

SlERF3ΔRD

Ethylene-responsive transcription factor deleted amphiphilic repression domain

Tomato

SP1 (stable protein 1)

Thermostable homooligomeric protein Regulation of cell expansion

Miscellaneous proteins Populus tremula Cucumber

Biosynthesis of systemin Anti-apoptotic proteins An inhibitor of apoptosis family protein

Tomato Human Spodoptera frugiperda

Cucumber expansin 1 (CsEXPA1) Prosystemin bcl-xL and ced-9 SfIAP (inhibitor of apoptosis)

In plants betaine is synthesized by two-step oxidation of choline by choline monooxygenase (Brouquisse et al., 1989) and subsequently by betaine aldehyde dehydrogenase (BADH) (Weigel et al., 1986). The simplicity of the betaine biosynthetic pathway has attracted the attention of molecular biologists for engineering plants for enhanced betaine accumulation as a strategy to enhance abiotic stress tolerance (Moghaieb et al., 2000; Jia et al., 2002; Park et al., 2004; Zhou et al., 2007). Expression of BADH in transgenic tomato hairy roots led to the accumulation of GB that contributed to the maintenance of high osmotic potential under salt stress (Moghaieb et al., 2000). Transgenic tomatoes with enhanced BADH activity showed elevated betaine content compared with the wild-type under stress conditions (Jia et al., 2002; Zhou et al., 2007). Similarly, transgenic tomato plants expressing a chloroplasttargeted Choline oxidase (codA) gene from Arthrobacter globiformis showed enhanced accumulation of GB in leaves (Park et al., 2004). Choline oxidase catalyzes the oxidation of choline to GB in transgenic tomato plants, and the accumulation of GB in chloroplasts of transgenics was positively correlated with the degree of chilling tolerance (Park et al., 2004). Further, these transgenic tomato plants showed enhanced tolerance to salt stress, which was attributed to the retention of chlorophyll and membrane integrity. Trehalose Trehalose is a disaccharide of glucose (a-d-glucopyranosyl-d-glucopyranoside) found to accumulate in many organisms including bacteria, yeast, and invertebrates under stressed conditions (Elbein, 1974). Trehalose acts as an osmolyte-compatible solute that protects membrane proteins and confers desiccation tolerance to cells (Crowe et al., 1984). It also stabilizes proteins in the native state and reduces the aggregation of denatured proteins (Singer crop science, vol. 51, september– october 2011

References

Enhanced tolerance to drought Resistance to salinity and oxidative stresses Drought tolerance

Vannini et al., 2007

Reduced levels of membrane lipid peroxidation and enhanced tolerance to salt stress

Pan et al., 2010

Tolerance to water stress

Roy et al., 2006

Tolerance to salt and ABA stress

Rochange et al., 2001

Tolerance to salt stress Enhanced tolerance to cold Tolerance to abiotic stresses, heat, and salinity

Orsini et al., 2010 Xu et al., 2004 Li et al., 2010

Seong et al., 2007 Na, 2005

and Lindquist, 1998). In Saccharomyces cerevisiae, trehalose accumulation has been correlated with thermo-tolerance (De Virgilio et al., 1994), resistance to cold and water stress (Mackenzie et al., 1988), and cell protection against oxygen radicals (Benaroudj et al., 2001). Transgenic tomato plants that expressed the trehalose-6-phosphate synthase (TPS1) gene from S. cerevisiae were found to be more drought tolerant than the wild-type plants, although the transgenic plants exhibited some undesirable pleiotropic changes in plant morphology (Cortina and Culianez-Macia, 2005). Glutathione Reduced glutathione (GSH) is the most abundant low molecular weight thiol compound in plants, having unique structural properties and a broad redox potential. It is synthesized from its constituent amino acids in an ATP-dependent, two-step reaction catalyzed by the enzymes Q-glutamylcysteine synthetase and GSH synthetase. Glutathione protects cells and tissues against a wide range of peroxides, xenobiotics, and heavy metals (May et al., 1998; Noctor et al., 1998). The level and redox state of the GSH pool in plants is altered by environmental factors and thereby plays a role in plant tolerance to environmental stress. The acclimation of GSH biosynthesis and GSH-utilizing enzymes to salt stress was studied in two tomato species differing in relative stress tolerance (Mittova et al., 2003). Salt-induced increase of lipid peroxidation and H2O2 was evident in S. lycopersicum mitochondria and coincided with reduced AsA and reduced GSH contents. In contrast, the mitochondria of salt-treated S. pennellii did not exhibit salt-induced oxidative stress, and the chloroplasts exhibited increased AsA and GSH contents under salt stress, which contributed to the enhanced tolerance of plants to salt stress (Mittova et al., 2003). Overexpression of a eukaryotic selenium-independent GSH peroxidase

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Gene


in transgenic tomato plants resulted in enhanced GPX activity and transgenic plants showed unaltered photosynthetic activity under chilling stress compared to wild-type plants (Herbette et al., 2005). Mannitol Mannitol is a sugar alcohol reported to play a role in osmoregulation of plants. Mannitol is synthesized from fructose in plants by the action of mannitol-1-phosphate dehydrogenase (mt1D). Constitutive overexpression of mt1D gene from Escherichia coli in transgenic tomato plants has been shown to confer enhanced tolerance to chilling, drought, and salinity stress (Khare et al., 2010). Transgenic tomato plants subjected to cold stress showed decreased electrolyte leakage and increased lipid peroxidation with a significant increase in the activities of antioxidant enzymes (catalase and superoxide dismutase). Osmotin Osmotin is a stress-responsive multifunctional 24-kDa protein that provides osmotolerance to plants. Osmotin is involved in osmotic adjustment of cells by facilitating the accumulation or compartmentalization of solutes (Barthakur et al., 2001). It is also known to protect the native structure of proteins during stress and repair denatured proteins. The overexpression of the tobacco osmotin gene in transgenic tomato resulted in increased plant tolerance to salt and drought stress (Goel et al., 2010). Transgenic tomatoes that overexpressed the osmotin gene exhibited significantly higher relative water content, chlorophyll content, proline content, and leaf expansion than wild-type plants under stress conditions. Fatty Acid Desaturases Changes in the degree of fatty acid desaturation are implicated in plant responses to various abiotic stresses such as heat, salt, and drought. However, it is still not clear whether decreased levels of linolenic acid found in many plants subjected to salt and drought stresses reflect a mechanism of defense to various biotic and abiotic stresses (Zhang et al., 2005). Overexpression of tomato omega-3 fatty acid desaturase (LeFAD3) gene led to increased tolerance of transgenic tomato plants to cold stress (Yu et al., 2009), which was attributed to increased levels of 18:3 fatty acid that alleviated injuries under chilling stress. Similarly, overexpression of omega-3-saturase in tomato resulted in increased fruit flavor and enhanced tolerance of tomato plants to chilling stress (Domínguez et al., 2010). In contrast to these studies, repression of LeFAD3 in transgenic tomato resulted in an increased degree of the saturation of fatty acids, alleviated photoinhibition of photosystem (PS)II and enhanced the tolerance to heat stress (Wang et al., 2010). These reports suggest that the differential behavior of transgenic plants overexpressing LeFAD3 may be due to fatty acid fluxes to ensure plant survival under adverse conditions. 10

Genes Regulating Phytohormone Levels Phytohormones constitute a large set of intracellular signal molecules that induce cell responses to various stresses. The most important among them are ethylene, SA, and ABA. These hormones are known to accumulate in higher levels under stress and influence the expression of many genes involved in defense mechanisms against biotic and abiotic stresses. Ethylene is produced under abiotic stresses such as flooding or water logging, and its production severely affects crop growth and yield by causing epinasty, chlorosis, and necrosis (Abeles et al., 1992). Increased ethylene production in flooded tomato plants is due to the induction of ACC synthase, a key enzyme in ethylene biosynthesis (Olson et al., 1995). Attempts were made to develop transgenic tomatoes overexpressing bacterial ACC deaminase, an enzyme that catalyzes the reversible conversion of ACC to 2-oxobutanoate and ammonia thus reducing the ethylene pool (Grichko and Glick, 2001). Transgenic tomato plants expressing ACC deaminase were characterized by a decreased level of ethylene under stress and enhanced tolerance to salt and water logging due to the degradation of ethylene by ACC deaminase (Grichko and Glick, 2001).

Genes Encoding Ion Transport Proteins (Halotolerant Genes) Halophytic plants grow under high salt conditions and display defense mechanisms against salt stress. The primary metabolic response to salt stress in these plants is the synthesis of compatible osmolytes, which mediate osmotic adjustment to protect subcellular structures and reduce oxidative damage caused by free radicals that are produced in response to high salinity (Hare et al., 1998). Based on mechanisms involved in plant adaptability to osmotic and ionic stresses in halotolerant plants, several strategies have been proposed to improve salt tolerance in sensitive plants. These include the overproduction of osmolytes to balance osmotic adjustment, modification of processes involved in free radical scavenging, and modification of transport systems of Na+ and Cl- in the vacuolar and plasma membranes (Serrano and Gaxiola, 1994; Bohnert and Jensen, 1996). Preservation of ion homeostasis in plant cells is one of the key points in plant tolerance to elevated levels of soil salinity. The maintenance of ion homeostasis in plants suffering from salt stress is regulated by the operation of genes related to vacuolar Na+/H+ antiports (Apse et al., 1999) and stress signaling through Ca2+ or calmodulin-dependent protein phosphatase and calcineurin (Liu and Zhu, 1998; Pardo et al., 1998). Calcineurin is a Ca2+–activated protein phosphatase that modulates Na+ and K+ transport in yeast and ion homeostasis in tomato cells (Marin-Manzano et al., 2004). Transgenic tomato plants expressing a yeast HAL2 gene showed a higher level of root proliferation on NaCl-supplemented medium (Arrillaga et al., 1998). In another study, Gisbert et al. (2000) introduced the yeast halotolerant HAL1

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Aquaporin Aquaporins are integral membrane proteins that increase the permeability of membranes to water and other small molecules such as CO2, glycerol, and boron (Uehlein et al., 2003; Kaldenhoff and Fischer, 2006). Aquaporins function as both water and CO2 channels in plants (Kimball and Idso, 1983; Li et al., 2007) and play a key role in plant water balance and water use efficiency (Knepper, 1994; Maurel, 2007). Overexpressing a tobacco AQP gene NtAQP1 in tomato resulted in higher stomatal conductance, whole-plant transpiration, and leaf net photosynthesis under control and salt stress conditions (Sade et al., 2010). These results suggested that the increase in water use and leaf net photosynthesis under saline conditions resulted in improved water use efficiency contributing to stress tolerance in terms of fruit yields.

Genes Encoding Enzymes in Antioxidant System Plants under abiotic stresses produce ROS in cells, which are associated with a number of physiological disorders in plants (Allen, 1995) such as lipid peroxidation, DNA mutation, and protein denaturation (Bowler et al., 1992; Scandalios, 1993; Apel and Hirt, 2004). Efficient removal of ROS is critical because trace quantities of H2O2 can inhibit CO2 fixation in chloroplasts (Kaiser, 1979; Takeda et al., 1995) due to the oxidation of several thiol-modulated enzymes. Plants have evolved efficient nonenzymatic and enzymatic mechanisms to cope with these ROS. Nonenzymatic systems such as ascorbate, GSH, a-tocopherol, and carotenoids can interact directly with ROS, while enzymatic systems involving ascorbate peroxidase (APX), superoxide dismutase (SOD), and GSH reductase scavenge ROS and maintain normal plant growth (Allen, 1995). The role of ascorbate in enhancing salt stress was crop science, vol. 51, september– october 2011

suggested by treatment of tomato and potato plants with ascorbic acid (Park et al., 2006; Sajid and Aftab, 2009). Ascorbate treatment enhanced the expression of ROSscavenging enzymes, peroxidase, catalase, and SOD. In addition, enhanced production of ascorbate in transgenic potato resulted in increased tolerance to oxidative stress caused by methyl viologen, salt, and water deficit (Hemavathi et al., 2009, 2010a, 2010b). Genes encoding enzymes with antioxidant activity such as peroxidase, catalase, and SOD have also been expressed in transgenic plants, which showed improved plant protection against oxidative and other stresses (Bowler et al., 1991; Sen Gupta et al., 1993; Bajaj et al., 1999). Major antioxidant genes that have been utilized for the improvement of tomato via a genetic engineering approach are summarized in following sections. Ascorbate Peroxidase Ascorbate peroxidase (EC 1:11:1:11) detoxifies H2O2 using ascorbate as a substrate. This catalyzes the transfer of electrons from ascorbate to H2O2 to form dehydroascorbate and water. The tomato cell wall peroxidase gene (TPX1) showed differential expression between salt-adapted and unadapted cells with respect to post-transcriptional processing and its sensitivity to external NaCl (Medina et al., 1999). These results indicated that the TPX1 gene product may be involved in the salt adaptation process, cell wall cross-linking, or the synthesis of lignin, the content of which was higher in the salt-adapted cells (Sancho et al., 1996). Transgenic tomato plants overexpressing the pea APX gene showed enhanced resistance to heat (40°C) and UV-B stress compared to wildtype plants (Wang et al., 2006). The increased APX activity in transgenic plants under heat, UV-B, and drought stresses coincided with increased generation of ROS. Catalase Catalase (EC 1.11.1.6) decomposes H 2O2 to water and oxygen. It is capable of scavenging large quantities of H 2O2 due to its very high reaction rate, but its location in microbodies limits its ability to quench H2O2. Overexpression of the E. coli kat E gene, which encodes a catalase having higher affinity for H 2O2 than plant catalase, in chloroplasts of transgenic tomato plants resulted in enhanced tolerance to oxidative stress caused by the herbicide paraquat (1,1¢-dimethyl-4,4¢-bipyridinium; Mohamed et al., 2003). In addition, transgenic plants showed increased tolerance to oxidative damage (decrease of CO2 fixation and photosystem II activity and increase of lipid peroxidation) caused by drought or chilling stress (4°C) under high light intensity (1000 μ mol m-2 s-1). Superoxide Dismutases Superoxide dismutases are metalloproteins that catalyze the conversion of superoxide radicals to H2O2 and oxygen. The superoxide radical is a potential precursor of a highly

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gene in tomato and attributed the increased salt tolerance in transgenic lines to alterations in Na+ and K+ homeostasis. Measurement of the intracellular K+ to Na+ ratios showed that transgenic tomato lines were able to retain more K+ than control plants under salt stress. These results suggested a positive effect of the yeast HAL genes on the level of salt tolerance in transgenic tomatoes. Similarly, transgenic tomato plants overexpressing a vacuolar Na+/H+ antiport were able to grow, flower, and produce fruits in presence of 200 mM NaCl (Zhang and Blumwald, 2001). Leaves of the transgenic plants accumulated high Na+ concentrations, but fruits displayed very low sodium. Transgenic tomato cells expressing a yeast calcineurin gene exhibited increased tolerance to salinity (Marin-Manzano et al., 2004). Transgenic cells showed reduced activity of plasma membrane H+-ATPase and contained higher levels of Ca2+ and K+, indicating a role of calcineurin in modulating ion homeostasis in plants by affecting the activity of primary ion transporters.


oxidizing hydroxyl radical and, therefore, SODs are a critical defense mechanism of plants (Bowler et al., 1992). The predominant forms of SOD are mitochondrial MnSOD, cytosolic Cu/ZnSOD, and chloroplastic Cu/ZnSOD and FeSOD (Bowler et al., 1994). Owing to their important role in oxidative stress, the genes have been expressed in transgenic plants to impart resistance to abiotic stresses. Serenko et al. (2009) produced transgenic tomato plants overexpressing FeSOD that showed differential membrane integrity and cell wall organelles compared to control plants exposed to sodium sulfate, suggesting the utility of this gene for improving salt stress tolerance. Polyphenol Oxidases Polyphenol oxidases (PPOs; EC 1.14.18.1 or EC 1.10.3.2) catalyze O2–dependent oxidation of mono and o-diphenols to o-diquinones. o-Diquinones are highly reactive intermediates whose secondary reactions are believed to be responsible for oxidative browning associated with plant senescence, wounding, and responses to pathogens (Mayer and Harel, 1991; Friedman, 1997). Apart from biotic stresses, PPO activity was shown to be induced under water stress in tomato (Thipyapong et al., 2004). Polyphenol oxidases function in the Mehler reaction for photoreduction of molecular oxygen by PSI, and under drought stress with reduced photosynthesis the Mehler reaction may provide a nondestructive sink for absorbed light energy not used in photochemistry (Biehler and Fock, 1996). This suggests that water-stressed plants with suppressed PPO would be expected to exhibit photooxidative damage, while plants with elevated PPO may show increased stress tolerance. However, experiments by Thipyapong et al. (2004) found that suppression of PPO activity increased water stress tolerance in transgenic tomato plants. Their studies further suggested a role of PPO in the development of plant tolerance to water stress and photo-oxidative damage unrelated to effects of the Mehler reaction.

Molecular Chaperones (Heat Shock Proteins) Plants respond to high temperatures through production of heat shock proteins (HSPs) to defend against adverse temperatures. Heat shock proteins belong to a chemical group named “chaperones” and are involved in cellular response to heat, cold, heavy metals, and oxidative stresses (Swindell et al., 2007). They are also involved in temperature-perception mechanisms coupled with multiple signal transduction pathways (Larkindale et al., 2005). These HSPs create conditions for correct conformational folding of essential proteins that are partly denatured under high temperature conditions (Neumann et al., 1989). A tomato HSP (Lehsp23.8) promoter region showed enhanced activity when plants were treated with heat, low temperature, heavy metal, or exogenous ABA, indicating its role in abiotic stress responses (Yi et al., 2006; Yi and Liu, 2009). Transgenic tomato fruits expressing the Arabidopsis HSP gene hsf showed increased tolerance to high 12

(47°C) and low (−2°C) temperatures during 4 wk of storage (Lurie, 1998). The endoplasmic reticulum (ER) is the site of the assembly of polypeptide chains destined for secretion or routing into various subcellular compartments. A variety of stress conditions including treatment with tunicamycin cause aberrant folding of newly synthesized polypeptides, leading to the accumulation of unfolded proteins in the ER referred to as ER stress (Pelham, 1989). Overexpression of a tomato putative ER small HSP (ER-sHSP) gene in tomato led to enhanced tolerance to tunicamycin-induced ER stress (Zhao et al., 2007).

Regulatory Genes for Abiotic Stress Tolerance During plant response to abiotic stress, regulatory genes play an important role by participating in the generation of molecules such as plant hormones, ABA, ethylene, and SA. These regulatory molecules modulate secondary messengers that initiate protein phosphorylation cascades that ultimately target proteins involved in cellular protection or transcription factors controlling stress-regulated genes (Xiong et al., 2002). Transcription Factors Transcription factors are key regulatory proteins in the terminal steps of signal transduction cascades activated in response to stress. Several transcription factors as well as target cis-acting elements involved in stress-responsive gene regulation have been identified (reviewed in Shinozaki and Yamaguchi-Shinozaki, 2007). Many of these regulatory signals are controlled by ABA, which participates in the adaptation of plant species to drought and salinity (Verslues and Zhu, 2005). In addition, ABA also induces the expression of several genes with roles in dehydration tolerance in plant tissues. The promoters of these genes share regulatory sequences that are recognized by trans-acting factors, among which, the ABRE has been identified as the major cis-acting regulatory element in ABA-dependent gene expression (Shinozaki and Yamaguchi-Shinozaki, 2007). The ABRE is recognized by a specific group of bZIP transcription factors known as ABA-response element binding factors (AREBs) (Uno et al., 2000) or ABFs (Choi et al., 2000). So far, involvement of this class of transcription factors in ABA-mediated stress signaling has been described in Arabidopsis (Kang et al., 2002; Oh et al., 2005), rice (Oryza sativa L.; Hobo et al., 1999; Lu et al., 2009), wheat (Triticum aestivum L.; Kobayashi et al., 2008), and barley (Hordeum vulgare L.; Casaretto and Ho, 2003). The cDNA encoding a bZIP was isolated from cultivated and wild species of tomato, and its expression was reported to be induced by ABA and different abiotic stresses including salinity, drought, and cold (Yanez et al., 2009). Expression of a cDNA clone of tomato bZIP (SlAREB1) in tobacco and tomato was shown to regulate the transcription of stress-responsive genes such as RD29B, LEA

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of the Myb4 transcription factor represents a promising approach to improve stress tolerance in crops. Transgenic tomato plants expressing pepper CaKR1 encoding an ankyrin repeat domain zinc finger showed lower production of free oxygen radicals, such as superoxide and H2O2, and enhanced resistance to salinity and oxidative stresses (Seong et al., 2007). In addition, transgenic plants produced higher levels of pathogenesis-related (PR) proteins LePR1, LePR2, and LePR3, as well as oxidative stress response proteins, superoxide dismutase (LeSOD2), and ascorbate peroxidase (LeAPX2 and LeAPX3), suggesting CaKR1 is a key signaling molecule for plant antioxidant metabolism and defense responses (Seong et al., 2007). Recently, Pan et al. (2010) reported that overexpression in transgenic tomato of an ethylene-responsive transcription factors (ERFs) having deletions in the ERF-associated amphiphilic repression domain (SlERF3ΔRD) led to reduced levels of membrane lipid peroxidation and enhanced tolerance to salt stress. In comparison with wild-type plants grown under stress conditions, transgenic SlERF3DRD tomatoes also produced more flowers, fruits, and seeds.

Miscellaneous Proteins

Hydrophilic Boiling-Resistant Protein Apart from the proteins mentioned in earlier sections, plants synthesize certain proteins that can activate specific enzymes involved in plant defense against stresses. One such protein is the hydrophilic boiling-resistant BspA protein in aspen (Populus tremula L.), which is synthesized under drought stress and by ABA induction. These boiling-tolerant proteins are involved in plant tolerance to different stresses through protecting cell membrane and cytoplasmic proteins (Wang et al., 2002, 2003). Transgenic tomato plants (‘Pusa Ruby’) expressing BspA gene from P. tremula showed enhanced tolerance to drought stress (Roy et al., 2006). Expansins Expansins are a group of proteins that appear to be involved in the disruption of noncovalent bonds within the cell wall. Distinctly expressed expansin genes can independently regulate cell expansion in place and time, and their diverse expression patterns suggest their distinct effects on plant growth (Gao et al., 2010). Bioassays showed that stomatal opening induced by light and K+, and stomatal closure induced by Ca2+, ABA, and darkness were promoted by overexpression of AtEXPA1 in transgenic tobacco (Zhao et al., 2006). Similarly, a high level of cucumber (Cucumis sativus L.) CsEXPA1 activity in transgenic tomatoes resulted in stunted growth with shorter leaves and internodes (Rochange et al., 2001). The CsEXPA1-overexpressing tomato plants showed reduced impairment under salt and ABA stresses. These results suggested that expansins affect cell wall organization under stress conditions and help plants adapt to adverse environments.

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genes ERD10B and TAS14, transcription factor PHI-2, and a trehalose-6-phosphate phosphatase gene (Yanez et al., 2009). These results also suggested that this class of bZIP plays a role in abiotic stress response in the Solanum genus. Another water stress–inducible gene, Asr2 (named after ABA, stress, ripening), encoding a putative transcriptional factor was found to be up-regulated in leaves and roots of tomato plants exposed to water-deficit stress (Frankel et al., 2003). In another study, Na (2005) investigated the possibility of developing drought-tolerant tomatoes by a transgenic approach using an ABRE-binding factor, ABF4, from Arabidopsis. Transgenic tomato plants expressing the Arabidopsis ABF4/AREB2 gene exhibited higher drought tolerance, which was attributed to decreased water loss per unit leaf area. Recently, Hsieh et al. (2010) overexpressed a tomato ABA-responsive element binding protein (SlAREB) in tomato and observed increased tolerance to water deficit and salinity. Overproduction of SlAREB in transgenic tomato plants regulated stress-related genes AtRD29A, AtCOR47, and SlCI7-like dehydrin under ABA and abiotic stress treatments. Expression of transcriptional factor DREB1A (dehydration response element binding factors) led to strong constitutive expression of stress-inducible genes that enhanced tolerance to salt and water stress in Arabidopsis and tomato (Liu and Zhu, 1998; Nakashima and Yamaguchi-Shinozaki, 2006). Transgenic tomato plants expressing the pepper CAP1F1 (Capsicum annuum pathogen-induced factor 1) gene exhibited enhanced tolerance to cold stress that correlated with enhanced level of CAP1F1 gene expression (Seong et al., 2007). Overexpression of the CBF1 (CSL family of DNA binding protein) gene induced expression of COR (cold-regulated) genes and increased freezing tolerance in Arabidopsis (Jaglo-Ottosen et al., 1998) and in Brassica napus, suggesting that the function of CBF1 may be highly conserved in plants (Jaglo et al., 2001). The existence of a CBF1-like expressed sequence tag in tomato (Jaglo et al., 2001) suggests that a pathway may exist in tomato that is similar to that of Arabidopsis. Transgenic tomato plants overexpressing CBF1 were found to be more resistant to water deficit than wildtype plants (Hsieh et al., 2002). However, transgenic tomato plants exhibited growth retardation with reduced fruit, seed number, and fresh weight. Also, transgenic tomato plants contained higher levels of proline than wild-type plants under normal or water deficit conditions. Similarly, Lee et al. (2003) expressed Arabidopsis CBF1 under the control of the barley stress-inducible ABRC1 promoter in tomato and found increased tolerance to chilling, water deficit, and salt stress when compared with untransformed control plants. These transgenic plants demonstrated normal growth and development under stress conditions. Tomato plants overexpressing the rice Osmyb4 gene coding for MYB transcriptional factor showed enhanced tolerance to drought stress and viral diseases (Vannini et al., 2007). This study suggests that heterologous expression


Systemins Systemins are the initial peptide signals found in plants involved in intracellular signaling of biotic stress tolerance (Pearce et al., 1991). A key role for systemin in systemic signaling was established in tomato plants expressing an antisense prosystemin gene, which showed malfunction of long-distance wound signaling and susceptibility to insect attacks (Orozco-Cárdenas et al., 1993). Evidence also indicates involvement of the signal peptide systemin, coupled with JA, in wound-induced salt-stress adaptation in tomato (Capiati et al., 2006). Overexpression of prosystemin, a precursor of systemin in transgenic tomato plants, caused a reduction in stomatal conductance (Orsini et al., 2010). However, transgenic tomato plants maintained a higher stomatal conductance in response to salt stress compared with wild-type control plants. Leaf concentrations of ABA and proline were lower in stressed transgenic plants expressing prosystemin compared with wild-type control plants. Under salt stress the transgenic plants also produced more biomass than untransformed control plants. Anti-Apoptotic Genes Apoptosis is a type of programmed cell death with specific biochemical characteristics. It involves cascades of capsases and Bcl-2 family members for execution and regulation of apoptosis (Steller, 1995). Bcl-xL is an anti-apoptotic member of the Bcl-2 family of proteins implicated in pivotal decision points regarding cell survival in animals (Schendel et al., 1998). Overexpression of bcl-xL extends cell survival against apoptotic signals induced by a variety of stress treatments including viral infection, UV and γ-radiation, heat shock, and agents that promote formation of free radicals. Transgenic tomato plants expressing animal anti-apoptotic genes bcl-xL and ced-9 showed enhanced tolerance to cold, and cold-induced cell death was prevented by inhibition of programmed cell death under low temperature (Xu et al., 2004). Expression of bcl-xL and ced-9 successfully abrogated low temperature–associated necrotic lesion formation. Under cold treatment at 7°C, premature senescence was dramatically delayed and anthocyanins accumulated to high levels in transgenic tomato plants. Accumulation of anthocyanins in leaves of transgenic tomato plants at low temperature protected plants from ROS damage and enhanced cell survival (Xu et al., 2004). Expression of Spodoptera frugiperda (J.E. Smith) SfIAP, an inhibitor of apoptosis family protein, in transgenic tomato conferred tolerance to abiotic stresses such as heat and salinity (Li et al., 2010). Expression of SfIAP in transgenic tomato plants also inhibited abiotic stress–induced DNA fragmentation and formation of apoptotic-like bodies before cell death.

Other Proteins That Have a Potential Role in Abiotic Stress Tolerance Protein kinases are enzymes that modify other proteins by chemically adding phosphate groups to them 14

(phosphorylation). Phosphorylation usually results in a functional change of the target protein by changing the target enzyme activity, cellular location, or association with other proteins. Calcium-dependent protein kinases (CDPKs) are serine/threonine protein kinases with a C-terminal calmodulin-like domain with up to four EF motifs that directly bind Ca2+. Calcium-dependent protein kinases from many species have been shown to be involved in stress responses such as cold, drought, salinity, and osmotic stress (Cheng et al., 2002; Sanchez-Barrena et al., 2005) and the expression of AtCDPK1 and AtCDPK2 in Arabidopsis greatly increased under the drought and salinity stresses (Urao et al., 1994). A novel isoform of CDPK from tomato, LeCRK1, was isolated from tomato fruit cDNA, and its expression was found to be induced by ethylene, SA, mechanical wounding, and cold treatment (Leclercq et al., 2005). Another group of protein kinases, mitogen-activated protein kinases (MAPKs), mediate the phosphorylation of serine/threonine residues of specific proteins within the cells. Under multiple stresses like salinity, drought, heat, wounding, and osmotic shock, the MAPK cascade is activated in plants (Zhu, 2002), suggesting its involvement in plant tolerance to abiotic stress. The manipulating of expression of these kinases in transgenic tomato may have beneficial effects on abiotic stress tolerance. Another group of proteins are the LEA proteins found in animals and plants. They protect other proteins from aggregation during desiccation or osmotic stresses associated with low temperature. These LEA proteins play a role in desiccation tolerance during seed development under dehydration, salinity, and cold stresses (Close, 1997), probably through maintenance of protein or membrane structure, sequestration of ions, binding of water, and their functioning as molecular chaperones (Bray, 1997). Generally, accumulation of LEA proteins occurs during seed maturation and desiccation, and their level increases in vegetative tissues when plants are exposed to water stress (Ingram and Bartels, 1996). Two classes of these proteins, HVA1, group 3 LEA proteins from barley, and LE25, group 4 LEA proteins from tomato, have been shown to have a role in stress tolerance in plants (Xu et al., 1996). Transcription of genes encoding these LEA proteins is activated under osmotic stress. Rice plants transformed with the barley HVA1 gene exhibited enhanced tolerance to drought and salinity (Xu et al., 1996). Similar overexpression of these proteins in tomato for generating transgenic plants with enhanced tolerance to abiotic stresses may be possible.

CONCLUSIONS The susceptibility and/or tolerance of plants to abiotic stress involve coordinated action of multiple stress-responsive genes that also interact with other components of stress signal transduction pathways. Understanding abiotic stress mechanisms is important for the design of strategies to improve stress tolerance in crop plants including tomato.

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However, few cultural and breeding approaches have been reported in tomato for improvement of plant tolerance to abiotic stresses such as drought, salinity, and cold (Fig. 2). Presently, genetic engineering of tomatoes overexpressing several genes encoding osmoprotectants, ion transporters, and antioxidant enzymes has resulted in notable success in enhancing abiotic stress tolerance. Further progress in improving resistance in tomato to abiotic stress will depend on additional gene discoveries through transcriptome and proteome studies, which may lead to a more complete understanding of stress protection pathways. Understanding the underlying physiological processes in response to different abiotic stresses could assist in determining what promoter or transcription factor would be appropriate for use for transformation. The current knowledge of the physiological and genetic basis of abiotic stress tolerance, coupled with use of genetic transformation technologies, should allow for significant progress in the development of tomato cultivars with enhanced tolerance. Acknowledgments Research pertaining to the topic of this review is supported by Konkuk University in 2008 and 2010 Brain Pool program of Konkuk University. The research fellowship to SKP, MAG, and VJ from Konkuk university research fund is gratefully acknowledged. crop science, vol. 51, september– october 2011

References Aazami, M.A., M. Torabi, and E. Jalili. 2010. In vitro response of promising tomato genotypes for tolerance to osmotic stress. Afr. J. Biotechnol. 9:4014–4017. Abdel-Raheem, A.T., A.R. Ragab, Z.A. Kasem, F.D. Omar, and A.M. Samera. 2007. In vitro selection for tomato plants for drought tolerance via callus culture under polyethylene glycol (PEG) and mannitol treatments. Afr. Crop Sci. Conf. Proc. 8:2027–2032. Abeles, G.B., P.W. Morgan, and M.E. Saltveit. 1992. Ethylene in plant biology. Academic Press, San Diego. Abu-El-Heba, G.A., G.M. Hussein, and N.A. Abdalla. 2008. A rapid and efficient tomato regeneration and transformation system. Agric. For. Res. 58:103–110. Agharbaoui, Z., A.F. Greer, and Z. Tabaeizadeh. 1995. Transformation of the wild tomato Lycopersicon chilense Dun. by Agrobacterium tumefaciens. Plant Cell Rep. 15:102–105. doi:10.1007/ BF01690263 Ahsan, N., D.G. Lee, S.H. Lee, K.W. Lee, J.D. Bahk, and B.H. Lee. 2007. A proteomic screen and identification of waterlogging-regulated proteins in tomato roots. Plant Soil 295:37–51. doi:10.1007/s11104-007-9258-9 Alcázar, R., T. Altabella, F. Marco, C. Bortolotti, M. Reymond, C. Koncz, P. Carrasco, and A.F. Tiburcio. 2010. Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249. doi:10.1007/s00425-010-1130-0 Allen, R. 1995. Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol. 107:1049–1054. Angeloni, S.V., and M. Potts. 1986. Polysome turnover in

www.crops.org

15


Figure 2. Summary of strategies employed in tomato for developing abiotic stress tolerance.


immobilized cells of Nostoc commune (Cyanobacteria) exposed to water stress. J. Bacteriol. 168:1036–1103. Apel, K., and H. Hirt. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701 Apse, M.P., G.S. Aharon, W.A. Snedden, and E. Blumwald. 1999. Salt tolerance conferred by overexpression of a vacuolar Na+/ H+ antiport in Arabidopsis. Science 285:1256–1258. doi:10.1126/ science.285.5431.1256 Arrillaga, I., R. Gil-Mascarell, C. Gisbert, E. Sales, C. Montesinos, R. Serrano, and V. Moreno. 1998. Expression of the yeast HAL2 gene in tomato increases the in vitro salt tolerance of transgenic progenies. Plant Sci. 136:219–226. doi:10.1016/ S0168-9452(98)00122-8 Bajaj, S., J. Targolli, L.F. Liu, T.H. Ho, and R. Wu. 1999. Transgenic approaches to increase dehydration stress tolerance in plants. Mol. Breed. 5:493–503. doi:10.1023/A:1009660413133 Barthakur, S., V. Babu, and K.C. Bansal. 2001. Over-expression of osmotin induces proline accumulation and confers tolerance to osmotic stress in transgenic tobacco. J. Plant Biochem. Biotechnol. 10:31–37. Benaroudj, N., D.H. Lee, and A.L. Goldberg. 2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276:24261–24267. doi:10.1074/jbc.M101487200 Benavides, M.P., P.L. Marconi, S.M. Gallego, M.E. Comba, and M.L. Tomaro. 2000. Relationship between antioxidant defense systems and salt tolerance in Solanum tuberosum. Aust. J. Plant Physiol. 27:273–278. Biehler, K., and H. Fock. 1996. Evidence for the contribution of the Mehler peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiol. 112:265–272. Blum, A. 1988. Improving wheat grain filling under stress by stem reserve mobilization. Euphytica 100:77–83. doi:10.1023/A:1018303922482 Bohnert, H.J., and R.G. Jensen. 1996. Strategies for engineering water stress tolerance in plants. Trends Biotechnol. 14:89–97. doi:10.1016/0167-7799(96)80929-2 Bouchereau, A., A. Aziz, F. Larther, and J. Martin-Tanguy. 1999. Polyamines and environmental challenges: Recent development. Plant Sci. 140:103–125. doi:10.1016/S01689452(98)00218-0 Bowler, C., L. Slooten, S. Vandenbranden, R. De Rycke, J. Botterman, C. Sybesma, M. Van Montagu, and D. Inze. 1991. Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J. 10:1723–1732. Bowler, C., W. Van Camp, M. Van Montagu, and D. Inze. 1994. Superoxide dismutase in plants. Crit. Rev. Plant Sci. 13:199– 218. Bowler, C., M. Van Montagu, and D. Inze. 1992. Super oxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:83–116. doi:10.1146/annurev.pp.43.060192.000503 Bray, E.A. 1997. Plant responses to water deficit. Trends Plant Sci. 2:48–54. doi:10.1016/S1360-1385(97)82562-9 Breto, M.P., M.J. Asins, and E.A. Carbonell. 1993. Genetic variability in Lycopersicon species and their genetic relationships. Theor. Appl. Genet. 86:113–120. doi:10.1007/BF00223815 Briza, J., D. Pavingerová, P. Prikrylova, J. Gazdova, J. Vlasák, and H. Niedermeierová. 2008. Use of phosphomannose isomerasebased selection system for Agrobacterium-mediated transformation of tomato and potato. Biol. Plant. 52:453–461. doi:10.1007/

16

s10535-008-0090-8 Brouquisse, R., P. Wiegel, D. Rhodes, C.F. Yocum, and A.D. Hanson. 1989. Evidence for a ferredoxin-dependent choline monooxygenase from spinach chloroplast stroma. Plant Physiol. 90:322–329. doi:10.1104/pp.90.1.322 Cano, E., F. Perez-Alfocea, V. Moreno, M. Caro, and M.C. Bolarín. 1998. Evaluation of salt tolerance in cultivated and wild tomato species through in vitro shoot apex culture. Plant Cell Tissue Organ Cult. 53:19–26. doi:10.1023/A:1006017001146 Capiati, D.A., S.M. Pais, and M.T. Tellez-Inon. 2006. Wounding increases salt tolerance in tomato plants: Evidence on the participation of calmodulin-like activities in cross-tolerance signalling. J. Exp. Bot. 57:2391–2400. doi:10.1093/jxb/erj212 Casaretto, J.A., and T.H. Ho. 2003. The transcription factors HvABI5 and HvVP1 are required for the ABA induction of gene expression in barley aleurone cells. Plant Cell 15:271–284. doi:10.1105/tpc.007096 Chaudhry, Z., and H. Rashid. 2010. An improved Agrobacterium mediated transformation in tomato using hygromycin as a selective agent. Afr. J. Biotechnol. 9:1882–1891. Chen, T.H., and N. Murata. 2002. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr. Opin. Plant Biol. 5:250–257. doi:10.1016/ S1369-5266(02)00255-8 Cheng, L., Y. Zou, S. Ding, J. Zhang, X. Yu, J. Cao, and G. Lu. 2009. Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J. Integr. Plant Biol. 51:489–499. doi:10.1111/j.1744-7909.2009.00816.x Cheng, S.H., M.R. Willmann, H.C. Chen, and J. Sheen. 2002. Calcium signaling through protein kinases: The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 129:469–485. doi:10.1104/pp.005645 Cheong, Y.H., H.S. Chang, R. Gupta, X. Wang, T. Zhu, and S. Luan. 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129:661–677. doi:10.1104/pp.002857 Choi, H., J. Hong, J. Ha, J. Kang, and S.Y. Kim. 2000. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275:1723–1730. doi:10.1074/jbc.275.3.1723 Chyi, Y.S., and G.C. Phillips. 1987. High efficiency Agrobacterium mediated transformation of Lycopersicon based on conditions favourable for regeneration. Plant Cell Rep. 6:105–108. Close, T. 1997. Dehydrins: A commonality in the response of plants to dehydration and low temperature. Physiol. Plant. 100:291– 296. doi:10.1111/j.1399-3054.1997.tb04785.x Cook, R.E. 1979. Patterns of juvenile morbidity and recruitment in plants. p. 207–301. In O.T. Solbrig et al. (ed.) Topics in plant population biology. Columbia Univ. Press, Los Angeles. Cortina, C., and F.A. Culianez-Macia. 2004. Tomato transformation and transgenic plant production. Plant Cell Tissue Organ Cult. 76:269–275. doi:10.1023/B:TICU.0000009249.14051.77 Cortina, C., and F.A. Culianez-Macia. 2005. Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci. 169:75–82. doi:10.1016/j.plantsci.2005.02.026 Crowe, J.H., L.M. Crowe, and D. Chapman. 1984. Preservation of membranes in anhydrobiotic organisms: The role of trehalose. Science 223:701–703. doi:10.1126/science.223.4637.701 Davis, M.E., R.D. Lineberger, and A.R. Miller. 1991a. Effects of tomato cultivar, leaf age, and bacterial strain on transformation by Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult. 24:115–121. doi:10.1007/BF00039739

www.crops.org



the efficiency of Agrobacterium-mediated transformation of tomato. Plant Cell Rep. 16:235–240. Frary, A., and C.M. Hamilton. 2001. Efficiency and stability of high molecular weight DNA transformation: An analysis in tomato. Transgenic Res. 10:121–132. doi:10.1023/A:1008924726270 Friedman, M. 1997. Chemistry, biochemistry, and dietary role of potato polyphenols. J. Agric. Food Chem. 45:1523–1540. doi:10.1021/jf960900s Gao, N., Y. Cao, Y. Su, W. Shi, and W. Shen. 2009. Influence of bacterial density during preculture on Agrobacterium-mediated transformation of tomato. Plant Cell Tissue Organ Cult. 98:321–330. doi:10.1007/s11240-009-9566-2 Gao, X., K. Liu, and Y.T. Lu. 2010. Specific roles of AtEXPA1 in plant growth and stress adaptation. Russ. J. Plant Physiol. 57:241–246. doi:10.1134/S1021443710020111 Gisbert, C., A.M. Rus, M.C. Bolarín, J.M. Coronado, I. Arrillaga, C. Montesinos, M. Caro, R. Serrano, and V. Moreno. 2000. The yeast HAL1 gene improves salt tolerance of transgenic tomato. Plant Physiol. 123:393–402. doi:10.1104/pp.123.1.393 Glick, B.R. 1995. The enhancement of plant growth by free-living bacteria. Can. J. Microbiol. 41:109–117. doi:10.1139/m95-015 Goel, D., A.K. Singh, V. Yadav, S.B. Babbar, and K.C. Bansal. 2010. Overexpression of osmotin gene confers tolerance to salt and drought stresses in transgenic tomato (Solanum lycopersicum L.). Protoplasma 245:133–141. doi:10.1007/s00709-010-0158-0 Grichko, V.P., and B.R. Glick. 2001. Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiol. Biochem. 39:11–17. doi:10.1016/S09819428(00)01212-2 Hamza, S., and Y. Chupeau. 1993. Re-evaluation of conditions for plant regeneration and Agrobacterium-mediated transformation from tomato (Lycopersicon esculentum). J. Exp. Bot. 44:1837– 1845. doi:10.1093/jxb/44.12.1837 Hare, P.D., W.A. Cress, and V.J. Staden. 1998. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21:535–554. doi:10.1046/j.1365-3040.1998.00309.x Hasan, H., A.J. Khan, S. Khan, A.H. Shah, A.R. Khan, and B. Mirza. 2008. Transformation of tomato (Lycopersicon esculentum Mill.) with Arabidopsis early flowering gene Apetalai (API) through Agrobacterium infiltration of ripened fruits. Pak. J. Bot. 40:161–173. Hazen, S.P., Y. Wu, and J.A. Kreps. 2003. Gene expression profiling of plant responses to abiotic stress. Funct. Integr. Genomics 3:105–111. doi:10.1007/s10142-003-0088-4 Hemavathi, C.P., Upadhyaya, A. Nookaraju, H.S. Kim, J.H. Jeon, O.M. Ho, S.C. Chun, D.H. Kim, and S.W. Park. 2010b. Biochemical analysis of enhanced tolerance in transgenic potato plants overexpressing D-galacturonic acid reductase gene in response to various abiotic stresses. Mol. Breed. doi:10.1007/ s11032-010-9465-6. Hemavathi, C.P., Upadhyaya, A. Nookaraju, E.Y. Ko, S.C. Chun, D.H. Kim, and S.W. Park. 2010a. Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnol. Lett. 32:321–330. doi:10.1007/ s10529-009-0140-0 Hemavathi, C.P., Upadhyaya, K.E. Young, A. Nookaraju, H.S. Kim, J.J. Heung, O.M. Ho, C.R. Aswath, S.C. Chun, D.H. Kim, and S.W. Park. 2009. Over-expression of strawberry D-galacturonic acid reductase in potato leads to accumulation of vitamin C with enhanced abiotic stress tolerance. Plant Sci. 177:659–667. doi:10.1016/j.plantsci.2009.08.004 Herbette, S., A. Le Menn, P. Rousselle, T. Ameglio, Z. Faltin, G.

www.crops.org

17


Davis, M.L., A.R. Miller, and R.D. Lineberger. 1991b. Temporal competence for transformation of Lycopersicon esculentum (L. Mill.) cotyledons by Agrobacterium tumefaciens: Relation to wound-healing and soluble plant factors. J. Exp. Bot. 42:359– 364. doi:10.1093/jxb/42.3.359 De Virgilio, C., T. Hottiger, J. Dominguez, T. Boller, and A. Wiemken. 1994. The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant. Eur. J. Biochem. 219:179–186. doi:10.1111/j.1432-1033.1994.tb19928.x Domínguez, T., M.L. Hernandez, J.C. Pennycooke, P. Jiménez, J.M. Martinez-Rivas, C. Sanz, E.J. Stockinger, J.J. SanchezSerrano, and M. Sanmartin. 2010. Increasing ω-3 desaturase expression in tomato results in altered aroma profile and enhanced resistance to cold stress. Plant Physiol. 153:655–665. doi:10.1104/pp.110.154815 Elbein, A. 1974. The metabolism of a,a-trehalose. Adv. Carbohydr. Chem. Biochem. 30:227–256. doi:10.1016/S00652318(08)60266-8 Ellul, P., B. Garcia-Sogo, B. Pineda, G. Rios, L.A. Roig, and V. Moreno. 2003. The ploidy level of transgenic plants in Agrobacterium mediated transformation of tomato cotyledons (Lycopersicon esculentum Mill.) is genotype and procedure dependent. Theor. Appl. Genet. 106:231–238. Estan, M.T., M.M. Martinez-Rodriguez, F. Perez-Alfocea, T.J. Flower, and M.C. Bolarin. 2005. Grafting raises the salt tolerance of tomato through limiting the transport of sodium and chloride to the shoot. J. Exp. Bot. 56:703–712. doi:10.1093/jxb/eri027 FAOSTAT. 2010. FAO statistical databases. FAO, Statistics Division, Rome. Fernandez-Munoz, R., J.J. Gonzalez-Fernandez, and J. Cuartero. 1995. Variability of pollen tolerance to low temperatures in tomato and related wild species. J. Hortic. Sci. 70:41–49. Fidalgo, F., A. Santos, I. Santos, and R. Salema. 2004. Effects of longterm salt stress on antioxidant defence systems, leaf water relations and chloroplast ultrastructure of potato plants. Ann. Appl. Biol. 145:185–192. doi:10.1111/j.1744-7348.2004.tb00374.x Fillati, J.J., J. Kiser, R. Ronald, and L. Comai. 1987. Efficient transfer of glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Biotechnology 5:726–730. doi:10.1038/nbt0787-726 Flors, V., M. Paradís, J. García-Andrade, M. Cerezo, C. GonzálezBosch, and P.G. Pilar. 2007. A tolerant behavior in salt-sensitive tomato plants can be mimicked by chemical stimuli. Plant Signal. Behav. 2:50–57. doi:10.4161/psb.2.1.3862 Foolad, M.R. 2007. Genome mapping and molecular breeding of tomato. Int. J. Plant Genomics 2007:64358. Foolad, M.R., and R.A. Jones. 1991. Genetic analysis of salt tolerance during germination in Lycopersicon. Theor. Appl. Genet. 81:321–326. Foolad, M.R., and G.Y. Lin. 2000. Relationship between cold tolerance during seed germination and vegetative growth in tomato. Germplasm evaluation. J. Am. Soc. Hortic. Sci. 125:679–683. Foolad, M.R., and G.Y. Lin. 2001. Relationship between cold tolerance during seed germination and vegetative growth in tomato. Analysis of response and correlated response to selection. J. Am. Soc. Hortic. Sci. 126:216–220. Frankel, N., E. Hasson, N.D. Iusem, and M.S. Rossi. 2003. Adaptive evolution of the water stress-induced gene Asr2 in Lycopersicon species dwelling in arid habitats. Mol. Biol. Evol. 20:1955–1962. doi:10.1093/molbev/msg214 Frary, A., and E.D. Earle. 1996. An examination of factors affecting


Branlard, Y. Eshdat, J.L. Julien, J.R. Drevet, and P. RoeckelDrevet. 2005. Modification of photosynthetic regulation in tomato overexpressing glutathione peroxidase. Biochim. Biophys. Acta 1724:108–118. Hobo, T., Y. Kowyama, and T. Hattori. 1999. A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc. Natl. Acad. Sci. USA 96:15348–15353. doi:10.1073/pnas.96.26.15348 Holmberg, N., and L. Bulow. 1998. Improving stress tolerance in plants by gene transfer. Trends Plant Sci. 3:61–66. doi:10.1016/ S1360-1385(97)01163-1 Hsieh, T.H., J.T. Lee, P.T. Yang, L.H. Chiu, Y. Charng, Y.C. Wang, and M.T. Chan. 2002. Heterologous expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol. 129:1086–1094. doi:10.1104/pp.003442 Hsieh, T.H., C.W. Li, R.C. Su, C.P. Cheng, Sanjaya, Y.C. Tsai, and M.T. Chan. 2010. A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473. doi:10.1007/s00425-010-1147-4 Hu, W., and G.C. Phillips. 2001. A combination of overgrowthcontrol and antibiotics improves Agrobacterium tumefaciensmediated transformation efficiency for cultivated tomato (L. esculentum). In Vitro Cell. Biol. Plant 37:12–18. doi:10.1007/ s11627-001-0003-4 Ieamkhang, S., and O. Chatchawankanphanich. 2005. Augmentin as an alternative antibiotic for growth suppression of Agrobacterium for tomato (Lycopersicon esculentum) transformation. Plant Cell Tissue Organ Cult. 82:213–220. doi:10.1007/s11240-005-0416-6 Ingram, J., and D. Bartels. 1996. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:377–403. doi:10.1146/annurev.arplant.47.1.377 Jackman, R.L., R.Y. Yada, A.G. Marangoni, K.L. Parkin, and D.W. Stanley. 1989. Chilling injury: A review of quality aspects. J. Food Qual. 11:253–278. doi:10.1111/j.1745-4557.1988.tb00887.x Jacobson, C.B., J.J. Pasternak, and B.R. Glick. 1994. Partial purification and characterization of ACC deaminase from the plant growth-promoting rhizobacterium Pseudomonas putida GR1 2-2S. Can. J. Microbiol. 40:1019–1025. doi:10.1139/m94-162 Jaglo, K.R., S. Kleff, K.L. Amundsen, X. Zhang, V. Haake, J.Z. Zang, T. Deits, and M.F. Thomashow. 2001. Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol. 127:910–917. doi:10.1104/pp.010548 Jaglo-Ottosen, K.R., S.J. Gilmour, D.G. Zarka, O. Schabenberger, and M.F. Tomashow. 1998. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106. doi:10.1126/science.280.5360.104 Jia, G.X., Z.Q. Zhu, F.Q. Chang, and Y.X. Li. 2002. Transformation of tomato with the BADH gene from Atriplex improves salt tolerance. Plant Cell Rep. 21:141–146. doi:10.1007/s00299002-0489-1 Johansson, I., C. Larsson, B. Ek, and P. Kjellbom. 1996. The major integral proteins of spinach leaf plasma membranes are putative aquaporines and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8:1181–1191. doi:10.1105/ tpc.8.7.1181 Kaiser, W.M. 1979. Reversible inhibition of the Calvin cycle and activation the oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145:377–382.

18

doi:10.1007/BF00388364 Kaldenhoff, R., and M. Fischer. 2006. Aquaporins in plants. Acta Physiol. (Oxf.) 187:169–176. doi:10.1111/j.17481716.2006.01563.x Kang, J., H. Choi, M. Im, and S.Y. Kim. 2002. Arabidopsis basic leucine zipper proteins mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357. doi:10.1105/tpc.010362 Katia, H., J. Lipp, and T.A. Brown. 1993. Enhanced transformation of tomato co-cultivated with Agrobacterium tumefaciens C58C1Rifr:pGSFR1161 in the presence of acetosyringone. Plant Cell Rep. 12:422–425. Kaur, P., and K.C. Bansal. 2010. Efficient production of transgenic tomatoes via Agrobacterium-mediated transformation. Biol. Plant. 54: \344–348. Kawaguchi, R., E.A. Bray, and J. Bailey-Serres. 2003. Water-deficit induced translational control in Nicotiana tabacum. Plant Cell Environ. 26:221–229. doi:10.1046/j.1365-3040.2003.00952.x Kawaguchi, R., T. Girke, E.A. Bray, and J. Bailey-Serres. 2004. Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J. 38:823–839. doi:10.1111/j.1365-313X.2004.02090.x Khare, N., D. Goyary, N.K. Singh, P. Shah, M. Rathore, S. Anandhan, D. Sharma, M. Arif, and Z. Ahmed. 2010. Transgenic tomato cv. Pusa Uphar expressing a bacterial mannitol-1-phosphate dehydrogenase gene confers abiotic stress tolerance. Plant Cell Tissue Organ Cult. 103:267–277. doi:10.1007/s11240-010-9776-7 Khoudi, H., A. Nouri-Khemakhem, S. Gouiaa, and K. Masmoudi. 2009. Optimization of regeneration and transformation parameters in tomato and improvement of its salinity and drought tolerance. Afr. J. Biotechnol. 8:6068–6076. Kimball, B.A., and S.B. Idso. 1983. Increasing atmospheric CO2 effects on crop yield, water-use and climate. Agric. Water Manage. 7:55–72. doi:10.1016/0378-3774(83)90075-6 Knepper, M.A. 1994. The aquaporin family of molecular water channels. Proc. Natl. Acad. Sci. USA 91:6255–6258. doi:10.1073/ pnas.91.14.6255 Kobayashi, F., E. Maeta, A. Terashima, and S. Takumi. 2008. Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings. Physiol. Plant. 134:74–86. doi:10.1111/j.13993054.2008.01107.x Kulkarni, M., and U. Deshpande. 2007. In vitro screening of tomato cultivars for drought resistance using polyethylene glycol. Afr. J. Biotechnol. 6:691–696. Kumar, S.V., M.L. Sharma, and M.V. Rajam. 2006. Polyamine biosynthetic pathway as a novel target for potential applications in plant biotechnology. Physiol. Mol. Biol. Plants 12:13–28. Larkindale, J., J.D. Hall, M.R. Knight, and E. Vierling. 2005. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138:882–897. doi:10.1104/pp.105.062257 Leclercq, J., B. Ranty, M.T. Sanchez-Ballesta, Z. Li, B. Jones, A. Jauneau, J.C. Pech, A. Latche, R. Ranjeva, and M. Bouzayen. 2005. Molecular and biochemical characterization of LeCRK1, a ripening-associated tomato CDPK-related kinase. J. Exp. Bot. 56:25–35. Lee, S.S., H.S. Cho, G.M. Yoon, J.W. Ahn, H.H. Kim, and H.S. Pai. 2003. Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J. 33:825–840. doi:10.1046/j.1365313X.2003.01672.x Li, J., J.M. Zhou, and Z.Q. Duan. 2007. Effects of elevated CO2

www.crops.org



regulates water channel activity of the seed specific alpha-TIP. EMBO J. 14:3028–3035. May, M.J., T. Vernoux, C. Leaver, M. Van Montagu, and D. Inzé. 1998. Glutathione homeostasis in plants: Implications for environmental sensing and plant development. J. Exp. Bot. 49:649– 667. doi:10.1093/jexbot/49.321.649 Mayak, S., T. Tirosh, and B.R. Glick. 1999. Effect of wild-type and mutant plant growth-promoting rhizobacteria on the rooting of mung bean cuttings. J. Plant Growth Regul. 18:49–53. doi:10.1007/PL00007047 Mayak, S., T. Tirosh, and B.R. Glick. 2004. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 42:565–572. doi:10.1016/j.plaphy.2004.05.009 Mayer, A.M., and E. Harel. 1991. Phenoloxidases and their significance in fruit and vegetables. Food Enzymol. 72:373–398. McCormick, S., J. Niedermeyer, B. Fry, A. Barnason, R. Horch, and R. Farley. 1986. Leaf disk transformation of cultivated tomato (L. esculentum) using Agrobacterium tumefaciens. Plant Cell Rep. 5:81–84. doi:10.1007/BF00269239 Medina, M.I., M.A. Quesada, F. Pliego, M.A. Botella, and V. Valpuesta. 1999. Expression of the tomato peroxidase gene TPX1 in NaCl-adapted and unadapted suspension cells. Plant Cell Rep. 18:680–683. doi:10.1007/s002990050642 Miller, J.C., and S.D. Tanksley. 1990. RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theor. Appl. Genet. 80:437–448. Mittova, V., M. Tal, M. Volokita, and M. Guy. 2003. Up-regulation of the leaf mitochondrial and peroxiomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ. 26:845–856. doi:10.1046/j.1365-3040.2003.01016.x Moghaieb, R., H. Saneoka, and K. Fujita. 2004. Shoot regeneration from Gus-transformed tomato (Lycopersicon esculentum) hairy root. Cell. Mol. Biol. Lett. 9:439–449. Moghaieb, R.E.A., N. Tanaka, H. Saneoka, H.A. Hussein, S.S. Yousef, M.A.F. Ewada, A.M.A. Mohamed, and F. Kounosuke. 2000. Expression of betaine aldehyde dehydrogenase gene in transgenic tomato hairy roots leads to the accumulation of glycine betaine and contributes to the maintenance of the osmotic potential under salt stress. Soil Sci. Plant Nutr. 46:873–883. Mohamed, E.A., T. Iwaki, I. Munir, M. Tamoi, S. Shigeoka, and A. Wadano. 2003. Overexpression of bacterial catalase in tomato leaf chloroplasts enhances photo-oxidative stress tolerance. Plant Cell Environ. 26:2037–2046. doi:10.1046/j.00168025.2003.01121.x Morgan, A., P. Cox, D. Turner, E. Pell, M. Davey, K. Gartland, and B. Mulligan. 1987. Transformation of tomato using an Ri plasmid vector. Plant Sci. 49:37–49. doi:10.1016/01689452(87)90018-5 Na, J.K. 2005. Genetic approaches to improve drought tolerance of tomato and tobacco. Ph.D. diss. The Ohio State University, Columbus. Nakashima, K., and K. Yamaguchi-Shinozaki. 2006. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol. Plant. 1126:62–71. doi:10.1111/j.1399-3054.2005.00592.x Neumann, D., L. Nover, B. Parthier, R. Rieger, K.D. Scharf, R. Wollgiehn, and U. zur Nieden. 1989. Heat shock and other stress response systems of plants. Biol. Zent. Bl. 108:1–155. Noctor, G., A.C.M. Arisi, L. Jouanin, K.J. Kunert, H. Rennenberg, and C.H. Foyer. 1998. Glutathione: Biosynthesis, metabolism

www.crops.org

19


concentration on growth and water usage of tomato seedlings under different ammonium/nitrate ratios. J. Environ. Sci. (China) 19:1100–1107. doi:10.1016/S1001-0742(07)60179-X Li, W., M. Kabbage, and M.B. Dickman. 2010. Transgenic expression of an insect inhibitor of apoptosis gene, SfIAP, confers abiotic and biotic stress tolerance and delays tomato fruit ripening. Physiol. Mol. Plant Pathol. 74:363–375. doi:10.1016/j. pmpp.2010.06.001 Ling, H.Q., D. Kriseleit, and M.W. Ganan. 1998. Effect of ticarcillin/ potassium clavulanate on callus growth and shoot regeneration in Agrobacterium-mediated transformation of tomato (Lycopersicon esculentum). Plant Cell Rep. 17:843–847. doi:10.1007/ s002990050495 Liu, J., and J.K. Zhu. 1998. A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945. doi:10.1126/science.280.5371.1943 Liu, J.H., H. Kitashiba, J. Wang, Y. Ban, and T. Moriguchi. 2007. Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol. 24:117–126. doi:10.5511/ plantbiotechnology.24.117 Lozano, R., T. Angosto, P. Gomez, C. Payan, J. Capel, P. Huijser, J. Salinas, and J. Martinez-Zapater. 1998. Tomato flower abnormalities induced by low temperatures are associated with changes of expression of MADS-box genes. Plant Physiol. 117:91–100. doi:10.1104/pp.117.1.91 Lu, G., C. Gao, X. Zheng, and B. Han. 2009. Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229:605–615. doi:10.1007/s00425008-0857-3 Lurie, S. 1998. Postharvest heat treatments. Postharvest Biol. Technol. 14:257–269. doi:10.1016/S0925-5214(98)00045-3 Mackenzie, K.F., K.K. Singh, and A.D. Brown. 1988. Water stress plating hypersensitivity of yeast: Protective role of trehalose in Saccharomyces cerevisiae. J. Gen. Microbiol. 134:1661–1666. Maggio, A., G. Barbieri, G. Raimondi, and S.D. Pascale. 2010. Contrasting effects of GA3 treatments on tomato plants exposed to increasing salinity. J. Plant Growth Regul. 29:63– 72. doi:10.1007/s00344-009-9114-7 Mäkelä, P., K. Jokinen, M. Kontturi, P. Peltonen-Sainio, E. Pehu, and S. Somersalo. 1998. Foliar application of glycine betaine— a novel product from sugar beet—as an approach to increase tomato yield. Ind. Crops Prod. 7:139–148. doi:10.1016/S09266690(97)00042-3 Mäkelä, P., M. Kontturi, E. Pehu, and S. Somersalo. 1999. Photosynthetic response of drought- and salt-stressed tomato and turnip rape plants to foliar-applied glycine betaine. Physiol. Plant. 105:45–50. doi:10.1034/j.1399-3054.1999.105108.x Marin-Manzano, M.C., M.P. Rodriguez-Rosales, A. Belver, J.P. Donaire, and K. Venema. 2004. Heterologously expressed protein phosphatase calcineurin downregulates plant plasma membrane H+-ATPase activity at the posttranslational level. FEBS Lett. 576:266–270. doi:10.1016/j.febslet.2004.09.008 Martinez-Rodriguez, M.M., M.T. Estan, E. Moyano, J.O. GarciaAbellan, F.B. Flores, J.F. Campos, M.J. Al-Azzawi, T.J. Flowers, and M.C. Bolarin. 2008. The effectiveness of grafting to improve salt tolerance in tomato when an ‘excluder’ genotype is used as scion. Environ. Exp. Bot. 63:392–401. doi:10.1016/j. envexpbot.2007.12.007 Maurel, C. 2007. Plant aquaporins: Novel functions and regulation properties. FEBS Lett. 581:2227–2236. doi:10.1016/j.febslet.2007.03.021 Maurel, C., R. Kada, and J.C.M. Guern. 1995. Phosphorylation


and relationship to stress tolerance explored in transformed plants. J. Exp. Bot. 49:623–647. doi:10.1093/jexbot/49.321.623 Oh, S.H., S.I. Song, I.S. Kim, H.J. Jang, S.Y. Kim, M. Kim, Y.K. Kim, B.H. Nahm, and J.K. Kim. 2005. Arabidopsis CBF3/ DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol. 138:341– 351. doi:10.1104/pp.104.059147 Olson, D.C., J.H. Oetiker, and S.F. Yang. 1995. Analysis of LEACS3, a 1-aminocyclopropane-1-carboxylic acid synthase gene expressed during flooding in the roots of tomato plants. J. Biol. Chem. 270:14056–14061. doi:10.1074/jbc.270.23.14056 Ordookhani, K., K. Khavazi, A. Moezzi, and F. Rejali. 2010. Influence of PGPR and AMF on antioxidant activity, lycopene and potassium contents in tomato. Afr. J. Agric. Res. 5:1108–1116. Orozco-Cárdenas, M., B. McGurl, and C.A. Ryan. 1993. Expression of an antisense prosystemin gene in tomato plants reduces the resistance toward Manduca sexta larvae. Proc. Natl. Acad. Sci. USA 90:8273–8276. doi:10.1073/pnas.90.17.8273 Orsini, F., P. Cascone, S.D. Pascale, G. Barbieri, G. Corrado, R. Rao, and A. Maggio. 2010. Systemin-dependent salinity tolerance in tomato: Evidence of specific convergence of abiotic and biotic stress responses. Physiol. Plant. 138:10–21. doi:10.1111/ j.1399-3054.2009.01292.x Ouziad, F., P. Wilde, E. Schmelzer, U. Hilderbrandt, and H. Bothe. 2006. Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ. Exp. Bot. 57:177–186. doi:10.1016/j.envexpbot.2005.05.011 Pan, I.C., C.W. Li, R.C. Su, C.P. Cheng, C.S. Lin, and M.T. Chan. 2010. Ectopic expression of an EAR motif deletion mutant of SlERF3 enhances tolerance to salt stress and Ralstonia solanacearum in tomato. Planta 232:1075–1086. doi:10.1007/ s00425-010-1235-5 Pardo, J.M., M.P. Reddy, S. Yang, A. Maggio, G.H. Huh, T. Matsumoto, M.A. Coca, M. Paino-D’Urazo, H. Koiwa, D.J. Yun, A.A. Watad, R.A. Bressan, and P.M. Hasegawa. 1998. Stress signaling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proc. Natl. Acad. Sci. USA 95:9681–9686. doi:10.1073/pnas.95.16.9681 Park, E.J., Z. Jeknić, and T.H.H. Chen. 2006. Exogenous application of glycine betaine increases chilling tolerance in tomato plants. Plant Cell Physiol. 47:706–714. doi:10.1093/pcp/pcj041 Park, E.J., Z. Jeknić, A. Sakamoto, J. DeNoma, R. Yuwansiri, N. Murata, and T.H. Chen. 2004. Genetic engineering of glycine betaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J. 40:474–487. doi:10.1111/j.1365313X.2004.02237.x Park, S.H., J.L. Morris, J.E. Park, K.D. Hirschi, and R.H. Smith. 2003. Efficient and genotype-independent Agrobacterium-mediated tomato transformation. J. Plant Physiol. 160:1253–1257. doi:10.1078/0176-1617-01103 Pearce, G., D. Strydom, S. Johnson, and C.A. Ryan. 1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–898. doi:10.1126/ science.253.5022.895 Pelham, H.R.B. 1989. Control of protein exit from the endoplasmic reticulum. Annu. Rev. Cell Biol. 5:1–23. doi:10.1146/annurev. cb.05.110189.000245 Pfitzner, A.J.P. 1998. Transformation of tomato. Methods Mol. Biol. 81:359–363. Qiu, D., G. Diretto, R. Tavarza, and G. Giuliano. 2007. Improved protocol for Agrobacterium mediated transformation of tomato

20

and production of transgenic plants containing carotenoid biosynthetic gene CsZCD. Sci. Hortic. (Amst.) 112:172–175. doi:10.1016/j.scienta.2006.12.015 Rahnama, H., and H. Ebrahimzadeh. 2005. The effect of NaCl on antioxidant enzyme activities in potato seedling. Biol. Plant. 49:93–97. doi:10.1007/s10535-005-3097-4 Rajam, M.V., S. Dagar, B. Waie, J.S. Yadav, P.A. Kumar, F. Shoeb, and R. Kumria. 1998. Genetic engineering of polyamine and carbohydrate metabolism for osmotic stress tolerance in higher plants. J. Biosci. 23:473–482. doi:10.1007/BF02936141 Rhodes, D., and A.D. Hanson. 1993. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:357–384. doi:10.1146/ annurev.pp.44.060193.002041 Rochange, S.F., C.L. Wenzel, and S.J. McQueen-Mason. 2001. Impaired growth in transgenic plants overexpressing an expansin isoform. Plant Mol. Biol. 46:581–589. doi:10.1023/A:1010650217100 Romero-Aranda, M.R., O. Jurado, and J. Cuartero. 2006. Silicon alleviates the deleterious salt effect on tomato plant growth by improving plant water status. J. Plant Physiol. 163:847–855. doi:10.1016/j.jplph.2005.05.010 Roy, R., R.S. Purty, V. Agrawal, and S.C. Gupta. 2006. Transformation of tomato cultivar Pusa Ruby with BspA gene from Populus tremula for drought tolerance. Plant Cell Tissue Organ Cult. 84:56–68. doi:10.1007/s11240-005-9000-3 Sade, N., M. Gebretsadik, R. Seligmann, A. Schwartz, R. Wallach, and M. Moshelion. 2010. The role of tobacco aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress. Plant Physiol. 152:245–254. doi:10.1104/pp.109.145854 Sajid, Z.A., and F. Aftab. 2009. Amelioration of salinity tolerance in Solanum tuberosum L. by exogenous application of ascorbic acid. In Vitro Cell. Dev. Biol. Plant 45:540–549. doi:10.1007/ s11627-009-9252-4 Sakamoto, A., and N. Murata. 2000. Genetic engineering of glycine betaine synthesis in plants: Current status and implications for enhancement of stress tolerance. J. Exp. Bot. 51:81–88. doi:10.1093/jexbot/51.342.81 Sanchez-Barrena, M.J., M. Martinez-Ripoll, J.K. Zhu, and A. Albert. 2005. The structure of the Arabidopsis thaliana SOS3: Molecular mechanism of sensing calcium for salt stress response. J. Mol. Biol. 345:1253–1264. doi:10.1016/j.jmb.2004.11.025 Sancho, M.A., S. Milrad de Forchetti, F. Pliego, V. Valpuesta, and M.A. Quesada. 1996. Peroxidase activity and isoenzymes in the culture medium of NaCl adapted tomato suspension cells. Plant Cell Tissue Organ Cult. 44:161–167. doi:10.1007/BF00048195 Santa-Cruz, A., M.M. Martínez-Rodríguez, M.C. Bolarín, and J. Cuartero. 2001. Response of plant yield and ion contents to salinity in grafted tomato plants. Acta Hortic. 559:413–417. Santa-Cruz, A., M.M. Martinez-Rodriguez, F. Perez-Alfocea, R. Romero-Aranda, and M.C. Bolarin. 2002. The rootstock effect on the tomato salinity response depends on the shoot genotype. Plant Sci. 162:825–831. doi:10.1016/S0168-9452(02)00030-4 Scandalios, J.G. 1993. Oxygen stress and superoxide dismutase. Plant Physiol. 101:7–12. Schendel, S.L., M. Montal, and J.C. Reed. 1998. Bcl-2 family proteins as ion-channels. Cell Death Differ. 5:372–380. doi:10.1038/sj.cdd.4400365 Sen Gupta, A., J.L. Heinen, S. Holaday, J.J. Burke, and R.D. Allen. 1993. Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase.

www.crops.org



environments. Theor. Appl. Genet. 101:733–741. doi:10.1007/ s001220051538 Sun, H.J., S. Uchii, S. Watanabe, and H. Ezura. 2006. A high efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol. 47:426– 431. doi:10.1093/pcp/pci251 Swindell, W.R., M. Huebner, and A.P. Weber. 2007. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8:125. doi:10.1186/1471-2164-8-125 Takeda, T., A. Yokota, and S. Shigeoka. 1995. Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol. 36:1089–1095. Thipyapong, P., J. Melkonian, D.W. Wolfe, and J.C. Steffens. 2004. Suppression of polyphenol oxidases increases stress tolerance in tomato. Plant Sci. 167:693–703. doi:10.1016/j. plantsci.2004.04.008 Thomas, J.C., M. Sepahi, B. Arendall, and H.J. Bohnert. 1995. Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant Cell Environ. 18:801–806. doi:10.1111/j.1365-3040.1995.tb00584.x Thomashow, M.F. 1999. Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:571–599. doi:10.1146/annurev. arplant.50.1.571 Uehlein, N., C. Lovisolo, F. Siefritz, and R. Kaldenhoff. 2003. The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737. doi:10.1038/ nature02027 Uno, Y., T. Furuhata, H. Abe, R. Yoshida, K. Shinozaki, and K. Yamaguchi-Shinozaki. 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. USA 97:11632–11637. doi:10.1073/pnas.190309197 Urao, T., T. Katagiri, T. Mizoguchi, K. Yamaguchi-Shinozaki, N. Hayashida, and K. Shinozaki. 1994. Two genes that encode Ca2+–dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Mol. Gen. Genet. 244:331–340. doi:10.1007/BF00286684 van Eck, J.M., A.D. Blowers, and E.D. Earle. 1995. Stable transformation of tomato cell cultures after bombardment with plasmid and YAC DNA. Plant Cell Rep. 14:299–304. van Roekel, J.S.C., B. Damm, L.S. Melchers, and A. Hoekema. 1993. Factors influencing transformation frequency of tomato (Lycopersicon esculentum). Plant Cell Rep. 12:644–647. Vannini, C., M. Campa, M. Iriti, A. Genga, F. Faoro, S. Carravieri, G.L. Rotino, M. Rossoni, A. Spinardi, and M. Bracale. 2007. Evaluation of transgenic tomato plants ectopically expressing the rice Osmyb4 gene. Plant Sci. 173:231–239. doi:10.1016/j. plantsci.2007.05.007 Venema, J.H., P. Linger, A.W. van Heusden, P.R. van Hasselt, and W. Bruggemann. 2005. The inheritance of chilling tolerance in tomato (Lycopersicon spp.). Plant Biol. 7:118–130. doi:10.1055/s-2005-837495 Verslues, P.E., and J.K. Zhu. 2005. Before and beyond ABA: Upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem. Soc. Trans. 33:375–379. doi:10.1042/BST0330375 Wang, G.P., X.Y. Zhang, F. Li, Y. Luo, and W. Wang. 2010. Over accumulation of glycine betaine enhances tolerance to drought

www.crops.org

21


Proc. Natl. Acad. Sci. USA 90:1629–1633. doi:10.1073/ pnas.90.4.1629 Seong, E.S., K.H. Baek, S.K. Oh, S.H. Jo, S.Y. Yi, J.M. Park, Y.H. Joung, S. Lee, H.S. Cho, and D. Choi. 2007. Induction of enhanced tolerance to cold stress and disease by over-expression of the pepper CAPIF1 gene in tomato. Physiol. Plant. 129:555–566. doi:10.1111/j.1399-3054.2006.00839.x Serenko, E.K., V.N. Ovchinnikova, L.V. Kurenina, E.N. Baranova, A.A. Gulevich, A.N. Maisuryan, and P.N. Kharchenko. 2009. Production of transgenic tomato plants with the Fe-dependent superoxide dismutase gene. Russ. Agric. Sci. 35:223–226. doi:10.3103/S1068367409040041 Serrano, R., and R. Gaxiola. 1994. Microbial models and salt stress tolerance in plants. Crit. Rev. Plant Sci. 13:121–133. Shahin, E.A., K. Sukhapinda, R.B. Simpson, and R. Spivey. 1986. Transformation of cultivated tomato by a binary vector in Agrobacterium rhizogenes: Transgenic plants with normal phenotypes harbor binary vector T-DNA, but not Ri-plasmid T-DNA. Theor. Appl. Genet. 72:770–777. doi:10.1007/BF00266543 Shalata, A., and P.M. Neumann. 2001. Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduce lipid peroxidation. J. Exp. Bot. 52:2207–2211. Sharma, M.K., A.U. Solanke, D. Jani, Y. Singh, and A.K. Sharma. 2009. A simple and efficient Agrobacterium-mediated procedure for transformation of tomato. J. Biosci. 34:423–433. doi:10.1007/s12038-009-0049-8 Sharom, M., C. Willemot, and J.E. Thompson. 1994. Chilling injury induces lipid phase changes in membranes of tomato fruit. Plant Physiol. 105:305–308. Shinozaki, K., and K. Yamaguchi-Shinozaki. 1997. Gene expression and signal transduction in water stress response. Plant Physiol. 115:327–334. doi:10.1104/pp.115.2.327 Shinozaki, K., and K. Yamaguchi-Shinozaki. 2000. Molecular response to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3:217–223. Shinozaki, K., and K. Yamaguchi-Shinozaki. 2007. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58:221–227. doi:10.1093/jxb/erl164 Shinozaki, K., K. Yamaguchi-Shinozaki, and M. Seki. 2003. Regulatory network of gene expression in the drought and cold stress response. Curr. Opin. Plant Biol. 6:410–417. doi:10.1016/ S1369-5266(03)00092-X Sigareva, M., R. Spivey, M. Willits, C. Kramer, and Y.F. Chang. 2004. An efficient mannose selection protocol for tomato that has no adverse effect on the ploidy level of transgenic plants. Plant Cell Rep. 23:236–245. doi:10.1007/s00299-004-0809-8 Singer, M.A., and S. Lindquist. 1998. Thermotolerance in Saccharomyces cerevisiae: The Yin and Yang of trehalose. Trends Biotechnol. 16:460–468. doi:10.1016/S0167-7799(98)01251-7 Singh, A.K., and D.R. Sharma. 2008. In vitro screening and regeneration of water stress tolerant culture of tomato. Indian J. Plant Physiol. 13:23–28. Stachel, S.E., E.W. Nester, and P.C. Zambryski. 1986. A plant cell factor induces Agrobacterium tumefaciens vir gene expression. Proc. Natl. Acad. Sci. USA 83:379–383. doi:10.1073/ pnas.83.2.379 Steller, H. 1995. Mechanisms and genes of cellular suicide. Science 267:1445–1449. doi:10.1126/science.7878463 Subudhi, P.K., D.T. Rosenow, and H.T. Nguyen. 2000. Quantitative trait loci for the stay green trait in sorghum (Sorghum bicolor L. Moench): Consistency across genetic backgrounds and


and heat stress in wheat leaves in the protection of photosynthesis. Photosynthetica 48:117–126. doi:10.1007/s11099-0100016-5 Wang, W.G., T. Barak, B. Vinocur, O. Shoseyov, and A. Altman. 2003. Abiotic resistance and chaperones: Possible physiological role of SP1, a stable and stabilizing protein from Populus. p. 439–443. In I.K. Vasil (ed.) Plant biotechnology 2002 and beyond. Kluwer Academic Publ., Dordrecht, Boston, London. Wang, W.X., D. Pelah, T. Alergand, O. Shoseyov, and A. Altman. 2002. Characterization of SP1, a stress-responsive, boiling-soluble, homo-oligomeric protein from aspen (Populus tremula L.). Plant Physiol. 130:865–875. doi:10.1104/pp.002436 Wang, Y., M. Wisniewski, R. Meilan, M. Cui, and L. Fuchigami. 2006. Transgenic tomato (Lycopersicon esculentum) that overexpress cAPX exhibits enhanced tolerance to UV-B and heat stress. J. Appl. Hort. 8:87–90. Weigel, P., E.A. Weretilnyk, and A.D. Hanson. 1986. Betaine aldehyde oxidation by spinach chloroplasts. Plant Physiol. 82:753– 759. doi:10.1104/pp.82.3.753 Wu, Y., Y. Chen, X. Liang, and X. Wang. 2006. An experimental assessment of the factors influencing Agrobacterium-mediated transformation in tomato. Russ. J. Plant Physiol. 53:252–256. doi:10.1134/S1021443706020166 Xiong, L., K.S. Schumaker, and J.K. Zhu. 2002. Cell signaling during cold, drought, and salt stress. Plant Cell 4:S165–S183. Xu, D., X. Duan, B. Wang, B. Hong, T. Ho, and R. Wu. 1996. Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol. 110:249–257. Xu, P., S.J. Rogers, and M.J. Roossinck. 2004. Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress. Proc. Natl. Acad. Sci. USA 101:15805–15810. doi:10.1073/pnas.0407094101 Yanez, M., S. Caceres, S. Orellana, A. Bastıas, I. Verdugo, S. RuizLara, and J.A. Casaretto. 2009. An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Rep. 28:1497–1507. doi:10.1007/s00299-009-0749-4 Yang, J.C., J.H. Zhang, K. Liu, Z.Q. Wang, and L.J. Liu. 2007. Involvement of polyamines in the drought resistance of rice. J. Exp. Bot. 58:1545–1555. doi:10.1093/jxb/erm032 Yi, S.H., A.Q. Sun, Y. Sun, J.Y. Yang, C.M. Zhao, and J. Liu. 2006. Differential regulation of Lehsp23.8 in tomato plants: Analysis

22

of a multiple stress-inducible promoter. Plant Sci. 171:398–407. doi:10.1016/j.plantsci.2006.04.011 Yi, S.Y., and J. Liu. 2009. Combinatorial interactions of two cisacting elements, AT-rich regions and HSEs, in the expression of tomato Lehsp23.8 upon heat and non-heat stresses. J. Plant Biol. 52:560–568. doi:10.1007/s12374-009-9072-4 Yu, C.H., H.S. Wang, S.H. Yang, X.F. Tang, M. Duan, and Q.W. Meng. 2009. Overexpression of endoplasmic reticulum omega-3 fatty acid desaturase gene improves chilling tolerance in tomato. Plant Physiol. Biochem. 47:1102–1112. doi:10.1016/j. plaphy.2009.07.008 Zhang, H.X., and E. Blumwald. 2001. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat. Biotechnol. 19:765–768. doi:10.1038/90824 Zhang, M., R. Barg, M. Yin, Y. Gueta-Dahan, A. Leikin-Frenkel, Y. Salts, S. Shabtai, and G. Ben-Hayyim. 2005. Modulated fatty acid desaturation via overexpression of two distinct omega-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J. 44:361–371. doi:10.1111/j.1365-313X.2005.02536.x Zhao, C., M. Shono, A. Sun, S. Yi, M. Li, and J. Liu. 2007. Constitutive expression of an endoplasmic reticulum small heat shock protein alleviates endoplasmic reticulum stress in transgenic tomato. J. Plant Physiol. 164:835–841. doi:10.1016/j. jplph.2006.06.004 Zhao, P., S. Chen, and X.C. Wang. 2006. Arabidopsis expansin AtEXP1 is involved in the regulation of stomatal movement. Acta Agron. Sin. 32:562–567. Zhou, S.F., X.Y. Chen, X.N. Xue, X.G. Zhang, and Y.X. Li. 2007. Physiological and growth responses of tomato progenies harboring the betaine aldehyde dehydrogenase gene to salt stress. J. Integr. Plant Biol. 49:628–637. doi:10.1111/j.17447909.2007.00464.x Zhu, J.K. 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53:247–273. doi:10.1146/annurev. arplant.53.091401.143329 Zhu, J.K., P.M. Hasegawa, and R.A. Bressan. 1997. Molecular aspects of osmotic stress in plants. Crit. Rev. Plant Sci. 16:253–277. Zijlstra, S., S.P.C. Groot, and J. Jansen. 1994. Genotypic variation of rootstocks for growth and production in cucumber; possibilities for improving the root system by plant breeding. Sci. Hortic. (Amsterdam) 56:185–196. doi:10.1016/0304-4238(94)90001-9

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