See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/257848482
The role of rhizobacteria in salinity effects on biochemical constituents of the halophyte Sesuvium portulacastrum Article in Russian Journal of Plant Physiology · January 2011 DOI: 10.1134/S1021443712010025
CITATIONS
READS
2
28
4 authors, including: Sivakumar Thirumal
Kathiresan Kandasamy
Annamalai University
Annamalai University
25 PUBLICATIONS 60 CITATIONS
298 PUBLICATIONS 5,826 CITATIONS
SEE PROFILE
SEE PROFILE
Some of the authors of this publication are also working on these related projects: Effect of mangroves on distribution, diversity and abundance of molluscs in mangrove ecosystem: A review View project I did my work and preparing research article. View project
All content following this page was uploaded by Sivakumar Thirumal on 11 June 2016.
The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document and are linked to publications on ResearchGate, letting you access and read them immediately.
ISSN 10214437, Russian Journal of Plant Physiology, 2012, Vol. 59, No. 1, pp. 115–119. © Pleiades Publishing, Ltd., 2012.
RESEARCH PAPERS
The Role of Rhizobacteria in Salinity Effects on Biochemical Constituents of the Halophyte Sesuvium portulacastrum1 R. Anburaj, M. A. Nabeel, T. Sivakumar, and K. Kathiresan Center of Advanced Study in Marine Biology, Annamalai University, Parangipettai, 608502, Tamil Nadu, India; fax: + 914144243555; email:
[email protected] Received June 23, 2010
Abstract—An experiment was conducted to understand the role of rhizospheric microorganisms in salinity effects on growth, antioxidants, pigments, and ion concentrations in the halophyte Sesuvium portulacastrum L. The plants grown in nonsterilized soil exhibited the enhanced growth rate, suppressed antioxidant enzymes, increased contents of chlorophylls and carotenoids, the greater accumulation of sodium and the reduction in the potassium ion concentration, as compared with the plants grown in microbefree soil. The dominant microbes identified from the rhizophere soil of nonsterilized plant groups included Bacillus cereus, Aeromo nas hydrophila, Pseudomonas aeruginosa, Corynebacterium xerosis, and Escherichia coli. The work emphasizes the importance of the rhizobacteria that colonize the root at the interface with soil in preventing the delete rious effects caused by salinity through accumulation of sodium and pigments and reduction of antioxidants and potassium. Keywords: Sesuvium portulacastrum, mangrove associate, halophyte, antioxidants, rhizobacteria, salinity. DOI: 10.1134/S1021443712010025 1
INTRODUCTION
Sesuvium portulacastrum belonging to the family Aizoaceae is a dicotyledonous facultative halophyte naturally growing in the subtropical, Mediterranean, coastal, and warmer zones of the world [1]. This plant has food and medicinal values and is also utilized as a wild vegetable, fodder crop for the cattle and domestic animals (goats, sheeps, and camels) and as bait in crab traps [2]. The plant has a remarkable ability to survive under stress conditions of salinity, drought, and heavy metal accumulation [1]. It is also considered as a pio neer species in the environmental protection, such as phytobioremediation sand dune fixation, desalina tion, desert greening, production of cheap biomass for renewable energy, climate improvement through CO2 sequestration, landscaping, and as an ornamental plant with its attractive pinkpurplish flowers [1–3]. Soil salinity is a growing problem due to a variety of natural and manmade factors. Seawater intrusion into coastal aquifers is one of the causes for salinity problems in coastal regions in almost all the regions of the world. One of the broad criteria for reclamation of saline soil is growing salttolerant wild plants in the arid and semiarid regions with the conventional crops, which can accumulate excessive amounts of salt from soil and will improve the fertility of soil. S. portu lacastrum is among the most appropriate species for the usage on saltaffected soils in arid and semiarid 1 This text was submitted by the authors in English.
regions. In India, it grows at the eastern and western coastal sides as a mangrove associate [1]. The soil bacteria growing at the soil–root interface, which are beneficial for the plants, are termed as plant growthpromoting rhizobacteria (PGPR). They are particularly important in controlling the chemical environment of the ecosystems, and they are also con sidered as the main primary producers, as well as being secondary producers and consumers. They perform different functions in the coastal ecosystems, such as photosynthesis, nitrogen fixation, and methanogene sis [3]. However, not many studies are currently avail able principally focusing on microbial aspects in rela tion to salt stress of S. portulacastrum. Hence, the present study was aimed at the study of the salinity induced changes in antioxidant and pigment contents, and also sodium and potassium uptake by the plant in relation to rhizobacterial presence. MATERIALS AND METHODS Study area and experimental plants. Sesuvium portulacastrum L. plants were collected freshly along with their habitat soil from Pichavaram mangrove for est (11°29′ to 11°30′N and 79°45′ to 79°55′E), south east coast of India. The plant materials were purified from rhizosphere soil; the roots were disinfected for 5 min in saturated calcium hypochlorite solution and rinsed thoroughly with distilled water. The rhizosphere soil samples were separately collected from the same
115
MRGR, cm/day
116 0.07 0.06 0.05 0.04 0.03 0.02 0.01 0
ANBURAJ et al. 1 2
Group I Group III Group V Group II Group IV Group VI Changes in mean relative growth rate of Sesuvium portula castrum during 30 (1) and 60 (2) days of experiment.
habitat. The plant materials and soil samples were transported in sterile polythene bags to the laboratory. Experimental groups. The healthy plants of appar ently uniform size were selected and maintained in the sterile polythene bag with rhizosphere soil. The entry of atmospheric microbes was blocked by closing the mouth of the bags. The plant stocks were separated into six different groups of soil treatments as follows: group I: nonsterilized rhizosphere soil watered with sterilized water; group II: sterilized rhizosphere soil watered with sterilized water; group III: nonsterilized rhizosphere soil watered with sterilized 50% seawater; group IV: sterilized rhizosphere soil watered with sterilized 50% seawater; group V: nonsterilized rhizosphere soil watered with sterilized 100% seawater; group VI: sterilized rhizosphere soil watered with sterilized 100% seawater. Each group consisted of five replicates. The exper imental plants were maintained under the natural sun light for a period of 60 days. Sterilized water was poured to plant stocks two times a day. The plants were analyzed for various parameters on the 60th day of experiment, except mean relative growth rate (RGR), which was measured on 30th and 60th days of experiment. For microbial analysis, a known weight of soil sam ple was aseptically removed from the roots using a ster ilized spatula. It was then transferred to a sterile coni cal 150ml flask containing 99 ml of sterile diluent, and serial dilution was performed to get 10−1, 10−2, 10−3, 10−4, and 10−5 suspension samples. The samples were used to isolate total Heterotrophic Bacteria by spread plate method on Zobell marine agar medium (Hi media, Mumbai) and enumerated as Colony Forming Units (CFU) per gram of the sample. The dominant bacteria present in the soil were identified by using biochemical and culture characteristics according to the Bergey’s Manual [4].
Concentrations of Na+ and K+ in leaf samples were determined using a flame photometer [5]. The total chlorophyll and carotenoids were extracted with ice cold 80% acetone from the leaves and estimated as described in [6]. Antioxidants, such as ascorbic acid [7], αtocopherol [8], reduced glutathione [9], super oxide dismutase [10], and ascorbate peroxidase [11] were also analyzed using standard procedures. Statistical analysis was carried out using SPSS ver sion 17.0. To test the statistical significance, twoway analysis of variance (ANOVA) was performed using Duncan’s Multiple Range Test (DMRT). RESULTS The relative growth rate varied significantly between the groups during 30 and 60 days of experi ment (P < 0.05) (figure). In general the nonsterilized plants showed the higher growth rates as compared with the sterilized plants. The increasing salinity also showed decreasing growth rates, and hence the lowest growth rate was observed when 100% seawater was applied. The total heterotrophic bacterial counts reduced from 10.5 to 1.9 CFU/g when seawater was treated to the soil. There was 3.75fold reduction in counts in soil treated with 50% seawater and 5.5fold reduction due to 100% seawater. Thus, salinity reduced the microbial counts in the soil. Microbes could not be enumerated in the sterilized soil throughout the exper iment (Table 1). The dominant microbes associated with rhizosphere soil were identified as Bacillus cereus, Aeromonas hydrophila, Pseudomonas aeruginosa, Corynebacterium xerosis, and Escherichia coli. The morphological and biochemical characteristics of the microbes used for identification are given in Table 2. There was a significant accumulation of Na+ in leaves of plants under nonsterile conditions as com pared to microbefree conditions. However, the trend was reverse in the case of K+ ion, since there was a reduction of K+ ion content under nonsterile condi tions. The accumulation of Na+ in leaves increased, while that of K+ ion decreased with increasing salinity. There was a significant increase in total chlorophylls and carotenoid pigments in the leaves of plants raised in nonsterilized soil than in sterilized soil. The total chlorophylls and carotenoids showed a decreasing trend with an increase in salinity. The levels of both enzymatic and nonenzymatic antioxidants increased in the leaves of plants growing in microbefree steril ized soil, but the nonsterilized soil resulted in a decreased antioxidant levels in plants. However anti oxidants manifested an increasing trend with an increase in salinity (Table 1). DISCUSSION Seawater intrusion into coastal ecosystems is one of the causes for salinity problems in almost all the
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
Vol. 59
No. 1
2012
THE ROLE OF RHIZOBACTERIA IN SALINITY EFFECTS ON BIOCHEMICAL
117
Table 1. Pigments, biochemical constituents, sodium and potassium ions in the leaves and microbial counts in soil of Sesu vium portulacastrum raised for 60 days in sterilized (S) and nonsterilized (NS) soil watered with freshwater, 50%, and 100% seawater 0% seawater
50% seawater
100% seawater
Variables NS Total heterotrophic bacteria in soil, CFU/g Total chlorophylls, mg/g fr wt Na+ content, mmol/kg fr wt K+ content, mmol/kg fr wt Carotenoids, μg/g fr wt Ascorbic acid, mg/g dry wt αTocopherol, mg/g dry wt Reduced glutathione, mg/g dry wt Superoxide dismutase, units/mg protein Ascorbate peroxidase, units/mg protein
S a
NS
b
0 10.5 ± 2.4 a 3.5 ± 0.6 0.9 ± 0.2b a 333 ± 29 124 ± 13b 123 ± 12a 194 ± 20b 133 ± 9a 54 ± 3b 1.31 ± 0.2a 1.9 ± 0.1b 5.1 ± 0.6a 5.9 ± 0.4a 0.77 ± 0.1a 0.85 ± 0.1b 0.61 ± 0.1a 0.79 ± 0.1b 0.85 ± 0.1a 1.17 ± 0.2b
S c
NS
b
S c
b
2.8 ± 0.8 0 1.9 ± 0.5 0 a b a 2.9 ± 0.7 0.7 ± 0.1 2.5 ± 0.5 0.5 ± 0.1b c b c 395 ± 32 179 ± 16 465 ± 35 225 ± 21d 115 ± 11a 279 ± 25c 105 ± 10a 229 ± 21b 95 ± 6c 47 ± 3b 65 ± 5b 25 ± 2d 1.72 ± 0.3b 2.3 ± 0.1c 1.8 ± 0.2b 2.3 ± 0.3c 7.1 ± 0.7b 7.8 ± 0.5b 7.8 ± 0.7b 8.5 ± 0.9c 0.89 ± 0.1b 1.0 ± 0.1c 0.9 ± 0.1b 1.0 ± 0.2c 0.81 ± 0.1b 0.89 ± 0.1c 0.92 ± 0.2c 0.96 ± 0.2c 1.42 ± 0.1c 1.89 ± 0.3d 1.29 ± 0.1b 1.38 ± 0.2c
Notes: Values are means ± SD; values in the same row not sharing a common superscript differ significantly between the groups (p < 0.05).
Table 2. Morphological, culture and biochemical characteristics of the identified microbes Organism Gram stain Lactose Dextrose Sucrose H2S production NO3 reduction Indole production Methyl Red reaction Voges Proskauer reaction Citrate use Urease activity Catalase activity Oxidase activity Gelatin liquefaction Starch hydrolysis Lipid hydrolysis
Ah
Bc
Cx
Ec
Pa
–Rod
+Rod
+Rod
–Rod
–Rod
± + ± + + + ± +
–
±
– –
+ + + + –
–
–
A± A±
AG AG A±
–
A A –
–
–
–
+
+ – –
+ + +
+
–
–
–
–
–
–
–
+
–
–
–
–
+
+
+
–
–
–
+, fast + ±
–
–
+ + +
–
–
–
–
–
+
– –
– –
Notes: A—acid production; AG—acid and gas production; ±—variable; A h—Aeromonas hydrophila; B c—Bacillus cereu; C x— Corynebacterium xerosis; E c—Escherichia coli; and P a—Pseudomonas aeruginosa.
regions of the world. Soil salinity limits plant growth and crop production in many parts of the world, par ticularly in arid and semiarid areas. The only plants that can survive under these conditions are halophytes. The increased research on the halophytic species, which have an economic utilization, may enable the restoration of saltaffected lands given that the appro priate soil and irrigation management are applied. The present study is focused on a halophyte species RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
Vol. 59
S. portulacastrum, an important pioneer species on sandy beaches in the subtropical and tropical regions of the world. It is having a matforming growth habit promoting embryonic sand dune formation in belts parallel to the shoreline. It has been earlier proved that S. portulacastrum is able to express the high growth potential, even under severe salinity [12]. However, in the present experiments, the lowest growth rate was observed when 100% seawater was applied (figure). No. 1
2012
118
ANBURAJ et al.
Maas [13] reported that, in most halophytic species, growth decreased gradually with the increase in salt concentration in the culture medium above a critical threshold one specific to each species. The low NaCl concentrations stimulated growth of halophytic spe cies, but an excess of salt decreased growth and biom ass production [14]. However, the soil with microbial strains improved plant biochemical potential under soil salinity conditions. A similar observation has been made by Han and Lee [15]. Na+ and Cl− – are the most abundant ions in the plants, and their concentrations increase with the increase of seawater concentration. In our experi ments, Na+ accumulated with increasing NaCl con centrations in all the treatments as compared to the control plants. However, K+ ion reduced and thus exhibited a reverse trend to that of Na+. This response of halophytes reflects the utilization of ions for osmotic adjustment, a process in which Na+ can be much more suitable than K+ since the halophyte accu mulates it preferentially in the vacuoles [16]. Interest ingly, even at the 0% saline, plants (groups I and II) accumulated NaCl to maintain normal growth. The Na+ presence in 0% saline plants might be because they have already been accumulated it prior to the beginning of experiment. The reported accumulation of ions in the leaves of S. portulacastrum is in agree ment with the experiments using other halophytic spe cies [14, 17]. In this study, growth reduction at high salinity was noted, which may be due to nutritional disruption by salt. Since the S. portulacastrum is a true halophyte, it requires saline soil because the excess of salt may affect biochemical characters. However, this view must be investigated in detail. The rhizosphere is defined as the zone, over which the growth and activity of soil microbes are influenced by nutrients derived from a living root. This region is a favorable habitat for the proliferation and metabolism of numerous types of microorganisms [18]. The reason is that microbial growth and activity are enhanced in the rhizosphere, as compared to the rootfree soil, and that microbial growth substrates from the growing plant root are continuously released by exudation, secretion, and from dead cells by autolysis. The rhizo bacteria can actively colonize plant roots and prevent the deleterious effects of phytopathogenic organisms by producing several siderophores and antibacterial peptides that inhibit pathogens [19]. They also pro duce several growthpromoting compounds, includ ing phytohormones (auxins, cytokinins, and gibberel lins) [18]. It has been shown that plants respond to rather unconventional bacterial signals, such as quo rum sensing molecules and volatile compounds. Some microbes stimulate plant growth by reduction of toxic ion uptake, increases in auxin contents, and formation of stressspecific proteins in plants under stress caused by the toxic ions [18]. In the present study, the plants raised in microberich soil showed significant bio
chemical changes, as compared to microbefree soil, in response to increasing salinity. The levels of total chlorophylls and carotenoids showed a trend of a decrease with increasing salinity in all plant groups. These results are supported by the previous studies showing changes in physiological processes in plants in response to salinity and many other stress factors [20]. Data relating to the effect of salinity on the primary photochemical reactions under in vivo conditions, however, are limited and conflict ing. Salinitycaused reduction in the net photosyn thetic rate is attributed to the reduced stomatal con ductance and/or to reduction in the capacity of pho tosynthetic machinery [21]. The decreased chlorophyll content can also be attributed to the fact that salt stress decreases total chlorophyll content by increasing the activity of chlorophylldegrading chlo rophyllase, inducing the destruction of chloroplast structure and the instability of pigment–protein com plexes [22]. The nonsterilized plants contained more chlorophylls and carotenoids than the sterilized plants did. This indicates the role of microbes in mitigating the reduction of pigments due to salinity stress. In sup port of this, Vivas et al. [23] reported increased chlo rophyll in Lactuca sativa plants inoculated with Bacil lus sp. from its soil. It is assumed that survival of plants in saline envi ronment depends upon the biochemical alterations and on the quantitative ratio between toxic and pro tective compounds [24]. A number of mechanisms are used by halophytes to achieve osmotic adjustment, including inorganic ion accumulation and synthesis or accumulation of organic compounds to prevent water loss. The levels of antioxidant enzymes are usually enhanced during salinity stress, and hence antioxidant concentrations are used as indicators of oxidative stress in plants. Reactive oxygen species cause oxida tive damage to biomolecules, such as lipids and pro teins and eventually lead to cell death [25]. To protect against oxidative stress, plant cells produce both anti oxidant enzymes, such as superoxide dismutase, per oxidase, and catalase, and nonenzymatic antioxi dants, such as ascorbate, glutathione, and tocopherol [24, 25]. The results of the present study revealed that increasing salinity stress significantly increased anti oxidant levels. It is interesting to note that microbial strains tended to reduce the salinity stress effect on the activity of antioxidants. A similar observation was noticed by Han and Lee [15] with strains of Serratia sp. and Rhizobium sp. in Lactuca sativa. The present study thus experimentally proved the role of microbes in reducing the effects of salinity stress in the halophyte, S. portulacastrum. The domi nant microbes present in the rhizosphere soil, such as Bacillus cereus, Aeromonas hydrophila, Pseudomonas aeruginosa, Corynebacterium xerosis, and E. coli were found. The decreased growth, the fall in the chloro phyll and carotenoid contents, oxidative stress, plant ion status changes in the plants that are grown in ster
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
Vol. 59
No. 1
2012
THE ROLE OF RHIZOBACTERIA IN SALINITY EFFECTS ON BIOCHEMICAL
ile soil under various salinity conditions were observed. However, it is necessary to delineate the changes caused by either stresses (salt and/or microbes). Much more detailed investigation is war ranted in order to elucidate the role of each microbe during salinity stress. ACKNOWLEDGMENTS The authors are thankful to Prof. T. Balasubrama nian, Director of this center, and authorities of Anna malai University for providing facilities.
12.
13.
14. 15.
REFERENCES 1. Lokhande, V.H., Tukaram, D.N., and Penna, S., Sesu vium portulacastrum (L.) a Promising Halophyte: Cul tivation, Utilization and Distribution in India, Genet. Resour. Crop EV, 2009, vol. 56, pp. 741–747. 2. Anonymous, Greenhouse Care for Transgenic Maize Plants, Iowa State University, Plant Transformation Facilit., 2009. 3. Rabhi, M., Giuntini, D., Castagna, A., Remorini, D., Baldan, B., Smaoui, A., Abdelly, C., and Ranieri, A., Sesuvium portulacastrum Maintains Adequate Gas Exchange, Pigment Composition, and Thylakoid Pro teins under Moderate and High Salinity, J. Plant Phys iol., 2010, vol. 167, pp. 1336–1341. 4. Buchanan, R.E. and Gibbons, N.E., Bergey’s Manual of Determinative Bacteriology, Baltmore: Williams and Wilkins, 1974. 5. Kingston, H.S., Microwave Assisted Acid Digestion of Sediments, Sludges, Soils and Oils: EPA Method 3051, Pittsburg, USA: Duquesne University, 1994. 6. Arnon, D.I., Copper Enzymes in Isolated Chloroplasts. Polyphenoloxidases in Beta cularis, Plant Physiol., 1949, vol. 24, pp. 1–15. 7. Omaye, S.T., Turnbull, J.D., and Souberlich, H.E., Selected methods for Determination of Ascorbic Acid in Animal Cells, Tissues and Fluids, Methods in Enzy mology, Mc. Cormick, D.B. and Wright, L.D., Eds., New York: Academic, 1979, pp. 3–47. 8. Baker, H.O., Frank, B., de Angelis, B., and Feingold, S., Plasma Alpha Tocopherol in Man at Various Times after Ingesting Free or Acetylated Tocopherol, Nutr. Rep. Int., 1980, vol. 21, pp. 531–536. 9. Moron, M.A., Depierre, J.W., and Mannervick, B., Levels of Glutathione, Glutathione Reductase and Glutathione STransferase Activities in Rat Lung and Liver, Biochim. Biophys. Acta, 1979, vol. 582, pp. 67–78. 10. Hwang, C.S., Rhie, G.E., Kim, S.T., Kim, Y.R., Huh, W.K., Baek, Y.U., and Kang, S.O., Copper and Zinc Containing Superoxide Dismutase and Its Gene from Candida albicans, Biochim. Biophys. Acta, 1999, vol. 1427, pp. 245–255. 11. Chen, G. and Asada, K., Ascorbate Peroxidase in Tea Leaves: Occurrence of Two Isozymes and Differences
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
View publication stats
Vol. 59
16.
17.
18. 19. 20.
21.
22.
23.
24.
25.
119
in Their Enzymatic and Molecular Properties, Plant Cell Physiol., 1989, vol. 30, pp. 987–992. Messedi, D., Sleimi, N., and Abdelly, C., Some Physi ological and Biochemical Aspects of Salt Tolerance in Sesuvium portulacastrum, Cash Crop Halophytes: Recent Studies Ten Years after El Ain Meeting, Lieth, H., Ed., Dordrecht: Kluwer, 2003, pp. 71–78. Maas, E.V., Salt Tolerance of Plants, CRC Handbook of Plant Sciences in Agriculture, Christie, B.R., Ed., 1987, vol. 2, pp. 57–75. Flowers, T.J., Physiology of Halophytes, Plant Soil, 1985, vol. 89, p. 41. Han, H.S. and Lee, K., Plant Growth Promoting Rhizobacteria: Effect on Antioxidant Status, Photo synthesis, Minerals Uptake and Growth of Lettuce under Soil Salinity, Res. J. Agric. Biol. Sci., 2005, vol. 1, pp. 210–215. Flowers, T.J. and Laushli, A., Sodium versus Potas sium: Substitution and Compartmentation, Encyclope dia of Plant Physiology, New Ser., vol. 15 B, Inorganic Plant Nutrition, Lauchli, A. and Bieleski, R.L., Eds., Berlin: SpringerVerlag, 1983, pp. 651–681. Kefu, Z., Hai, F., San, Z., and Jie, S., Study on the Salt and Drought Tolerance of Suaeda salsa and Kalanchoe claigeremontiana under IsoOsmotic Salt and Water Stress, Plant Sci., 2003, vol. 165, pp. 837–844. Alexander, M., Introduction to Soil Microbiology, New Delhi: Wiley, 1987. Mittler, R., Oxidative Stress, Antioxidants and Stress Tolerance, Trends Plant Sci., 2002, vol. 7, pp. 405–410. Younis, M.E., Hasaneen, M.A., Ahmed, A.R., and El Bialy, D.A., Plant Growth, Metabolism and Adaptation in Relation to Stress Conditions. XXI. Reversal of Harmful NaClEffects in Lettuce Plants by Foliar Application with Urea, Aust. J. Crop Sci., 2008, vol. 2, pp. 83–95. Seeman, J.R. and Sharkey, T.D., Salinity and Nitrogen Effects on Photosynthesis, Ribulose1,5Bisphosphate Carboxylase and Metabolite Pool Sizes in Phaseolus vulgaris L., Plant Physiol., 1986, vol. 82, pp. 555–560. Singh, A.K. and Dubey, R.S., Changes in Chlorophyll a and b Contents and Activities of Photosystems 1 and 2 in Rice Seedlings Induced by NaCl, Photosynthetica, 1995, vol. 31, pp. 489–499. Vivas, A., Marulanda, A., RuizLozano, J.M., Barea, J.M., and Azcon, R., Influence of a Bacillus sp. on Physiological Activities of Two Arbuscular Mycorrhizal Fungi and on Plant Responses to PEGInduced Drought Stress, Mycorrhiza, 2003, vol. 13, pp. 249–256. Shalata, A. and Tal, M., The Effect of Salt Stress on Lipid Peroxidation and Antioxidants in the Leaf of the Cultivated Tomato and Its Wild SaltTolerant Relative Lycopersicon pennellii, Physiol. Plant., 1998, vol. 104, pp. 169–174. Mittler, R., Oxidative Stress, Antioxidants and Stress Tolerance, Trends Plant Sci., 2002, vol. 7, pp. 405–410.
No. 1
2012
