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Chapter 9

Efficiency of Phytohormone-Producing Pseudomonas to Improve Salt Stress Tolerance in Jew’s Mallow (Corchorus olitorius L.) Dilfuza Egamberdieva and Dilfuza Jabborova

9.1

Introduction

Natural salinity is the result of a long-term natural accumulation of salts in the soil or in surface water, and it is estimated that 33 % of the potentially arable land area of the world is affected by salinity (Ondrasek et al. 2009). Climate change will even increase soil salinity further, since it is accompanied by less rainfall and higher temperatures (Othman et al. 2006). Many studies have demonstrated that salinity inhibits seed germination and growth of various agriculturally important crops, vegetables, and also medicinally important plants (Teixeira da Silva and Egamberdieva 2013; Egamberdieva et al. 2011, 2013a; Jamil et al. 2006; Xu et al. 2011; Khodarahmpour et al. 2012). In aromatic and medicinal plants, growth and synthesis of biological active compounds are influenced by various environmental factors such as salinity, drought, and water stresses (Hasegawa et al. 2000; Parida and Das 2005). Soil salinity inhibits plant growth and the development of Satureja hortensis and Eragrostis curvula (Colom and Vazzana 2002; Baher et al. 2002), Citronella (Kumar and Gill 1995), Ammolei majus, and Hyoscyamus niger (Ashraf 2004). Several explanations for these effects have been proposed, such as inhibition of the activity of enzymes involved in nucleic acid metabolism (Arbona et al. 2005) and inhibition of biosynthesis of plant hormones within plant tissues (Prakash and Parthapasenan 1990). Debez et al. (2001) observed that salt stress caused by NaCl inhibited the endogenous levels of phytohormones such as gibberellins, abscisic acid, jasmonic acid, and salicylic acid in plants, which correlated with a reduction of root growth in salt bush (Atriplex halimus L.). In other study, Figueiredo et al. (2008) reported decreased levels of auxins and gibberellins in the roots of common beans. D. Egamberdieva (*) • D. Jabborova Department of Biotechnology and Microbiology, National University of Uzbekistan, University str. 1, Tashkent 100174, Uzbekistan e-mail: [email protected] © Springer International Publishing Switzerland 2015 D. Egamberdieva et al. (eds.), Plant-Growth-Promoting Rhizobacteria (PGPR) and Medicinal Plants, Soil Biology 42, DOI 10.1007/978-3-319-13401-7_9

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Jew’s mallow is, in the tropics and sub-tropics, among the most common plants that thrive nearly anywhere including Middle East, Asia and Africa. The plant is used as food ingredient, herb, and vegetable, and contains acidic polysaccharides, proteins, calcium, thiamin, riboflavin, and dietary fibers (Leung et al. 1968; Tsukui et al. 2004). C. olitorius is mostly distributed in arid and stress environment (Fawusi et al. 1984; Chaudhuri and Choudhuri 1997). However its production is reduced by high salinity and poor soil conditions (Velempini et al. 2003). It has been reported that the plant growth and yield of jew’s mallow could be improved by Arbuscular mycorrhizal (AM) fungi (Nwangburuka et al. 2012). It has been proposed that the external supply of plant growth regulators produced by root-associated microorganisms under stressed conditions may help plants to cope with abiotic stress (Li et al. 2005). Most of the root-associated bacteria produce phytohormones such as IAA, GA, abscisic acids, and cytokinins (Egamberdieva et al. 2001, 2004; Egamberdieva and Hoflich 2002; Lyan et al. 2013; Jabborova et al. 2013a; Matiru and Dakora 2004; Hayat et al. 2008). The abilities of PGPR strains to produce plant growth regulators could balance the decrease in the phytohormone levels of the plant roots and alleviate salt stress in plants (Egamberdieva 2009, 2013). The ameliorative effects of PGPR on plant growth under saline conditions have been shown on various plant species, including medicinally important plants (Yildirim and Taylor 2005; Egamberdieva and Lugtenberg 2014). For example, Pseudomonas strains alleviated the salinity effects on the growth of basil (Ocimum basilicum) (Golpayegani and Tilebeni 2011), goats rue (Galega officinalis L.), and milk thistle (Silybum marianum) (Egamberdieva et al. 2013a). This study was conducted to evaluate the effectiveness of phytohormoneproducing Pseudomonas strain and plant growth regulators such as auxins and gibberellins in improving growth and salt tolerance of jew’s mallow (Corchorus olitorius L.) under saline conditions.

9.2 9.2.1

Materials and Methods Plant and Bacteria

The seeds of jew’s mallow (Corchorus olitorius L.) were obtained from the Department of Botany, Faculty of Biology and Soil Sciences of Uzbekistan. Seeds were sorted to eliminate broken, small, and infected seeds. Seeds were surface-sterilized by immersing them for 1 min in concentrated 10 % v/v NaOCl, followed by 3 min in 70 % ethanol, and rinsed five times with sterile, distilled water. The sterility of seeds was tested on Nutrient agar by incubating plates for 3 days at 28 C. The salt-tolerant bacterial strain Pseudomonas extremorientalis TSAU6, which produces IAA under saline conditions (7.4 μg/ml) and GA (0.4 μg/ml) was obtained from the culture collection of National University of Uzbekistan. The strain

9 Efficiency of Phytohormone-Producing Pseudomonas to Improve Salt. . .

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Pseudomonas fluorescens WCS365, which doesn’t produce IAA, was obtained from the culture collection of Leiden University of the Netherlands.

9.2.2

Germination and Seedling Growth

Seed germination was carried out in 85 mm 15 mm tight fitting plastic petri dishes with 5 ml solution consisting of 0 and 100 mM NaCl. Ten healthy and uniform seeds were sown in each petri plate with three replicates. A filter paper (Whatman No. 2) was soaked in a solution of the respective salt concentrations. To determine the effects of plant growth regulators on seed germination and seedling growth, auxins (IAA) and gibberellic acid (GA) were used at 1 and 0.1 and 0.01 and 0.001 μM concentrations under nonsaline and saline (100 mM NaCl) conditions. Bacterial strains Pseudomonas fluorescens WCS365 and Pseudomonas extremorientalis TSAU6 were grown overnight in KB broth. 1 ml of each culture was pelleted by centrifugation, and the supernatant was discarded. Cell pellets were washed with 1 ml phosphate buffered saline (PBS, 20 mM sodium phosphate, 150 mM NaCl, pH 7.4) and suspended in PBS. Cell suspensions were diluted to an optical density of 0.1 at 620 nm, corresponding to a cell density of 108 cells/ml. Seeds were placed in the bacterial suspension using sterile forceps and shaken gently for a few seconds. After 10 min, the inoculated seeds were then aseptically placed into petri dishes moistened with water, with 100 mM NaCl solution. All germinations were carried out in a plant growth chamber at 28 C. The lengths of roots and shoots of the germinated seeds which were more than 0.2 mm in length were measured and recorded after 5 days.

9.2.3

Plant Growth in Gnotobiotic Sand Tubes

The effect of seed inoculation with IAA- and GA-producing Pseudomonas extremorientalis TSAU6 and Pseudomonas fluorescens WCS365 on the growth of jew’s mallow seedlings exposed to salt stress (100 mM NaCl) was studied under gnotobiotic conditions. Experiments were carried out in test tubes (25 mm in diameter, 200 mm in length) as described by Simons et al. (1996). The tubes contained 60 g of sterilized high-quality sand (quartz sand 0.1–0.3 mm), which was treated with 10 % Plant Nutrient Solution (PNS) (Kuiper et al. 2001). Salinity conditions were established by adding 100 mM NaCl into the nutrient solution. Bacterial inoculants were grown and prepared, and the sterilized seeds were inoculated as described above. Inoculated seeds were planted into sterile glass tubes, one seed per tube with three replicates. The seedlings were grown in a growth cabinet with a 16-h light period at 22 C and an 8-h dark period at 16 C. At harvest after 18 days, the length of the shoots and roots and the fresh weight of whole plants were measured.

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9.2.4


Plant Growth in Saline Soils

The effect of Pseudomonas strain on plant growth of jew’s mallow under saline soil conditions was conducted in plastic pots (12-cm diameter, 15-cm deep). The soil has an EC value of 685 mS m1 and contains 43 9 g sand/kg, 708 12 g silt/kg, and 249 13 g clay/kg. The organic matter content of the soil is 0.694 %; total N, 0.091 %; Ca, 63.5 g/kg; Mg, 20.7 g/kg; K, 6.2 g/kg; P, 1.2 g/kg; Cl, 0.1 g/kg; and Na, 0.7 g/kg, and the pH is 8.0. The plant seeds were sterilized, allowed to germinate, and coated with bacteria as described above, and the inoculated seedlings were planted in the plastic pots. The inoculation treatments were set up in a randomized design with ten replications. The pot experiment had two treatments: seeds noninoculated with bacteria, and the seeds inoculated with bacteria. Plants were grown at 19–22 C during the day and 10–11 C at night, and after 8 weeks the shoot and root length and dry matter of jew’s mallow were measured.

9.2.5

Statistical Analysis

Data were tested for statistical significance using the analysis of variance package included in Microsoft Excel 2007. Mean comparisons were conducted using a least significant difference (LSD) test (P < 0.05). Standard error and an LSD result were recorded.

9.3 9.3.1

Results and Discussions Microbial Plant Growth Stimulation

Seed germination is usually the most critical stage in seedling establishment (Almansouri et al. 2001). In this study, salinity (100 mM NaCl) inhibited the germination of jew’s mallow seeds by 30 %. Salt-exposed plants exhibited a reduction in shoot and root growth and biomass compared to control plants. NaCl reduced root length by 25 %, shoot length by 20 %, and plant’s fresh weight by 25 %. The present result agrees with the work of Gandour (2002) and Vadez et al. (2007) where they observed decreases in percentage germination and seedling emergence of chickpea with increases in salinity. Atak et al. (2006) and Neamatollahi et al. (2009) pointed out that higher saline condition may reduce germination percentage due to higher osmotic pressures. Ashraf (2004) found that increasing salt concentrations caused a significant reduction in the shoot and root growth as well as seed yield of Ammolei majus and Hyoscyamus niger. Similar results were observed by Razmjoo et al. (2008), where increased salinity and


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drought stress caused reduction in the fresh and dry flower weight and essential oil content of Matricaria chamomila. It has been reported that salinity reduces the recovery of diffusible auxins from maize coleoptile tips (Itai et al. 1968). It has been suggested that plants might benefit from external supply of plant growth regulators under stressed conditions (Li et al. 2005). The root-associated bacteria which produce various phytohormones such as auxins, gibberellins, and cytokinins may help plants to cope with salt stress (Egamberdieva and Tulyasheva 2007; Yue et al. 2007; Egamberdieva et al. 2012). In this study, bacterial strains which produce IAA and GA were also able to alleviate salt stress in plants and improve seed germination of jew’s mallow (up to 90 %). They also did reverse the growth-inhibiting effect of salt stress to a certain extent in both shoot and root. The IAA-producing strain P. extremorientalis TSAU6 significantly improved root length (66 %), shoot length (43 %), and fresh weight of plants (11 %) under nonsaline conditions, whereas strain P. fluorescens WCS365, which doesn’t produce IAA, stimulated root and shoot length and fresh weight by 8, 25, and 6 %, respectively (Fig. 9.1a, c). The inoculated jew’s mallow seeds with P. extremorientalis TSAU6 significantly increased jew’s mallow seedling root growth up to 45 % and shoot growth up to 84 % at 100 mM NaCl compared to control plants (Fig. 9.1b, c). The strain P. fluorescens WCS365 was not able to stimulate plant growth under salt stress conditions. There are many reports on the role of phytohormones in changes of root morphology exposed to drought, salinity, temperature, and heavy metal toxicity (Spaepen et al. 2008; Spaepen and Vanderleyden 2010). In our previous works, we have observed that IAA-producing root-associated bacteria increase root growth, development, and yield of various agricultural crops such as soybean, cotton, wheat, maize, cucumber, and pea (Egamberdieva and Hoflich 2003; Jabborova et al. 2013b; Berg et al. 2010; Egamberdieva and Jabborova 2012, 2013a, b). These results agree with Heidari et al. (2011) who reported that the plant growth and auxin and protein contents of Ocimum basilicum inoculated by Pseudomonas sp. under drought stress conditions were increased compared to the control. Those reports demonstrated that phytohormones play a major role in improving plant growth and development under saline conditions.

9.3.2

The Effect of Phytohormones on Plant Growth

We also determined the effect of individual phytohormones such as auxins and gibberellins on the plant growth of jew’s mallow and development under saline conditions. We observed that seed dormancy enforced by salinity was substantially alleviated and germination was promoted by gibberellins and auxins from 80 to 95 % (data not shown). This finding agrees with other studies in which GA and IAA improved the emergence of rice (Wahyuni et al. 2003), wheat seedlings (Egamberdieva 2009), radishes (Egamberdieva 2008), brinjal (Solanum melongena L.) (Gupta 1971),

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Fig. 9.1 Effect of inoculation of jew’s mallow (Corchorus olitorius L.) seedlings with Pseudomonas extremorientalis TSAU6 (produce IAA and GA) and Pseudomonas fluorescens WCS365 (doesn’t produce IAA and GA) on (a) length of roots, (b) length of shoots, and (c) fresh weight of whole plants. The seedlings were grown in petri plates with 0 mM and 100 mM NaCl solution. Columns represent means for five seedlings (N ¼ 5) with error bars showing standard error. Columns with different letters indicate significant differences between treatments at P < 0.05 (Tukey’s t-test)


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chayote (Sechium edule) (Gregorio et al. 1995), and red sanders (Pterocarpus santalinus Linn. F) (Naidu 2001). In previous works, several plant growth regulators such as gibberellins (Afzal et al. 2005), auxins (Khan et al. 2004), and cytokinins (Gul et al. 2000) have been shown to alleviate salinity stress in plants. All concentrations of IAA and GA showed stimulatory effect on the root and shoot growth of jew’s mallow seedling under nonsaline and salt stress conditions (Fig. 9.2a–c).


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Fig. 9.2 The effect of various concentrations of IAA on the seedling growth of jew’s mallow (Corchorus olitorius L.): (a) length of roots, (b) length of shoots, and (c) fresh weight of whole plants. The seedlings were grown in petri plates with 0 mM and 100 mM NaCl solution. Columns represent means for five seedlings (N ¼ 5) with error bars showing standard error. Columns with different letters indicate significant differences between treatments at P < 0.05 (Tukey’s t-test)

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We have also observed that GA stimulated the root and/or shoot growth of jew’s mallow seedling at concentrations 0.1, 0.01, and 0,001 mM under nonsaline and saline conditions (Fig. 9.3a–c). Lin and Kao (1995) reported that the application of growth regulators such as GA3 and cytokinin on rice seedlings improved seedling growth. Similar results were observed by Gul et al. (2000), where gibberellic acid and zeatin alleviate the effect of salinity on germination and growth of Ceratoides lanata, Salicornia pacifica, and Allenrolfea occidentalis (Khan et al. 2004). Under both nonsaline and saline conditions, lower concentrations of GA (0.1, 0.01, and 0.001 mM) showed higher stimulatory effect compared to control plants. Similar findings were reported by Remans et al. (2007), where low concentration of pure IAA or low titer of IAA-producing bacteria enhanced root growth. Javid et al. (2011) reviewed the importance of IAA, cytokinins, and gibberellic acid in ameliorating salt stress in various plants. It is also suggested that IAA enhanced different cellular defense systems for protecting plants from external abiotic stresses (Bianco and Defez 2010).

9.3.3

Plant Growth in Gnotobiotic Sand System and Saline Soil

The growth-promoting effect of IAA- and GA-producing P. extremorientalis TSAU6 strain was also studied by growing inoculated salt-stressed jew’s mallow seedlings for 18 days in a gnotobiotic sand system and 8 weeks in pots with saline soil. The presence of NaCl clearly impaired the plant growth of jew’s mallow seedlings. At 100 mM, the length of root, length of shoot, and fresh weight of whole plants were inhibited by 54, 59, and 45 % than those of nonstressed seedlings. The coinoculation of salt-stressed jew’s mallow exposed to 100 mM NaCl with P. extremorientalis TSAU6 significantly improved fresh weight of plants (on average by 35 %), length of shoots (by 42 %), and length of roots (by 50 %). Also under nonstressed conditions, the addition of Pseudomonas strain significantly enhanced root and shoot growth compared to uninoculated control plants. Plant growth-promoting properties of the strain in pot experiments with saline soil showed that P. extremorientalis TSAU6 significantly increased shoot length by 21 % and dry matter by 18 % (data not shown). These results were somewhat similar to those obtained by Golpayegani and Tilebeni (2011) in which salinity decreased plant growth, photosynthesis, and chlorophyll content of basil, whereas Pseudomonas sp. alleviated the effects of salinity on plant growth. In our previous work, we have also observed that IAA-producing Pseudomonas strains promoted the enlargement of root system, enhancing nutrient uptake, and growth of goat’s rue (Galega officinalis) (Egamberdieva et al. 2013a) and milk thistle (Silybum marianum) (Egamberdieva et al. 2013b) grown in a salt-affected soil. Similar observations were reported by other authors in which Pseudomonas fluorescens stimulated the growth and yield of Catharanthus roseus under drought stress (Attia


a 6.0

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Fig. 9.3 The effect of various concentrations of GA on the seedling growth of jew’s mallow (Corchorus olitorius L.): (a) length of roots, (b) length of shoots, and (c) fresh weight of whole plants. The seedlings were grown in petri plates with 0 mM and 100 mM NaCl solution. Columns represent means for five seedlings (N ¼ 5) with error bars showing standard error. Columns with different letters indicate significant differences between treatments at P < 0.05 (Tukey’s t-test)

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and Saad 2001; Jaleel et al. 2007). Karthikeyan et al. (2010) reported that PGPR strains Pseudomonas significantly increased plant height, root length, root girth, and alkaloid content in Madagascar periwinkle (Catharanthus roseus) relative to the control.

9.4

Conclusions

The results presented here make it possible to recommend root-colonizing, phytohormone-producing P. extremorientalis TSAU to improve the growth of jew’s mallow under saline soil conditions. It is also indicated that plant growth regulators, such as auxins and gibberellins, considerably alleviated salinity stress in plants and stimulated their growth and development.

References Afzal I, Basra S, Iqbal A (2005) The effect of seed soaking with plant growth regulators on seedling vigor of wheat under salinity stress. J Stress Physiol Biochem 1:6–14 Almansouri M, Kinet JM, Lutts S (2001) Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant Soil 231:243–254 Arbona V, Marco AJ, Iglesias DJ, Lopez-Climent MF, Talon M, Gomez-Cadenas A (2005) Carbohydrate depletion in roots and leaves of salt-stressed potted Citrus clementina L. Plant Growth Regul 46:153–160 Ashraf M (2004) Photosynthetic capacity and ion accumulation in a medicinal plant henbane (Hyoscyamus niger L.) under salt stress. J Appl Bot 78:91–96 Atak M, Kaya MD, Kaya G, Çıkılı Y, Çiftçi CY (2006) Effects of NaCl on the germination, seedling growth and water uptake of triticale. Turk J Agric For 30:39–47 Attia FA, Saad OAO (2001) Biofertilizers as potential alternative of chemical fertilizer for Catharanthus roseus G. Don. J Agric Sci 26:7193–7208 Baher ZF, Mirza M, Ghorbanli M, Rezaii MB (2002) The influence of water stress on plant height, herbal and essential oil yield and composition in Satureja hortansis L. Flavour Fragrance J 17:275–277 Berg G, Egamberdieva D, Lugtenberg B, Hagemann M (2010) Symbiotic plant-microbe interactions: stress protection, plant growth promotion and biocontrol by Stenotrophomonas. In: Seckbach J, Grube M (eds) “Symbioses and Stress”, cellular origin, life in extreme habitats and astrobiology, vol 17. Springer, Berlin, pp 445–460 Bianco C, Defez R (2010) Improvement of phosphate solubilization and Medicago plant yield by an indole-3-acetic acid-overproducing strain of Sinorhizobium meliloti. Appl Environ Microbiol 76:4626–4632 Chaudhuri K, Choudhuri MA (1997) Effect of short-term NaCl stress on water relations and gas exchange of two jute species. Biol Plant 40:373–380 Colom MR, Vazzana C (2002) Water stress effects on three cultivars of Eragrostis curvula. Italy J Agron 6:127–132 Debez A, Chaibi W, Bouzid S (2001) Effect du NaCl et de regulatoeurs de croissance sur la germination d’ Atriplex halimus L. Cahiers Agric 10:135–138 Egamberdieva D (2008) Alleviation of salinity stress in radishes with phytohormone producing rhizobacteria. J Biotechnol 136:262


211

Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864 Egamberdieva D (2013) The role of phytohormone producing bacteria in alleviating salt stress in crop plants. In: Miransari M (ed) Biotechnological techniques of stress tolerance in plants. Studium, Houston, TX, pp 21–39 Egamberdieva D, Hoflich G (2002) Root colonization and growth promotion of winter wheat and pea by Cellulomonas spp. at different temperatures. J Plant Growth Regul 38:219–224 Egamberdieva D, Hoflich G (2003) The effect of associative bacteria from different climates on plant growth of pea at different soils and temperatures. Arch Agron Soil Sci 49:203–213 Egamberdieva D, Jabborova D (2012) The use of plant growth promoting bacteria for improvement plant growth of wheat, maize and cotton in serosem soil. Uzb Biol J 2:51–54 Egamberdieva D, Jabborova D (2013a) Improvement of cotton production in arid saline soils by beneficial microbes. In: Huang L, Zhao Q (eds) Crop yields: production, management practices and impact of climate change. Nova, New York, pp 109–122 Egamberdieva D, Jabborova D (2013b) Diversity and physiological characterization of root associated bacteria of cotton. Uzb Biol J 2:50–53 Egamberdieva D, Lugtenberg B (2014) PGPR to alleviate salinity stress on plant growth. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses, vol 1. Springer, New York, pp 73–96 Egamberdieva D, Tulyasheva Z (2007) IAA producing salt tolerant bacteria: its stimulatory effect on celery in nutrient poor arid soils. Uzb J Agric Sci 3:65–69 Egamberdieva D, Hoflich G, Davranov K (2001) Influence of growth-promoting bacteria on the growth and nutrient uptake of cotton and wheat. In: Horst WJ et al (eds) Developments in plant and soil sciences, plant nutrition: food security and sustainability of agro-ecosystems through basic and applied research, vol 92. Kluwer, Dordrecht, pp 674–675 Egamberdieva D, Juraeva D, Haitov B (2004) Stimulation of wheat and maize growth through plant growth promoting rhizobacteria. Uzb J Agric Sci 2:44–47 Egamberdieva D, Shurigin V, Davranov K (2011) Colonisation of Pseudomonas chlororaphis TSAU13 and P. extremorientalis TSAU20 in the rhizosphere of wheat under salt stress. Uzb Biol J 4:26–30 Egamberdieva D, Shurigin V, Lyan Y, Davranov K (2012) Physiological characterization of Arthrobacter species isolated from salinated soil of Uzbekistan. Uzb Biol J 2:49–53 Egamberdieva D, Jabborova D, Mamadalieva N (2013a) Salt tolerant Pseudomonas extremorientalis able to stimulate growth of Silybum marianum under salt stress condition. Med Aromat Plant Sci Biotechnol 7:7–10 Egamberdieva D, Berg G, Lindstro¨m K, Ra¨sa¨nen LA (2013b) Alleviation of salt stress of symbiotic Galega officinalis L. (goat’s rue) by co-inoculation of Rhizobium with root colonising Pseudomonas. Plant Soil 1:453–465 Fawusi MOA, Ormrod DP, Eastham AM (1984) Response to water stress of Celosia argentea and Corchorus olitorius in controlled environments. Sci Hortic 22:163–171 Figueiredo MV, Burity HA, Martınez CR, Chanway C (2008) Alleviation of drought stress in the common bean Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 4:182–188 Gandour G (2002) Effect of salinity on development and production of chickpea genotypes. PhD Thesis, Aleppo University, Syria Golpayegani A, Tilebeni HG (2011) Effect of biological fertilizers on biochemical and physiological parameters of Basil (Ocimum basilicum L.) medicine plant. Am Eurasian J Agric Environ Sci 11:411–416 Gregorio S, Passerini P, Picciarelli P, Ceccarelli N (1995) Free and conjugated Indole-3-acetic acid in developing seeds of Sechium edule Sw. J Plant Physiol 145:736–740 Gul B, Khan MA, Weber DJ (2000) Alleviation salinity and dark-enforced dormancy in Allenrolfea occidentalis seeds under various thermoperiods. Aust J Bot 48:745–752

212


Gupta SC (1971) Effect of NAA, IAA and GA on germination of brinjal (Solanum melongena L.) seeds. Indian J Agric Res 5:215–216 Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499 Hayat R, Ali S, Siddique MT, Chatha TH (2008) Biological nitrogen fixation of summer legumes and their residual effects on subsequent rainfed wheat yield. Pak J Bot 40:711–722 Heidari M, Mosavinik SM, Golpayegani A (2011) Plant growth promoting rhizobacteria (PGPR) effect on physiological parameters and mineral uptake in basil (Ocimum basilicum L.) under water stress. ARPN J Agric Biol Sci 6:6–11 Itai C, Richmond AE, Vaada Y (1968) The role of root cytokinins during water and salinity stress. Israel J Bot 17:187–195 Jabborova D, Egamberdieva D, Ra¨sa¨nen L, Liao H (2013a) Salt tolerant Pseudomonas strain improved growth, nodulation and nutrient uptake of soybean grown under hydroponic salt stress condition. In: XVII international plant nutrition colloquium and boron satellite meeting proceedings book, pp 260–261 Jabborova D, Qodirova D, Egamberdieva D (2013b) Improvement of seedling establishment of soybean using IAA and IAA producing bacteria under saline conditions. Soil Water J 2: 531–539 Jaleel CA, Manivavannan P, Sankar P, Krishnakumar B, Gopi AR, Somasundaram R, Pannerselvam R (2007) Pseudomonas fluorescens enhances biomass yield and Ajmalicine production in Catharanthus roseus under water deficit stress. Colloids Surf B Biointerfaces 60: 7–11 Jamil M, Lee DB, Jung KY, Ashraf M, Lee SC, Rha ES (2006) Effect of salt (NaCl) stress on germination and early seedling growth of four vegetables species. Cent Eur Agric 7:273–282 Javid MG, Sorooshzadeh A, Moradi F, Sanavy SAMM, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 5:726–734 Karthikeyan B, Joe MM, Jaleel CA, Deiveekasundaram M (2010) Effect of root inoculation with plant growth promoting rhizobacteria (PGPR) on plant growth, alkaloid content and nutrient control of Catharanthus roseus (L.) G. Don. Nat Croat 1:205–212 Khan MA, Gul B, Weber D (2004) Action of plant growth regulators and salinity on seed germination of Ceratoides lanata. Can J Bot 82:37–42 Khodarahmpour Z, Ifar M, Motamedi M (2012) Effects of NaCl salinity on maize (Zea mays L.) at germination and early seedling stage. Afr J Biotechnol 11:298–304 Kuiper I, Bloemberg GV, Lugtenberg BJ (2001) Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-(PAH)-degrading bacteria. Mol Plant Microbe Interact 14:1197–1205 Kumar AA, Gill KS (1995) Performance of aromatic grasses under saline and sodic stress condition. Salt tolerance of aromatic grasses. Indian Perfumer 39:39–44 Leung WTH, Busson F, Jardin C (1968) Food composition table for use in Africa. FAO, Rome, 306 Li W, Liu X, Khan MA, Yamaguchi S (2005) The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. J Plant Res 118:207–214 Lin CC, Kao CH (1995) NaCl stress in rice seedlings: starch mobilization and the influence of gibberellic acid on seedling growth. Bot Bull Acad Sin 36:169–173 Lyan Y, Shurigin V, Egamberdieva D, Davranov K (2013) Isolation and characterization of new Pseudomonas species. Ann Uzb Acad Sci 4:65–70 Matiru VN, Dakora FD (2004) Potential use of rhizobial bacteria as promoters of plant growth for increased yield in landraces of African cereal crops. Afr J Biotechnol 3:1–7 Naidu CV (2001) Improvement of seed germination in red sanders (Pterocarpus santalinus Linn. F) by plant growth regulators. Indian J Plant Physiol 6:205–207


213

Neamatollahi E, Bannayan M, Souhani DA, Ghanbari A (2009) Does hydro and osmo-priming improve fennel (Foeniculum vulgare) seeds germination and seedlings growth? Notulae Botanicae Horti Agrobotanici Cluj-Napoca 37:190–194 Nwangburuka CC, Olawuyi OJ, Oyekale K, Ogunwenmo KO, Denton OA, Nwankwo E (2012) Arbuscular mycorrhizae(AM), poultry manure(PM), combination of AM-PM and inorganic fertilizer (NPK). Adv Appl Sci Res 3:1466–1471 Ondrasek G, Rengel Z, Romic D, Poljak M, Romic M (2009) Accumulation of non/essential elements in radish plants grown in salt-affected and cadmium contaminated environment. Cereal Res Commun 37:9–12 Othman Y, Al-Karaki G, Al-Tawaha AR, Al-Horani A (2006) Variation in germination and ion uptake in barley genotypes under salinity conditions. World J Agric Sci 2:11–15 Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349 Prakash L, Parthapasenan G (1990) Interactive effect of NaCl salinity and gibberellic acid on shoot growth, content of abscisic acid and gibberellin like substances and yield of rice (Oryza sativa). Plant Sci 100:173–181 Razmjoo K, Heydarizadeh P, Sabzalian MR (2008) Effect of salinity and drought stresses on growth parameters and essential oil content of Matricaria chamomila. Int J Agric Biol 10: 451–454 Remans R, Croonenborghs A, Torres Gutierrez R, Michiels J, Vanderleyden J (2007) Effects of plant growth promoting rhizobacteria on nodulation of Phaseolus vulgaris L. are dependent on plant P nutrition. Eur J Plant Pathol 119:341–351 Simons M, van der Bij AJ, Brand I, de Weger LA, Wijffelman CA, Lugtenberg BJ (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol Plant Microbe Interact 9:600–607 Spaepen S, Vanderleyden J (2010) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 17. doi:10.1101/cshperspect.a001438 Spaepen S, Boddelaere S, Croonenborghs A, Vanderleyden J (2008) Effect of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312:15–23 Teixeira da Silva JA, Egamberdieva D (2013) Plant-growth promoting rhizobacteria and medicinal plants. In: Govil JN et al (eds) Recent progress in medicinal plants, vol 38, Essential oils III and phytopharmacology. Studium, Houston, pp 26–42 Tsukui M, Uchino M, Takano K (2004) Fractionation and properties of the mucilage from jew’s marrow. Kanto Gakuin Univ Soc Humanity Environ Bull 1:143–152 Vadez V, Krishnamurthy L, Serraj R, Gaur PM, Upadhyaya HD, Hoisington DA, Varshney RK, Turner NC, Siddique KHM (2007) Large variation in salinity tolerance in chickpea is explained by differences in sensitivity at the reproductive stage. Field Crop Res 104:123–129 Velempini P, Riddoch I, Batisani N (2003) Seed treatments for enhancing germination of wild okra Corchorus olitorius. Exp Agric 39:441–447 Wahyuni S, Sinniah UR, Amarthalingam R, Yusop MK (2003) Enhancement of seedling establishment in rice by selected growth regulators as seed treatment. J Penelitian Pertanian Tanaman Pangan 22:51–55 Xu GY, Rocha PS, Wang ML, Xu ML, Cui YC, Li LY, Zhu YX, Xia X (2011) A novel rice calmodulin-like gene, OsMSR2, enhances drought and salt tolerance and increases ABA sensitivity in Arabidopsis. Planta 234:47–59 Yildirim E, Taylor AG (2005) Effect of biological treatments on growth of bean plants under salt stress. Ann Rep Bean Improv Coop 48:176–177 Yue HT, Mo WP, Li C, Zheng YY, Li H (2007) The salt stress relief and growth promotion effect of Rs-5 on cotton. Plant Soil 297:139–145