اثر اندوفیت باکتریایی (aurantiacum Exigubacterium) جداسازی شده از گیاه شورپسند (Salsola imbricata) بر صفات رشدی گیاهچه گوجه‌فرنگی تحت تنش شوری

نوع مقاله : مقالات پژوهشی

نویسندگان

• سهیلا آقائی درگیری ¹
• داود صمصام پور ¹
• مجید عسکری سیاهویی ²
• عبدالنبی باقری ²

¹ دانشگاه هرمزگان

² عضو هیات علمی، اگروه تحقیقات گیاه پزشکی، مرکز تحقیقات کشاورزی و منابع طبیعی هرمزگان، سازمان تحقیقات، آموزش و ترویج کشاورزی،

https://doi.org/10.22067/jhs.2021.61963.0

چکیده

اندوفیت‌ها می‌توانند نقش مهمی در بقای گیاهان در شرایط تنش شوری به واسطه کاهش اثر سو سدیم داشته باشند. این مطالعه با هدف بررسی اثر اندوفیت باکتریایی (aurantiacumExigubacterium)، جداسازی شده که از گیاه شورپسند(Salsola imbricata) در بهبود رشد گیاهچه گوجه‌فرنگی (Solanum lycopersicum L.) رقم ’8320‘، تحت شرایط تنش شوری انجام شد. بذور تلقیح شده با باکتری به صورت آزمایش فاکتوریل در قالب طرح کاملاً تصادفی با سه تکرار در سینی نشاء کشت و بعد از رشد، انتقال گیاهچه به گلدان‌ها در گلخانه دانشکده کشاورزی دانشگاه هرمزگان انجام گردید. تیمارهای آزمایش شامل پنج سطوح تنش شوری (صفر، 4، 6، 8 و 10 دسی‌زیمنس بر متر) و تلقیح باکتری بود. در این آزمایش صفات ارتفاع ساقه، وزن خشک ساقه، برگ و ریشه، تعیین درصد نشت الکترولیت، کلروفیل a، کلروفیل b، کارتنوئید، پرولین و محتوای کربوهیدارت مورد بررسی قرار گرفتند. نتایج مقایسه میانگین نشان داد تنش شوری باعث کاهش معنی‌دار ارتفاع ساقه، وزن خشک ساقه، برگ و ریشه، کلروفیل a، کلروفیل b، کاروتنوئید و افزایش نشت الکترولیت شد؛ اما باکتری باعث کاهش اثرات منفی تنش شوری روی گوجه‌فرنگی شد. گیاهچه گوجه‌فرنگی تحت تیمار با اندوفیت باکتریایی سطوح بالاتری از اسمولیت‌های کلیدی؛ پرولین آزاد و کربوهیدرات‌های محلول کل در مقایسه با گیاهچه تیمار نشده در شرایط تنش شوری نشان دادند. نتایج همچنین نشان داد باکتری باعث افزایش رشد گوجه‌فرنگی در آب و خاک شور می‌شود و می‌توان از آن به عنوان یک ابزار موثر برای کشت گیاهان حساس به شوری مانند گوجه‌فرنگی استفاده کرد.

کلیدواژه‌ها

• اندوفیت
• تحمل شوری
• کربوهیدرات محلول کل
• کود بیولوژیک
• گوجه‌فرنگی

20.1001.1.20084730.1400.35.1.12.2

موضوعات

• فیزیولوژی پس از برداشت

عنوان مقاله [English]

The Effect of Bacterial Endophyte (Exigubacterium aurantiacum) Isolated from Salsola imbricata on Growth Characteristics of Tomato Seedlings under Salinity Stress

نویسندگان [English]

• Soheila Aghaei Dargiri ¹
• Davood Samsampour ¹
• Majid Askari Seyahooei ²
• Abdolnabi Bagheri ²

¹ Department of Horticulture Sciences, Faculty of Agriculture and Natural Resource, University of Hormozgan

² Plant Protection Research Department, Hormozgan Agricultural and Natural Resources Research and Education Center, Agricultural Research Education and Extension Organiziation (AREEO), Bandar Abbas

چکیده [English]

Introduction: Tomato (Solanum lycopersicum L.) is a common vegetable that is widely cultivated and consumed worldwide in the Solanaceae family (global tomato production is estimated at approximately 182 million tons in 2017). Tomato, because of its elevated nutritional value, is the second most common vegetable commodity in the world after potatoes. As with other crops, the global production of tomatoes is threatened by certain biological stresses (such as pests, plant diseases and weeds) and non-biological stresses (such as salinity, drought, floods, cold and heat stress). Nowadays, the excessive use of chemical fertilizers in tomato production in order to increase yields, has resulted in environmental pollution and dangers on the health of consumers. The reaction of cultivated plants to these challenges is indicated by numerous morphological, physiological, biochemical and molecular changes, leading to a direct and indirect decrease in plant growth and productivity. Salinity as a non-biological stress can cause osmotic or ionic imbalance in plant cells. Salinity stress also limits growth and germination by affecting water and reducing water availability and affects crop production. Endophytes represent an eco-friendly option for the promotion of plant growth and for serving as sustainable resources of novel bioactive natural products. One of the alternative ways to restore normal plant growth under salinity stress may be to use plant growth to stimulate endophytes. Endophytes can play an important role in plant survival under salinity stress by reducing the adverse effects of sodium ion. Therefore, this work provides strong evidence that endophyte halophyte can be beneficial for tomato that help tolerate the plants stress.
Materials and Methods: The main aim of this study was to investigate the role of endophytic bacteria (Exigubacterium aurantiacum), isolated from Salsola imbricate, in improving the growth of Solanum lycopersicum L. (8320) under salinity stress. The salinity tolerance potential of bacterial endophytes was investigated in vitro. The bacterial was cultured in Nutrient Agar with different concentrations of NaCl (1, 2 and 3 M) and its growth dynamics were investigated after 24 and 120 hours. To prepare the bacterial suspension for inoculation with tomato seeds, the bacteria were cultured on NB (Nutrient Broth) medium for 24 hours in an incubator at 28±1 °C at 130 rpm. The OD suspension was adjusted to a concentration of 1×10⁸ ml. Tomato seeds (cultivar 8320) were washed with ethanol (70%) for 30 seconds and then sterilized with 0.5% sodium hypochlorite for 90 minutes and then completely distilled three times with distilled water. They were autoclaved and washed. For better contact of seeds with bacteria, 1% carboxymethylcellulose was used and then the seeds inoculated with bacterial treatments were placed on a shaker for six hours. Seeds inoculated with bacterial endophytes were planted in seedlings and then placed in pots containing autoclaved soil in the greenhouse of the Faculty of Agriculture, Hormoz University. The experiment was arranged in a factorial experiment based on randomized complete block design with three replications. Experimental treatments included five levels of salinity stress (0, 4, 6, 8 and 10 dS/m^-1) and bacterial endophyte inoculation (E. aurantiacum). Analysis of variance of traits was performed using SAS software version 9.4 and the means were compared using LSD method with a probability level of p < /em>
Results and Discussion: Analysis of variance showed that among treatments there is significant difference on growth parameters of tomato seedling (p < /em>  0.01), this indicate the positive impact of the bacterial endophyte on the growth parameters of tomato seedling is inoculated with the bacterial than the control plants. In this experiment, stem height, dry weight of stem, leaf and root, percentage of electrolyte leakage, chlorophyll a, chlorophyll b, carotenoid, proline and carbohydrate content were examined. The results of mean comparison showed that salinity stress significantly reduced stem height, stem dry weight, leaves and roots, chlorophyll a, chlorophyll b, carotenoids and increased electrolyte leakage; however, bacterial endophyte reduced the negative effects of salinity stress on tomatoes. Tomato seedling treated with endophytic bacteria showed higher levels of key osmolytes, total soluble carbohydrates and free proline compared to untreated plants under salinity stress.
Conclusion: The results also showed that the use of endophytic bacteria increased the growth of tomatoes in saline soil and water, thereby it can be used as an effective tool for growing salinity-sensitive plants such as tomatoes in saline conditions.

کلیدواژه‌ها [English]

• Bio-fertilizer
• Endophyte
• Salinity tolerance
• Total soluble carbohydrates
• Tomato

مراجع

1- Abdelaziz M.E., Kim D., Ali S., Fedoroff N.V., and Al-Babili S. 2017. The endophytic fungus Piriformospora indica enhances Arabidopsis thaliana growth and modulates Na⁺/K⁺ homeostasis under salt stress conditions. Journal of Plant Science 263: 107-115.

2- Abdelshafy Mohamad O.A., Ma J.B., Liu Y.H., Zhang D., Hua S., Bhute S., Hedlund B.P., Li W.J., and Li L. 2020. Beneficial endophytic bacterial populations associated with medicinal plant Thymus vulgaris alleviate salt stress and confer resistance to Fusarium oxysporum. Journal of Frontiers in Plant Science 11: 47.

3- Ahmad P., Hashem A., Abd-Allah E.F., Alqarawi A.A., John R., Egamberdieva D., and Gucel S. 2015. Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L.) through antioxidative defense system. Journal of Frontiers in Plant Science 6: 868.

4- Arbona V., Manzi M., Zandalinas, S.I., Vives-Peris V., Pérez-Clemente R.M., and Gómez-Cadenas A. 2017. Physiological, metabolic, and molecular responses of plants to abiotic stress. In Stress Signaling in Plants: Genomics and Proteomics Perspective 2: 1-35. Journal of Springer, Cham.

5- Askari M., Maghsodei Mod A., and Safari V.R. 2012. Journal of Production and Processing of Crops and Horticultural Products, Third Year, Ninth Issue. (In Persion)

6- Babu A.N., Jogaiah S., Ito S.I., Nagaraj A.K., and Tran L.S.P. 2015. Improvement of growth, fruit weight and early blight disease protection of tomato plants by rhizosphere bacteria is correlated with their beneficial traits and induced biosynthesis of antioxidant peroxidase and polyphenol oxidase. Journal of Plant Science 231: 62-73.

7- Bai Y., Kissoudis C., Yan Z., Visser R.G., and van der Linden G. 2018. Plant behaviour under combined stress: tomato responses to combined salinity and pathogen stress. The Plant Journal 93(4): 781-793.

8- Bashan, Y., de-Bashan, L.E., Prabhu, S.R. and Hernandez J.P. 2014. Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Journal of Plant and Soil 378(1-2): 1-33.

9- Bates L.S., Waldren R.P., and Teare I.D. 1973. Rapid determination of free proline for water-stress studies. Plant and Soil 39(1(: 205-207.

10- Begum F., Sultana, W. and Nessa A. 1996. Effect of NaCl salinity stress on seed germination and seedling growth of maize. Seed Research Jouranl 24: 97-101.

11- Bergna A., Cernava T., Rändler M., Grosch R., Zachow C., and Berg G. 2018. Tomato seeds preferably transmit plant beneficial endophytes. Phytobiomes Journal 2(4): 183-193.

12- Bolan N.S. 1991. A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Journal of Plant and Soil 134:189–207.

13- Brader G., Compant S., Mitter B., Trognitz F., and Sessitsch A. 2014. Metabolic potential of endophytic bacteria. Current Opinion in Biotechnology Journal 27: 30-37.

14- Bu N., Li X., Li Y., Ma C., Ma L., and Zhang C. 2012. Effects of Na₂CO₃ stress on photosynthesis and antioxidative enzymes in endophyte infected and non-infected rice. Journal of Ecotoxicology and Environmental Safety 78: 35-40.

15- Buwalda J.G., Stribley D.P., and Tinker P.B. 1983. Increased uptake of bromide and chloride by plants infected with vesicular‐arbuscular mycorrhizas. New Phytologist 93(2): 217-225.

16- Chanratana M., Joe M.M., Choudhury A.R., Anandham R., Krishnamoorthy R., Kim K., Jeon S., Choi J., Choi J. and Sa T. 2019. Physiological response of tomato plant to chitosan-immobilized aggregated Methylobacterium oryzae CBMB20 inoculation under salinity stress.Journal 3 Biotech 9(11): 397.

17- Chen T., Li C., White J.F., and Nan Z. 2019. Effect of the fungal endophyte Epichloë bromicola on polyamines in wild barley (Hordeum brevisubulatum) under salt stress. Plant and Soil 436(1-2): 29-48.

18- Chojak-Koźniewska J., Linkiewicz A., Sowa S., Radzioch M.A., and Kuźniak E. 2017. Interactive effects of salt stress and Pseudomonas syringae pv. lachrymans infection in cucumber:involvement of antioxidant enzymes, abscisic acid and salicylic acid. Journal of Environmental and Experimental Botany 136: 9-20.

19- Dias M.P., Bastos M.S., Xavier V.B., Cassel E., Astarita L.V., and Santarém E.R. 2017. Plant growth and resistance promoted by Streptomyces spp. in tomato. Journal of Plant Physiology and Biochemistry 118: 479-493.

20- Egamberdieva D., and Lugtenberg B. 2014. Use of plant growth-promoting rhizobacteria to alleviate salinity stress in plants. In Use of Microbes for the Alleviation of Soil Stresses,Journal of Springer, New York, NY. 1: 73-96.

21- English J.P., and Colmer T.D. 2011. Salinity and waterlogging tolerances in three stem-succulent halophytes (Tecticornia species) from the margins of ephemeral salt lakes. Journal of Plant and Soil 348(1-2): 379.

22- Evelin H., Kapoor R., and Giri B. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Journal of Annals of Botany 104(7): 1263-1280.

23- Farkhondeh R., Nabizadeh E., and Jalilnezhad N. 2012. Effect of salinity stress on proline content, membrane stability and water relations in two sugar beet cultivars. International Journal of AgriScience 2(5): 385-392.

24- Flo1wers T.J. 2004. Improving salt stress tolerance. Journal of Experimental Botany 55: 307-319.

25- Flowers, T.J. and Colmer T.D. 2008. Abstract. New Phytologist 179(4): 945-963.

26- Flowers T.J. and Yeo A.R. 1995. Breeding for salinity resistance in crop plants: where next. Journal of Functional Plant Biology 22(6): 875-884.

27- Gedemann J.W. 1975. Vesicular arbuscular mycorrhizal. In: The development and function of roots. Torrey, D. G. and Clarkson, D. T. C. (Eds), Academic Press, London, 575-591.

28- Ghabooli M. 2014. Effect of Piriformospora indica inoculation on some physiological traits of barley (Hordeum vulgare) under salt stress. Chemistry of Natural Compounds 50(6):1082-1087.

29- Gharsallah C., Fakhfakh H., Grubb D., and Gorsane F. 2016. Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. Journal of AoB Plants, 8.

30- Giri B. and Mukerji K.G. 2004. Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake.  Mycorrhiza, Journal of Springer 14(5): 307-312.

31- Giri B., Kapoor R., and Mukerji K.G. 2003. Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Journal of Biology and Fertility of Soils 38(3):170-175.

32- Giri B., Kapoor R., and Mukerji K.G. 2007. Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microbial ecology, Journal of Springer 54(4): 753-760.

33- Golparyan F., Azizi A., and Soltani J. 2018. Endophytes of Lippia citriodora (Syn. Aloysia triphylla) enhance its growth and antioxidant activity. European Journal of Plant Pathology 152(3): 759-768.

34- Hasegawa P.M., Bressan R.A., Zhu J.K., and Bohnert H.J. 2000. Plant cellular and molecular responses to high salinity. Journal of Annual Review of Plant Biology 51(1): 463-499.

35- Hatimi A. 1999. Effect of salinity on the association between root symbionts and Acacia cyanophylla Lind: growth and nutrition. Plant and Soil, Journal of Springer 216: 93–101.

36- Hedarzadeh M., and Marvatei A. 2020. Investigation of the effect of different levels of urea fertilizer and different sources of iron fertilizer on quantitative and qualitative yield to lemon (Lippia citriodora H. B. and K.). Journal of Horticultural Sciences (Agricultural Sciences and Industries) 34(1): 45-59 (In Persian)

37- Herlemann D.P., Labrenz M., Jürgens K., Bertilsson S., Waniek J.J. and Andersson A.F. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. The ISME Journal 5(10): 1571-1579.

38- Iqbal M., Akhtar J., Anwar-Ul-Haq M., Nasim M., Saeed A., and Naveed M. 2007. Variation in growth and ion uptake in rice cultivars under NaCl stress in hydroponics. Pakistan Journal Agriculture Science 44(3):393-400.

39- Jan F.G., Hamayun M., Hussain A., Jan G., Iqbal A., Khan A. and Lee I.J. 2019. An endophytic isolate of the fungus Yarrowia lipolytica produces metabolites that ameliorate the negative impact of salt stress on the physiology of maize. BMC microbiology 19(1): 1-10.

40- Kafi M., Borzuyi A., Salehi M., Kamandi A., Masoumi A. and Nabati C. 2015 Physiology of environmental stresses in plants. Mashhad University Press, Mashhad. (In Persian)

41- Karim M.A., Nawata E. and Shigenaga S. 1993. Effect of Salinity and Temperature on Yield, Mineral Ion Concentrations and Physiology in Hexaploid Triticale. Japanese Journal of Crop Science 62(3): 419-428.

42- Kaur G. and Asthir B.J.B.P. 2015. Proline: a key player in plant abiotic stress tolerance. Biologia plantarum, Journal of Springer 59(4): 609-619.

43- Khan A.L., Hussain J., Al-Harrasi A., Al-Rawahi A. and Lee I.J. 2013. Endophytic fungi: a source of gibberellins and crop resistance to abiotic stress. Crit Reviews Biotech 35(1): 62-74.

44- Khan A.L., Waqas M., Asaf S., Kamran M., Shahzad R., Bilal S., Khan M.A., Kang S.M., Kim Y.H., Yun B.W. and Al-Rawahi A. 2017. Plant growth-promoting endophyte Sphingomonas sp. LK11 alleviates salinity stress in Solanum pimpinellifolium. Journal of Environmental and Experimental Botany, 133: 58-69.

45- Khan, M.H., Singha, K.L. and Panda S.K. 2002. Changes in antioxidant levels in Oryza sativa L. roots subjected to NaCl-salinity stress. Journal of Acta Physiologiae Plantarum 24(2): 145-148.

46- Khan M.I.R., Asgher M. and Khan N.A. 2014. Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Journal of Plant Physiology and Biochemistry 80: 67-74.

47- Kirch H.H., Vera-Estrella R., Golldack D., Quigley F., Michalowski C.B., Barkla B.J. and Bohnert H.J. 2000. Expression of water channel proteins in Mesembryanthemum crystallinum. Journal of Plant Physiology 123(1):111-124.

48- Li J.H., Wang E.T., Chen W.F. and Chen W.X. 2008. Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Journal of Soil Biology and Biochemistry 40(1): 238-246.

49- Li L., Li L., Wang X., Zhu P., Wu H. and Qi S. 2017. Plant growth-promoting endophyte Piriformospora indica alleviates salinity stress in Medicago truncatula. Journal of Plant Physiology and Biochemistry 119: 211-223.

50- Liang, W., Ma, X., Wan, P. and Liu L. 2018. Plant salt-tolerance mechanism: A review. Journal of Biochemical and biophysical research communications 495(1): 286-291.

51- Lichtenthaler H.K. and Buschmann C. 2001. Chlorophylls and carotenoids: Measurement and characterization by UV‐VIS spectroscopy. Journal of Current protocols in food analytical chemistry, 1(1):F4-3.

52- Lucero M.E., Barrow J.R., Osuna P., Reyes I. and Duke S.E. 2008. Enhancing native grass productivity by cocultivating with endophyte-laden calli. Journal of Rangeland Ecology and Management 61(1): 124-130.

53- Manchanda, G. and Garg N. 2011. Alleviation of salt-induced ionic, osmotic and oxidative stresses in Cajanus cajan nodules by AM inoculation. Journal of Plant Biosystems, 145(1): 88-97.

54- Massaretto I.L., Albaladejo I., Purgatto E., Flores F.B., Plasencia F., Egea-Fernández J.M., Bolarin M.C. and Egea I. 2018. Recovering tomato landraces to simultaneously improve fruit yield and nutritional quality against salt stress. Journal of Frontiers in Plant Science 9: 1778.

55- Mayak S., Tirosh T. and Glick B.R. 2004. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Journal of Plant physiology and Biochemistry 42(6): 565-572.

56- Mercado-Blanco J. and JJ. Lugtenberg B. 2014. Biotechnological applications of bacterial endophytes. Journal of Current Biotechnology 3(1): 60-75.

57- Munns R. 2005. Genes and salt tolerance: bringing them together. Journal of New Phytologist 167(3): 645–663.

58- Munns R. and Tester M. 2008. Mechanisms of salinity tolerance. Annu. Review. Journal of Plant Biology 59: 651-681.

59- Murillo-Amador B., Reyes-Pérez J.J., Hernandez-Montiel L.G., Rueda-Puente E.O., De Lucia B., Beltrán-Morales F.A. and Ruiz-Espinoza F.H. 2017. Physiological responses to salinity in Solanum lycopersicum L. varieties. Pakistan Journal of Botany 49(3):809-818.

60- Negrão S., Schmöckel S.M. and Tester M. 2017. Evaluating physiological responses of plants to salinity stress. Annals of Botany 119(1): 1-11.

61- Niamat B., Naveed M., Ahmad Z., Yaseen M., Ditta A., Mustafa A., Rafique M., Bibi R., Sun N. and Xu M. 2019. Calcium-Enriched Animal Manure Alleviates the Adverse Effects of Salt Stress on Growth, Physiology and Nutrients Homeostasis of Zea mays L. Journal of Plants 8(11): 480.

62- Porcel R. and Ruiz-Lozano J.M. 2004. Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. Journal of Experimental Botany 55(403):1743-1750.

63- Qi W. and Zhao L. 2013. Study of the siderophore‐producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. Journal of basic microbiology, 53(4): 355-364.

64- Rawat L., Bisht T.S., Upadhayay R.G. and Kukreti A. 2016. Selection of Salinity Tolerant Trichoderma Isolates and Evaluating their Performance in Alleviating Salinity Stress in Rice (Oryzae Sativa L.).International Journal of National Acadmy of Agricultural Science (NAAS). 34(6): 1869-1875.

65- Romero F.M., Marina M. and Pieckenstain F.L. 2016. Novel components of leaf bacterial communities of field-grown tomato plants and their potential for plant growth promotion and biocontrol of tomato diseases. Journal of Research in Microbiology 167(3): 222-233.

66- Rueda-Puente E.O., Renganathan P., Farmohammadi S., Moghaddam A. and Zakeri O. 2013. Plant growth promoting bacteria associated to Salicornia rhyzosphere in bandarAbbas, Iran. In Proceedings of the International Conference on Environmental Science and Technology, Athens.

67- Ruiz-Lozano J.M., Porcel R., Azcón C. and Aroca R. 2012. Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. Journal of Experimental Botany 63(11): 4033-4044.

68- Sadeghi F., Samsampour D., Seyahooei M.A., Bagheri A. and Soltani J. 2020. Fungal endophytes alleviate drought-induced oxidative stress in mandarin (Citrus reticulata L.): Toward regulating the ascorbate–glutathione cycle. Journal of Scientia Horticulturae 261: 108991.

69- Sairam R.K., Rao K.V. and Srivastava G.C. 2002. Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Journal of Plant Science 163(5): 1037-1046.

70- Sathiyaraj G., Srinivasan S., Kim Y.J., Lee O.R., Parvin S., Balusamy S.R.D., Khorolragchaa A. and Yang D.C. 2014. Acclimation of hydrogen peroxide enhances salt tolerance by activating defense-related proteins in Panax ginseng CA Meyer. Molecular Biology Reports 41(6): 3761-3771.

71- Sattelmacher B. 2001. The apoplast and its significance for plant mineral nutrition. Journal of New Phytologist 149(2): 167-192.

72- Shahzad R., Khan AL., Bilal S., Waqas M., Kang SM. and Lee IJ. 2017. Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa. Environ Exp Bot. 136:68–77.

73- Shankar S. and Shanker U. 2014. Arsenic contamination of groundwater: a review of sources, prevalence, health risks, and strategies for mitigation. The Scientific World Journal.

74- Sherameti Irena, Bationa Shahollari, Yvonne Venus, Lothar Altschmied, Ajit Varma, and Ralf Oelmüller. 2005. "The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters." Journal of Biological Chemistry 280(28): 26241-26247.

75- Sholi N.J. 2012. Effect of salt stress on seed germination, plant growth, photosynthesis and ion accumulation of four tomato cultivars. American Journal of Plant Physiology 7(6): 269-275.

76- Soad A., Algam X., Guan-lin and Coosemans J. 2005. Delivery Methods for Introducing Endophytic Bacillus into Tomato and Their Effect on Growth Promotion and Suppression of Tomato Wilt. Plant Pathology Journal 4: 69-74.

77- Soltani J. 2017. Endophytism in Cupressoideae (Coniferae): a model in endophyte biology and biotechnology. In Endophytes: Biology and Biotechnology Journal of Springer, Cham 15: 280(28): 26241-7.

78- Suzuki, N., Bassil, E., Hamilton, J.S., Inupakutika, M.A., Zandalinas, S.I., Tripathy, D., Luo, Y., Dion, E., Fukui, G., Kumazaki, A. and Nakano R. 2016. ABA is required for plant acclimation to a combination of salt and heat stress. Journal of PloS one, 11(1): e0147625.

79- Szymańska S., Płociniczak T., Piotrowska-Seget Z. and Hrynkiewicz K. 2016. Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L.–community structure and metabolic potential. Journal of Microbiological research, 192: 37-51.

80- Tefera T. and Vidal S. 2009. Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. Journal of BioContro 54(5): 663-669.

81- Torabian S., Farhangi-Abriz S. and Zahedi M. 2018. Efficacy of FeSO 4 nano formulations on osmolytes and antioxidative enzymes of sunflower under salt stress. Indian Journal of Plant Physiology 23(2): 305-315.

82- Valentovic P., Luxova M., Kolarovic L. and Gasparikova O. 2006. Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars. Journal of Plant Soil and Environment 52(4): 184.

83- Ventosa A. and Arahal D.R. 2009. Halophily (halophilism and halophilic microorganisms). Extremophiles vol. Encyclopedia of life support systems. EOLSS Publishers Company Limited, Oxford 233-246.

84- Waller F., Achatz B., Baltruschat H., Fodor J., Becker K., Fischer M., Heier T., Hückelhoven R., Neumann C., Von Wettstein D. and Franken P. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Journal of Proceedings of the National Academy of Sciences 102(38): 13386-13391.

85- Yan N., Marschner P., Cao W., Zuo C. and Qin W. 2015. Influence of salinity and water content on soil microorganisms. International Soil and Water Conservation Research 3(4):316-323.

86- Yang H., Hu J., Long X., Liu Z. and Rengel Z. 2016. Salinity altered root distribution and increased diversity of bacterial communities in the rhizosphere soil of Jerusalem artichoke. Scientific Reports 6(1): 1-10.

87- Yemm E.W. and Willis A. 1954. The estimation of carbohydrates in plant extracts by anthrone. Biochemical Journal 57(3): 508-514.

88- Yeo A.R., Caporn S.J.M. and Flowers T.J. 1985. The effect of salinity upon photosynthesis in rice (Oryza sativa L.): gas exchange by individual leaves in relation to their salt content. Journal of Experimental Botany 36(8): 1240-1248.

89- Yurtseven E., Kesmez G.D. and Ünlükara A. 2005. The effects of water salinity and potassium levels on yield, fruit quality and water consumption of a native central Anatolian tomato species (Lycopersicon esculantum). Journal of Agricultural Water Management 78(1-2): 128-135.

90- Zarea M.J., Hajinia S., Karimi N., Goltapeh E.M., Rejali F. and Varma A. 2012. Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Journal of Soil Biology and Biochemistry 45: 139-146.

91- Zhang F., Wang Y., Liu C., Chen F., Ge H., Tian F., Yang T., Ma K. and Zhang Y. 2019. Trichoderma harzianum mitigates salt stress in cucumber via multiple responses. Journal of Ecotoxicology and Environmental Safety 170: 436-445.

92- Zhang H.X., and Blumwald E. 2001. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Journal of Nature Biotechnology 19(8): 765-768.

93- Zhang S., Gan Y. and Xu B. 2016. Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Journal of Frontiers in Plant Science 7:1405.

94- Zhang W., Wang X.X., Yang Z., Ashaduzzaman S.M., Kong M.J., Lu L.Y., Shen J.X. and Dai C.C. 2017. Physiological mechanisms behind endophytic fungus Phomopsis liquidambari-mediated symbiosis enhancement of peanut in a monocropping system. Journal of Plant and Soil 416(1-2): 325-342.

95- Zuccarini P. and Okurowska P. 2008. Effects of mycorrhizal colonization and fertilization on growth and photosynthesis of sweet basil under salt stress. Journal of Plant Nutrition 31(3): 497-513.