Document Type : Research paper

Authors

1 Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Golestan, Iran

2 Gorgan University of Agricultural Sciences and Natural resources, Gorgan, Golestan, Iran

Abstract

Soil salinity and water deficit are major problems for development of agricultural production. In this study, effects of growth promoting microorganisms (inoculation with Piriformospora indica and two isolates of Streptomyces sp.) on the leaf yield and absorption rate of some elements in leaves and roots of stevia plant was investigated under salinity conditions for two consecutive years (2016-2017). The fresh and dry weights of the leaves were significantly affected by microorganism and salinity. High salinity level led to sodium accumulation in the root and leaf; while the amount of potassium and K+/Na+ ratio decreased in both root and leaf. The accumulation of phosphorus in both leaf and root was significantly decreased in 3 ds m-1 salinity. Plants exposed to Piriformospora indica and Streptomyces strains, showed lower sodium content in their leaves and roots. In contrast, an increase in the content of potassium and phosphorus was observed in the growth stimulator microbes-treated plants. However, the K+/Na+ ratio in the growth stimulator microbes-treated plants was to some extent lower than its ratio in control plants. In conclusion, P. indica and Streptomyces strains improved the biomass formation of the stevia plant under salinity conditions by controlling the uptake of potassium, phosphorus and sodium.

Keywords

  1. Abdelaziz M.E, Kim D, Ali S, Fedoroff N.V, Al-Babili S. 2017. The endophytic fungus Piriformospora indica enhances Arabidopsis thaliana growth and modulates Na+/K+ homeostasis under salt stress conditions. Plant Science 263, 107-115.
  2. Adeleke R, Nwangburuka C, Oboirien B. 2017. Origins, roles and fate of organic acids in soils: A review. South African Journal of Botany 108,393-406.
  3. Ahmad I, Maathuis F.J.M. 2014. Cellular and tissue distribution of potassium: physiological relevance, mechanisms and regulation. Journal of plant Physiology 171:708-714.
  4. Ahmad P, Hakeem K.R, Kumar A, Ashraf M, Akram N.A. 2012. Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). African Journal of Biotechnology 11, 2694-2703.
  5. Aldesuquy H.S, Mansour F.A, Abo-Hamed S.A. 1998. Effect of the culture filtrates of Streptomyces on growth and productivity of wheat plants. Folia Microbiol (Praha) 43, 465-70.
  6. Ali S, Charles T.C, Glick B.R. 2014. Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiology and Biochemistry 80,160-167.
  7. Almeida D.M, Oliveira M.M, Saibo N.J. 2017. Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genetics and Molecular Biology 40, 326-345.
  8. Andrés-Barrao C, Lafi F.F, Alam I. 2017. Complete Genome Sequence Analysis of Enterobacter sp. SA187, a Plant Multi-Stress Tolerance Promoting Endophytic Bacterium. Front Microbiology 8, 2023.
  9. Anuar E.N, Nulit R, Idris AS. 2015. Growth promoting effects of endophytic fungus Phlebia gano EF3 on oil palm (Elaeis guineensis) seedlings. International Journal of Agric Biology 17,135-141.

10. Bacilio M, Rodrguez H, Moreno M, Hernandez J.P, Bashan Y. 2004. Mitigation of salt stress in wheat seedlings by a gfp-tagged Azospirillum lipoferum. Biology Fertility of Soils 40, 188-193.

11. Bacon C.W, Jr J.F.W. 2015. Functions, mechanisms and regulation of endophytic and epiphytic microbial communities of plants. Symbiosis 68,1-12

12. Balsanelli E, Tadra-Sfeir M.Z, Faoro H, Pankievicz V.C, De Baura V.A, Pedrosa F.O, De Souza E.M, Dixon R, Monteiro R.A. 2015. Molecular adaptations of Herbaspirillum seropedicae during colonization of the maize rhizosphere. Environal Microbiology 18(8), 2343-56.

13. Baltruschat H, Fodor J, Harrach B.D, Niemczyk E, Barna B, Gullner G. 2008. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist 180, 501-510.

14. Barrett-Lennard E.G, Bathgate A.D, Malcolm C.V. 2003. Saltland pastures in Australia, a practical guide. Department of Agriculture and Food, Western Australia, Perth Bulletin 4312.

15. Blumwald E. 2000. Sodium transport and salt tolerance in plants. Current Opinion of Cell Biology 12, 431-434.

16. Bucio J.L, Campos Cuevas J.C, Hernandez-Calderon E, Valasquez- Bacerra C, Farias-Rodriguez R, Macias-Rodriguez L.I, Valencia- Cantero E. 2007. Bacillus megaterium rhizobacteria promote growth and alter root system architecture through an auxin and ethylene-independent signaling mechanism in Arabidopsis thaliana. Molecular Plant Microbe Interactions 20, 207-217.

17. Cantrell I.C, Linderman R.G. 2001. Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity. Plant and Soil 233, 269-281.

18. Chapman H, Pratt P.E. 1982. Methods of analysis for soils, plants, and waters. University of California, Division of Agricultural sciences. California. USA. Riverside press.

19. Chen S, Hawighorst P, Sun J, Polle A. 2014. Salt tolerance in Populus: Significance of stress signaling networks, mycorrhization, and soil amendments for cellular and whole-plant nutrition. Environmental Experimental Botany 107, 113-124.

20. Das A, Kamal Sh, Shakil N.A, Sherameti I, Oelmüller R, Dua M, Tuteja N, Johri A.K, Varma A. 2012. The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii. Plant Signaling and Behavior 7(1), 103 -112.

21. Dejampour J, Aliasgarzad N, Zeinalabedini M, Rohani niya M, Majidi Hervan E. 2012. Evaluation of salt tolerance in almond [Prunus dulcis (L.) Batsch] rootstocks. African Journal of Biotechnology 11(56), 11907-11912.

22. De Zélicourt A, Synek L, Saad MM, Alzubaidy H, Jalal R, Xie Y. 2018. Ethylene induced plant stress tolerance by Enterobacter sp. SA187 is mediated by 2‐keto‐4‐methylthiobutyric acid production. PLoS Genetic 14, 1-28

23. Dreyer I, Gomez-Porras J.L, Riedelsberger J. 2017. The potassium battery: a mobile energy source for transport processes in plant vascular tissues. New Phytolology 216,1049-1053.

24. Drüge U, Baltruschat H, Franken P. 2007. Piriformospora indica promotes adventitious root formation in cuttings. Scientia Horticulturae. 112, 422-426.

25. Dworkin M, Falkow S. 2006. The prokaryotes: vol. 4: bacteria: firmicutes, cyanobacteria, vol. 4. Berlin: Springer Science and Business Media.

26. Earanna N. 2007. Response of Stevia rebaudiana to biofertilizers. Karnataka Journal of Agricultural Science 20, 616-617.

27. Egamberdieva D, Wirth S.J, Shurigin V.V, Hashem A, Abdallah E.F. 2017. Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiology 8,1887-1899.

28. El-Tarabily K.A. 2008. Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase– producing Streptomycete actinomycetes. Plant Soil 308, 161-74.

29. Emami A. 1997. Plant decomposition methods. Agricultural Research, Training and Promotion Organization, Soil and Water Research Institute 2, 182.

30. Essa T.A. 2002. Effect of salinity stress on growth and nutrient composition of three soybean cultivars. Journal of Agronomy and Crop Science 188, 86-93.

31. Fallahi H, Ghorbany M, Samadzadeh A, Aghhavani-Shajari M, Asadian A. 2016. Influence of arbuscular mycorrhizal inoculation and humic acid application on growth and yield of Roselle (Hibiscus sabdariffa L.) and its mycorrhizal colonization index under deficit irrigation. International Journal of Horticultural Science and Technology 3(2), 113-128.

32. Franken P. 2012. The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Applied Microbiology and Biotechnology 96, 1455-1464.

33. Gerke J. 2015. The acquisition of phosphate by higher plants: effect of carboxylate release by the roots. A critical review, Journal of Plant Nutrition and Soil Science 178, 351-364.

34. Ghaffari M.R, Ghabooli M, Khatabi B., Hajirezaei, M.R, Schweizer P, Salekdeh GH. 2016. Metabolic and transcriptional response of central metabolism affected by root endophytic fungus Piriformospora indica under salinity in barley. Plant Molecular Biology 90(6), 699-717.

35. Ghorbani A, Razavi S.M, Ghasemi Omran V.O, Pirdashti H. 2018. Piriformospora indica inoculation alleviates the adverse effect of NaCl stress on growth, gas exchange and chlorophyll fluorescence in tomato (Solanum lycopersicum L.). Plant Biology 20(4), 725-736.

36. Gopalakrishnan S, Humayun P, Srinivas V, Vijayabharathi R, Bhimineni R.K, Rupela O. 2012. Plant growth-promoting traits of Streptomyces with bio-control potential isolated from herbal vermicompost. Biocontrol Science and Technology 22, 1199-210.

37. Gopalakrishnan S, Pande S, Sharma M, Humayun P, Kiran B.K, Sandeep D, Vidya M.S, Deepthi K, Rupela O. 2011. Evaluation of actinomycete isolates obtained from herbal vermicompost for biologicalcontrol of Fusarium wilt of chickpea. Crop Protection 30, 1070-1078.

38. Gopalakrishnan S, Vadlamudi S, Bandikinda P, Sathya A, Vijayabharathi R, Rupela O, Kudapa H, Katta K, Varshney R.K. 2014. Evaluation of Streptomyces strains isolated from herbal vermicompost for their plant growth-promotion traits in rice. Microbiological Research 169, 40-48.

39. Guerrero-Galán C, Calvo-Polanco M, Zimmermann S.D. 2019. Ectomycorrhizal symbiosis helps plants to challenge salt stress conditions. Mycorrhiza 29(4), 291-301.

40. Gul M, Wakeel A, Steffens D, Lindberg S. 2019. Potassium‐induced decrease in cytosolic Na+ alleviates deleterious effects of salt stress on wheat (Triticum aestivum L.). Plant Biology 4, 1-23.

41. Gutierrez-Oliva V.F, Abud-Archila M, Flores-Perez A, Alvarez-Solis J.D, Gutierrez-Miceli F.A. 2009. Influencia de los hongos micorrizicos arbuscularessobre el crecimiento de vitro plantulas de pi˜na (Ananas comosus (L.) Merr.) Condiferentes niveles de fosforo. Gayana Botany 66 (1), 1-9.

42. Hajar E.W.I, Sulaiman A.Z.B, Sakinah A.M. 2014. Assessment of heavy metals tolerance in leaves, stems and flowers of Stevia rebaudiana plant. Procedia Environmental Sciences 20, 386-393.

43. Hajienia S, Zare M, Mohammadi Gultepeh A, Rejali F. 2013. Study on the usefulness of Piriformospora indica and Azospirillum Sp. in increasing tolerance of wheat cultivar Sardari (Triticum aestivum) to salinity stress. Journal of Environmental Stress in Agricultural Sciences 4(1), 31-21.

44. Heidari Z, Nazarideljou M, Rezaie Danesh Y, Khezrinejad N. 2016. Morphophysiological and biochemical responses of Zinnia elegans to different irrigation regimes in symbiosis with Glomus mosseae. International Journal of Horticultural Science and Technology 3(1), 19-32.

45. Hosseini A, Gharghani A. 2015. Effects of Arbuscular Mycorrhizal Fungi on Growth and Nutrient Uptake of Apple Rootstocks in Calcareous Soil. International Journal of Horticultural Science and Technology 2(2), 173-185.

46. Hosseini R.Z, Mohammadi E, Kalatejari S. 2015. Effect of bio-fertilizer on growth, development and nutrient content (leaf and soil) of Stevia rebaudiana Bertoni. Journal of Crop Protection 4, 691-704.

47. Hosseini Y, Homaee M, Karimian N, Saadat S. 2009. Modeling of canola response to combined salinity and nitrogen stresses. Journal of Science and Technology in. Agricultural Natural Resources 12, 721-734. (In Persian)

48. Jin W, Peng L, Zhang X, Sun H, Yuan Z. 2019. Effects of endophytic and actomycorrhizal basidiomycetes on Quercus virginiana seedling growth and nutrient absorption. Journal of Sustainable Forestry 4, 1-14.

49. Jog R, Pandya M, Nareshkumar G, Rajkumar S. 2014. Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160(4), 778-788.

50. Jogawat A, Saha S, Bakshi M, Dayaman, V, Kumar M, Dua M. 2013. Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signal Behavior 8,91-96.

51. Jose A.I. 2002. Package of Practices Recommendations: Crops. Kerala Agricultural University, Trichur, Kerala, India 278.

52. Kader M.A, Lindberg S. 2005. Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice, Oryza sativa L. determined by the fluorescent dye SBFI. Journal of Experimental Botany 56(422), 3149-3158.

53. Kaefer E. 1977. Meiotic mitotic recombination in Aspergillus and its chromosomal aberration. Advances in Genetics 19, 33-131.

54. Kämpfer P, Glaeser S.P, Parkes L, Keulen G.V, Dyson P. 2014. The family Streptomycetaceae, in the prokaryotes. Berlin: Springer 889-1010.

55. Kao W.Y, Tsai T, Tsai H, Shih C.N. 2006. Response of three glycine species to salt stress. Environmental and Experimental Botany 56, 120-125.

56. Karlidag H, Esitken A, Yildirim E, Figen-Donmez M, Turan M. 2011. Effects of plant growth promoting bacteria on yield, growth, leaf water content, membrane permeability and ionic composition of strawberry under saline conditions. Journal of Plant Nutrition 34, 34-45.

57. Kazemein, S.A, Alinia M, Shakeri E. 2016. Interaction effect of salinity stress and nitrogen on growth and activity of antioxidant enzymes of blue panicgrass (Panicum antidotale Retz.). Journal of environmental stresses in crop sciences 3(10), 279-289.

58. Khalvati M.A, Mozafar A, Schmidhalter U. 2005. Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biology Stuttgart 7, 706-712.

59. Lanza M, Haro R, Conchillo L.B, Benito B. 2019. The endophyte Serendipita indica reduces the sodium content of Arabidopsis plants exposed to salt stress: fungal ENA ATPases are expressed and regulated at high pH and during plant co‐cultivation in salinity. Environmental Microbiology 4, 1-19.

60. Ludwig W, Euzéby J, Schumann P, Busse H.J, Trujillo M.E, Kämpfer P, Whitman W.B. 2012. Road map of the phylum Actinobacteria, in Bergey’s manual of systematic bacteriology. Berlin, Springer 2012, 1-28.

61. Mandal S, Evelin H, Giri B, Singh V.P, Kapoor R. 2013. Arbuscular mycorrhiza enhances the production of stevioside and rebaudioside-A in Stevia rebaudiana via nutritional and non-nutritional mechanisms. Applied Soil Ecology 72, 187-194.

62. Martínez-Medina A, Roldán A, Albacete A, Pascual J.A. 2011. The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry 72, 223-229.

63. Meena KK, Mesapogu S, Kumar M, Yandigeri MS, Singh G, Saxena AK. 2010. Co-inoculation of the endophytic fungus Piriformospora indica with the phosphate-solubilising bacterium Pseudomonas striata affects population dynamics and plant growth in chickpea. Biology of Fertility Soils 46(2), 169-174.

64. Molassiotis A, Sotiropoulos T, Tanou G, Diamantidis G, Therios I. 2006. Boron-induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh). Environmental and Experimental Botany 56(1), 54-62.

65. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Physiology 59, 651- 681.

66. Nadeem S.M, Zahir Z.A, Naveed M, Arshad M, Shahzad S.M. 2006. Variation in growth and ion uptake of maize due to inoculation with plant growth promoting rhizobacteria under salt stress. Plant Soil and Environment 25, 78-84.

67. Netondo G.W, Onyango J.C, Beck E. 2004. Sorghum and salinity: I. Response of growth, water relations, and ion accumulation to NaCl salinity. Crop science 44, 797-805.

68. Noaman M.H, El-Haddad E. 2000. Effects of irrigation water salinity and leaching fraction on the growth of six halophyte species. Journal of Agricultural Science 135, 279-285.

69. Page A.L, Miller R.H, Keeney D.R. 1982. Methods of soil analysis, part 2, second edition, American Society of Agronomy-Soil Science Society of America, Madison, USA 1159.

70. Pan R, Xu L, Wei Q, Wu C, Tang W, Oelmüller R, Zhang W. 2017. Piriformospora indica promotes early flowering in Arabidopsis through regulation of the photoperiod and gibberellin pathways. PLoS ONE 12(12), 1-15.

71. Percey W.J, Shabala L, Wu Q, Su N, Breadmore M.C, Guijt R.M, Bose J, Shabala S. 2016. Potassium retention in leaf mesophyll as an element of salinity tissue tolerance in halophytes. Plant Physiol. Biochem. 109, 346-354

72. Péret B, Desnos T, Jost R, Kanno S, Berkowitz O, Nussaume L. 2014. Root architecture responses: in search of phosphate, Plant Physiology 166, 1713-1723.

73. Petrus M.L.C, Claessen D. 2014. Pivotal roles for Streptomyces cell surface polymers in morphological differentiation, attachment and mycelial architecture. Antonie Van Leeuwenhoek International Journal of Gen Molecular Microbiology 106(1), 39-127.

74. Portugal E.P, Mercuri Quitério G.C, Honório S.L. 2006. Seleção de fungos micorrízicos arbusculares para estévia, Stevia Rebaudiana (bert.) Bertoni. E dilberto. MultiCiencia: Revista Interdisciplinar Dos Centros E Nucleos Da Unicamp 7, 2-20.

75. Purkayastha S, Markosyan A, Prakash M, Bhusari S, Pugh Jr.G, Lynch B, Roberts A. 2016. Steviol glycosides in purified Stevia leaf extract sharing the same metabolic fate. Regulatory Toxicology and Pharmacology 77, 125-133.

76. Qin Y, Pan X, Kubicek C, Druzhinina I, Chenthamara K, Labbé J.L, Yuan Z. 2017. Diverse plant-associated pleosporalean fungi from saline areas: Ecological tolerance and nitrogen-status dependent effects on plant growth. Frontiers in Microbiology 8(6), 1-14.

77. Rajput M.S, Kumar G, Rajkumar S. 2013. Repression of oxalic acid-mediated mineral phosphate solubilization in rhizospheric isolates of Klebsiella pneumoniae by succinate. Archive of Microbiology 195(2), 81-8.

78. Rodriguez-Romero A.S, Azcon R, Jaizme-Vega M.C, 2011. Early mycorrhizationof two tropical crops, papaya (Carica papaya L.) and pineapple [Ananas comosus (L.) Merr.], reduces the necessity of P fertilization during the nursery stage. Fruits 66(1), 3-10.

79. Sadeghi A, Karimi E, Dahazi PA, Javid MG, Dalvand Y, Askari H. 2012. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil condition. World J Microbiology and Biotechnology 28, 1503-9.

80. Sairam R.K, Tyagi A. 2004. Physiology and molecular biology of salinity stress tolerance in plants. Current Science 86, 407-421.

81. Santoyo G, Morenohagelsieb G, Del COM, Glick B.R. 2016. Plant growth-promoting bacterial endophytes. Microbiol Research 183, 92-99

82. Satheesan J, Narayanan A.K, Sakunthala M. 2012. Induction of root colonization by Piriformospora indica leads to enhanced asiaticoside production in Centella asiatica. Mycorrhiza 22,195.202.

83. Shabala S, Babourina O, Newman I. 2000. Ion specific mechanisms of osmoregulation in bean mesophyll cells. Journal of Experimental Botany 51, 1243-1253.

84. Shabala S, Bose J, Fuglsang A.T, Pottosin I. 2015. On a quest for stress tolerance genes: membrane transporters in sensing and adapting to hostile soils. Journal of Experimental Botany 67(4), 1015-1031.

85. Siddikee A, Glick B.R, Chauhan S, Yim W, Sa T. 2011. Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1- aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiology and Biochemistry 49, 427-434.

86. Silva, E.N., Silveira, J.A.G., Rodrigues, C.R.F. and Viégas, R.A., 2015. Physiological adjustment to salt stress in J atropha curcas is associated with accumulation of salt ions, transport and selectivity of K+, osmotic adjustment and K+/Na+ homeostasis. Plant Biology, 17(5), pp.1023-1029.

87. Soejarto D.D, Kinghorn A.D, Farnsworth N.R. 1982. Potential sweetening agents of plant origin. III. Organoleptic evaluation of Stevia leaf herbarium samples for sweetness. Journal of Natural Production 45, 590-599.

88. Song M, Chai Q, Li X, Yao X, Li Ch, Christensen M.J, Nan Zh. 2015. An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant Soil 387, 153-165.

89. Sun Y, Lindberg S, Shabala L, Morgan S, Shabala S, Jacobsen S.E. 2017. A comparative analysis of cytosolic Na+ changes under salinity between halophyte quinoa (Chenopodium quinoa) and glycophyte pea (Pisum sativum). Environmental and Experimental Botany 141, 154-160.

90. Tavarini S, Passera B, Martini A, Avio L, Sbrana C, Giovannetti M.G. Angelinia L. 2018. Plant growth, steviol glycosides and nutrient uptake as affected by arbuscular mycorrhizal fungi and phosphorous fertilization in Stevia rebaudiana Bert. Industrial Crops and Products 111, 899-907.

91. Tian B, Zhang C, Ye Y, Wen J, Wu Y, Wang H. 2017. Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome. Agriculture, Ecosystem and Environment 247, 149-156

92. Tokala R.K, Strap J.L, Jung C.M, Crawford D.L, Salove M.H, Deobald L.A, Bailey J.F, Morra M.J, 2002. Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Applied Environmental Microbiology 68, 2161-71.

93. Vafadar F, Amooaghaie R, Otroshy M. 2014. Effects of plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungus on plant growth, stevioside, NPK, and chlorophyll content of Stevia rebaudiana. Journal of Plant Interaction 9, 128-136.

94. Wakeel A. 2013. Potassium–sodium interactions in soil and plant under saline‐sodic conditions. Journal of Plant Nutrition and Soil Science 176(3), 344-354.

95. Wu C, Li B, Wei Q, Pan R, Zhang W. 2019. Endophytic fungus Serendipita indica increased nutrition absorption and biomass accumulation in Cunninghamia lanceolata seedlings under low phosphate. Acta Ecologica Sinica 39(1), 21-29.

96. Xia Y, Sahib M.R, Amna A, Opiyo S.O, Zhao Z, Gao Y.G. 2019. Culturable endophytic fungal communities associated with plants in organic and conventional farming systems and their effects on plant growth. Scientific reports 9(1), 1-10.

97. Xie Y, Han Sh, Li X, Amombo E, Fu J. 2017. Amelioration of Salt Stress on Bermudagrass by the Fungus Aspergillus aculeatus. Molecular Plant-Microbe Interactions 30(3), 245-254.

98. Yun P, Le X, SaiSai W, Shabala L, Shabala S, Zhang W. 2018. Piriformospora indica improves salinity stress tolerance in Zea mays L. plants by regulating Na+ and K+ loading in root and allocating K+ in shoot. Plant Growth Regulator 86(2), 323-331.

99. Zahir A.Z, Arshad M, Frankenberger W.F. 2004. Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Advances in Agronomy 81, 97-168.

  1. Zahir Z.A, Ghani U, Naveed M, Nadeem S.M, Asghar H.N, 2009. Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.) under salt-stressed conditions. Archive of Microbiology 191, 415-424.
  2. Zanetti F, Zegada-Lizarazu W, Lambertini C, Monti A. 2019. Salinity effects on germination, seedlings and full-grown plants of upland and lowland switchgrass cultivars. Biomass and Bioenergy 120, 273-280.
  3. Zarea M.J, Hajinia S, Karimi N, Goltapeh E.M, Rejali F, Varma A. 2012. Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biology and Biochemistry 45, 139-146.
  4. Zhang Y, Yu X, Zhang W, Lang D, Zhang X, Cui G, Zhang X. 2019. Interactions between endophytes and plants: beneficial effect of endophytes to ameliorate biotic and abiotic stresses in plants. Journal of plant biology 62(1), 1-13.
  5. Zhao S, Zhou N, Zhao Z.Y, Zhang K, Wu G.H, Tian C.Y. 2016. Isolation of endophytic plant growth-promoting bacteria associated with the halophyte Salicornia europaea and evaluation of their promoting activity under salt stress. Current Microbiology 73, 574-581.