2,842
Views
9
CrossRef citations to date
0
Altmetric
Plant-Microorganism Interactions

Endophytic fungus Bipolaris sp. CSL-1 induces salt tolerance in Glycine max.L via modulating its endogenous hormones, antioxidative system and gene expression

, , ORCID Icon, , ORCID Icon, & show all
Pages 319-332 | Received 11 Aug 2021, Accepted 28 Jan 2022, Published online: 27 Feb 2022

References

  • AbdElgawad H, Zinta G, Hegab MM, Pandey R, Asard H, Abuelsoud W. 2016. High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci. 7:276–276.
  • Abdel Latef AAH, Chaoxing H. 2011. Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic. 127:228–233.
  • Ahmad P, Abdel Latef AA, Hashem A, Abd Allah EF, Gucel S, Tran LS. 2016. Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci. 7:347. DOI:10.3389/fpls.2016.00347.
  • Amtmann A, Troufflard S, Armengaud P. 2008. The effect of potassium nutrition on pest and disease resistance in plants. Physiol Plant. 133:682–691.
  • Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S. 2020. Salinity induced physiological and biochemical changes in plants: an omic approach towards salt stress tolerance. Plant Physiol Biochem. 156:64–77.
  • Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA. 100:15649–15654.
  • Asaf S, Khan AL, Khan MA, Imran QM, Yun B-W, Lee I-J. 2017a. Osmoprotective functions conferred to soybean plants via inoculation with Sphingomonas sp. LK11 and exogenous trehalose. Microbiol Res. 205:135–145.
  • Asaf S, Khan M, Khan A, Waqas M, Shahzad R, Kim A-Y, Kang S-M, Lee I-J. 2017b. Bacterial endophytes from arid land plants regulate endogenous hormone content and promote growth in crop plants: an example of Sphingomonas sp. and Serratia marcescens. J Plant Interact. 12:31–38.
  • Awan SA, Ilyas N, Khan I, Raza MA, Rehman AU, Rizwan M, Rastogi A, Tariq R, Brestic M. 2020. Bacillus siamensis reduces cadmium accumulation and improves growth and antioxidant defense system in two wheat (Triticum aestivum L.) varieties. Plants. 9:878.
  • Barrow JR, Lucero ME, Reyes-Vera I, Havstad KM. 2008. Do symbiotic microbes have a role in regulating plant performance and response to stress? Commun Integr Biol. 1:69–73.
  • Bilal L, Asaf S, Hamayun M, Gul H, Iqbal A, Ullah I, Lee I-J, Hussain A. 2018. Plant growth promoting endophytic fungi Asprgillus fumigatus TS1 and Fusarium proliferatum BRL1 produce gibberellins and regulates plant endogenous hormones. Symbiosis. 76:117–127.
  • Bömke C, Rojas MC, Gong F, Hedden P, Tudzynski B. 2008. Isolation and characterization of the gibberellin biosynthetic gene cluster in Sphaceloma manihoticola. Appl Environ Microbiol. 74:5325–5339.
  • Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254.
  • Chan C-X, Teo S-S, Ho C-L, Othman RY, Phang S-M. 2004. Optimisation of RNA extraction from Gracilaria changii (Gracilariales, Rhodophyta). J Appl Phycol. 16:297–301.
  • Chaoui A, Mazhoudi S, Ghorbal MH, El Ferjani E. 1997. Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci. 127:139–147.
  • Cheng C, Li C, Wang D, Zhai L, Cai Z. 2018. The soybean GmNARK affects ABA and salt responses in transgenic arabidopsis thaliana. Front Plant Sci. 9:514.
  • Colla G, Rouphael Y, Cardarelli M, Tullio M, Rivera CM, Rea E. 2008. Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol Fertil Soils. 44:501–509.
  • Cuevas J, Daliakopoulos IN, del Moral F, Hueso JJ, Tsanis IK. 2019. A review of soil-improving cropping systems for soil salinization. Agronomy. 9:295.
  • Daei G, Ardekani MR, Rejali F, Teimuri S, Miransari M. 2009. Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J Plant Physiol. 166:617–625.
  • El-Esawi MA, Alaraidh IA, Alsahli AA, Alamri SA, Ali HM, Alayafi AA. 2018. Bacillus firmus (SW5) augments salt tolerance in soybean (Glycine max L.) by modulating root system architecture, antioxidant defense systems and stress-responsive genes expression. Plant Physiol Biochem. 132:375–384.
  • Evelin H, Giri B, Kapoor R. 2012. Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed trigonella foenum-graecum. Mycorrhiza. 22:203–217.
  • Giri B, Kapoor R, Mukerji KG. 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. Microb Ecol. 54:753–760.
  • Guo L, Shi D, Wang D. 2010. The key physiological response to alkali stress by the alkali-resistant halophyte Puccinellia tenuiflora is the accumulation of large quantities of organic acids and into the rhyzosphere. J Agron Crop Sci. 196:123–135.
  • Gupta S, Schillaci M, Walker R, Smith PMC, Watt M, Roessner U. 2020. Alleviation of salinity stress in plants by endophytic plant-fungal symbiosis: current knowledge, perspectives and future directions. Plant Soil. 461:219–244.
  • Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C. 2010. Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil. 331:313–327.
  • Hamayun M, Hussain A, Khan SA, Kim H-Y, Khan AL, Waqas M, Irshad M, Iqbal A, Rehman G, Jan S, Lee I-J. 2017. Gibberellins producing endophytic fungus porostereum spadiceum AGH786 rescues growth of salt affected soybean. Front Microbiol. 8:686.
  • Hamayun M, Khan SA, Ahmad N, Tang D-S, Kang S-M, Na C-I, Sohn E-Y, Hwang Y-H, Shin D-H, Lee B-H. 2009. Cladosporium sphaerospermum as a new plant growth-promoting endophyte from the roots of Glycine max (L.) merr. World J Microbiol Biotechnol. 25:627–632.
  • Hamayun M, Khan SA, Khan AL, Rehman G, Kim Y-H, Iqbal I, Hussain J, Sohn E-Y, Lee I-J. 2010a. Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp. MH-6 isolated from cucumber (Cucumis sativus L.). Mycologia. 102:989–995.
  • Hamayun M, Khan SA, Khan AL, Shinwari ZK, Hussain J, Sohn E-Y, Kang S-M, Kim Y-H, Khan MA, Lee I-J. 2010b. Effect of salt stress on growth attributes and endogenous growth hormones of soybean cultivar Hwangkeumkong. Pak J Bot. 42:3103–3112.
  • Hasan H. 2002. Gibberellin and auxin production by plant root-fungi and their biosynthesis under salinity-calcium interaction. Rostl Vyroba. 48:101–106.
  • Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V. 2020. Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants (Basel, Switzerland). 9:681.
  • Ighodaro OM, Akinloye OA. 2018. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alex J Med. 54:287–293.
  • Ikram M, Ali N, Jan G, Jan FG, Rahman IU, Iqbal A, Hamayun M. 2018. IAA producing fungal endophyte Penicillium roqueforti Thom., enhances stress tolerance and nutrients uptake in wheat plants grown on heavy metal contaminated soils. PLOS ONE. 13:e0208150.
  • Ismail, Hamayun M, Hussain A, Iqbal A, Khan SA, Lee I-J. 2018. Endophytic fungus Aspergillus japonicus mediates host plant growth under normal and heat stress conditions. BioMed Res Int. 2018:7696831.
  • Jabeen Z, Hussain N, Irshad F, Zeng J, Tahir A, Zhang G. 2020. Physiological and antioxidant responses of cultivated and wild barley under salt stress. Plant Soil Environ. 66:334–344.
  • Jan R, Aaqil Khan M, Asaf S, Lubna, Park J-R, Lee I-J, Kim K-M. 2021. Flavonone 3-hydroxylase relieves bacterial leaf blight stress in rice via overaccumulation of antioxidant flavonoids and induction of defense genes and hormones. Int J Mol Sci. 22:6152.
  • Jan R, Khan MA, Asaf S, Lee I-J, Bae J-S, Kim K-M. 2020a. Overexpression of OsCM alleviates BLB stress via phytohormonal accumulation and transcriptional modulation of defense-related genes in Oryza sativa. Sci Rep. 10:19520.
  • Jan R, Khan MA, Asaf S, Lee I-J, Kim K-M. 2020b. Modulation of sugar and nitrogen in callus induction media alter PAL pathway, SA and biomass accumulation in rice callus. Plant Cell Tissue Organ Cult. 143:517–530.
  • Jan R, Khan MA, Asaf S, Lubna L, and Kim I-J, M K. 2019. Metal resistant endophytic bacteria reduces cadmium, nickel toxicity, and enhances expression of metal stress related genes with improved growth of Oryza Sativa, via regulating its antioxidant machinery and endogenous hormones. Plants. 8:363.
  • Jithesh MN, Prashanth SR, Sivaprakash KR, Parida AK. 2006. Antioxidative response mechanisms in halophytes: their role in stress defence. J Genet. 85:237–254.
  • Jung J-H, Dong-Min S, Woo-Chul B, Soon-Kwang H, Joo-Won S, Sangho K, Byeong-Chul J. 2002. Identification of FM001 as plant growth-promoting substance from acremonium strictum MJN1 culture. J Microbiol Biotechnol. 12:327–330.
  • Kang S-M, Khan AL, Waqas M, You Y-H, Kim J-H, Kim J-G, Hamayun M, Lee I-J. 2014. Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact. 9:673–682.
  • Kang S-M, Shahzad R, Khan MA, Hasnain Z, Lee K-E, Park H-S, Kim L-R, Lee I-J. 2021. Ameliorative effect of indole-3-acetic acid- and siderophore-producing Leclercia adecarboxylata MO1 on cucumber plants under zinc stress. J Plant Interact. 16:30–41.
  • Kaya C, Ashraf M, Alyemeni MN, Ahmad P. 2020. The role of endogenous nitric oxide in salicylic acid-induced up-regulation of ascorbate-glutathione cycle involved in salinity tolerance of pepper (Capsicum annuum L.) plants. Plant Physiol Biochem. 147:10–20.
  • Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA. 2009. The influence of arbuscular mycorrhizal colonisation on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hortic. 121:1–6.
  • Khalil HA, Eissa AM, El-Shazly SM, Aboul Nasr AM. 2011. Improved growth of salinity-stressed citrus after inoculation with mycorrhizal fungi. Sci Hortic. 130:624–632.
  • Khan A, Geetha R, Akolkar A, Pandya A, Archana G, Desai AJ. 2006. Differential cross-utilization of heterologous siderophores by nodule bacteria of Cajanus cajan and its possible role in growth under iron-limited conditions. Appl Soil Ecol. 34:19–26.
  • Khan AL, Hamayun M, Ahmad N, Hussain J, Kang S-M, Kim Y-H, Adnan M, Tang D-S, Waqas M, Radhakrishnan R. 2011. Salinity stress resistance offered by endophytic fungal interaction between Penicillium minioluteum LHL09 and Glycine max. J Microbiol Biotechnol. 21:893–902.
  • Khan MA, Asaf S, Khan AL, Adhikari A, Jan R, Ali S, Imran M, Kim K-M, Lee I-J. 2019a. Halotolerant rhizobacterial strains mitigate the adverse effects of NaCl stress in soybean seedings. BioMed Res Int. 2019:9530963. DOI:10.1155/2019/9530963.
  • Khan MA, Asaf S, Khan AL, Adhikari A, Jan R, Ali S, Imran M, Kim KM, Lee IJ. 2020a. Plant growth-promoting endophytic bacteria augment growth and salinity tolerance in rice plants. Plant Biol. 22:850–862.
  • Khan MA, Asaf S, Khan AL, Jan R, Kang S-M, Kim K-M, Lee I-J. 2019b. Rhizobacteria AK1 remediates the toxic effects of salinity stress via regulation of endogenous phytohormones and gene expression in soybean. Biochem J. 476:2393–2409.
  • Khan MA, Asaf S, Khan AL, Jan R, Kang SM, Kim KM, Lee IJ. 2020b. Extending thermotolerance to tomato seedlings by inoculation with SA1 isolate of Bacillus cereus and comparison with exogenous humic acid application. PLoS One. 15:e0232228.
  • Khan MA, Hamayun M, Asaf S, Khan M, Yun B-W, Kang S-M, Lee I-J. 2021a. Rhizospheric bacillus spp. rescues plant growth under salinity stress via regulating gene expression, endogenous hormones, and antioxidant system of Oryza sativa L. Front Plant Sci. 12:1145.
  • Khan MA, Hamayun M, Iqbal A, Khan SA, Hussain A, Asaf S, Khan AL, Yun B-W, Lee I-J. 2018. Gibberellin application ameliorates the adverse impact of short-term flooding on Glycine max L. Biochem J. 475:2893–2905.
  • Khan MA, Sahile AA, Jan R, Asaf S, Hamayun M, Imran M, Adhikari A, Kang S-M, Kim K-M, Lee I-J. 2021b. Halotolerant bacteria mitigate the effects of salinity stress on soybean growth by regulating secondary metabolites and molecular responses. BMC Plant Biol. 21:176.
  • Kia SH, Jurkechova M, Glynou K, Piepenbring M, Maciá-Vicente JG. 2018. The effects of fungal root endophytes on plant growth are stable along gradients of abiotic habitat conditions. FEMS Microbiol Ecol. 94:fix162.
  • Kim YN, Khan MA, Kang SM, Hamayun M, Lee IJ. 2020. Enhancement of drought-stress tolerance of brassica oleracea var. italica L. by newly isolated variovorax sp. YNA59. J Microbiol Biotechnol. 30:1500–1509.
  • Kinkema M, Gresshoff PM. 2008. Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol Plant-Microbe Interact. 21:1337–1348.
  • Kubi HAA, Khan MA, Adhikari A, Imran M, Kang S-M, Hamayun M, Lee I-J. 2021. Silicon and plant growth-promoting rhizobacteria pseudomonas psychrotolerans CS51 mitigates salt stress in Zea mays L. Agriculture. 11:272.
  • Li S, Wang N, Ji D, Zhang W, Wang Y, Yu Y, Zhao S, Lyu M, You J, Zhang Y, et al. 2019. A GmSIN1/GmNCED3s/GmRbohBs feed-forward loop acts as a signal amplifier that regulates root growth in soybean exposed to salt stress. Plant Cell. 31:2107–2130.
  • Li Y, Chen Q, Nan H, Li X, Lu S, Zhao X, Liu B, Guo C, Kong F, Cao D. 2017. Overexpression of GmFDL19 enhances tolerance to drought and salt stresses in soybean. PLOS ONE. 12:e0179554.
  • Lu Y, Wang G, Meng Q, Zhang W, Duan B. 2014. Growth and physiological responses to arbuscular mycorrhizal fungi and salt stress in dioecious plant Populus tomentosa. Can J For Res. 44:1020–1031.
  • Lubna, Asaf, S., Hamayun, M., Gul, H., Lee, I.-J., and Hussain, A. (2018a). Aspergillus niger CSR3 regulates plant endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic acid. J Plant Interac. 13:100–111.
  • Lubna, Asaf, S., Hamayun, M., Khan, A. L., Waqas, M., Khan, M. A., Jan, R., Lee, I.-J., and Hussain, A. (2018b). Salt tolerance of Glycine max.L induced by endophytic fungus Aspergillus flavus CSH1, via regulating its endogenous hormones and antioxidative system. Plant Physiol Biochem. 128:13–23.
  • Lubna, Asaf, S., Khan, A. L., Waqas, M., Kang, S.-M., Hamayun, M., Lee, I.-J., and Hussain, A. (2019). Growth-promoting bioactivities of Bipolaris sp. CSL-1 isolated from Cannabis sativa suggest a distinctive role in modifying host plant phenotypic plasticity and functions. Acta Physiol Plant. 41:65.
  • Mbarki S, Cerdà A, Brestic M, Mahendra R, Abdelly C, Pascual JA. 2017. Vineyard compost supplemented with trichoderma harzianum T78 improve saline soil quality. Land Degrad Dev. 28:1028–1037.
  • Molina-Montenegro MA, Acuña-Rodríguez IS, Torres-Díaz C, Gundel PE, Dreyer I. 2020. Antarctic root endophytes improve physiological performance and yield in crops under salt stress by enhanced energy production and Na+ sequestration. Sci Rep. 10:5819.
  • Muchate N, Nikalje G, Rajurkar N, Penna S, Nikam T. 2016. Plant salt stress: adaptive responses, tolerance mechanism and bioengineering for salt tolerance. Bot Rev. 82:371–406.
  • Murkute A, Singh S. 2006. Studies on salt stress tolerance of citrus rootstock genotypes with arbuscular mycorrhizal fungi. Hortic Sci. 33:70–76.
  • Navarro J, Pérez-Tornero O, Morte A. 2013. Alleviation of salt stress in citrus seedlings inoculated with arbuscular mycorrhizal fungi depends on the rootstock salt tolerance. J Plant Physiol. 171:76–85.
  • Nilsen ETO, David M. 1996. The physiology of plants under stress: abiotic factors. New York: John Wiley & Sons, Inc.
  • Parida AK, Das AB. 2005. Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf. 60:324–349.
  • Pollastri S, Savvides A, Pesando M, Lumini E, Volpe MG, Ozudogru EA, Faccio A, De Cunzo F, Michelozzi M, Lambardi M, et al. 2018. Impact of two arbuscular mycorrhizal fungi on Arundo donax L. response to salt stress. Planta. 247:573–585.
  • Radhakrishnan R, Khan AL, Lee I-J. 2013. Endophytic fungal pre-treatments of seeds alleviates salinity stress effects in soybean plants. J Microbiol. 51:850–857.
  • Rahneshan Z, Nasibi F, Moghadam AA. 2018. Effects of salinity stress on some growth, physiological, biochemical parameters and nutrients in two pistachio (Pistacia vera L.) rootstocks. J Plant Interact. 13:73–82.
  • Rasel M, Tahjib-Ul-Arif M, Hossain MA, Hassan L, Brestic M. 2020. Screening of salt-tolerant rice landraces by seedling stage phenotyping and dissecting biochemical determinants of tolerance mechanism. J Plant Growth Regul. 40:1853–1868.
  • Rathod S, Brestic M, Shao H. 2011. Chlorophyll a fluorescence determines the drought resistance capabilities in two varieties of mycorrhized and non-mycorrhized Glycine max linn. Afr J Microbiol Res. 5:4197–4206.
  • Ren C-G, Kong C-C, Xie Z-H. 2018. Role of abscisic acid in strigolactone-induced salt stress tolerance in arbuscular mycorrhizal Sesbania cannabina seedlings. BMC Plant Biol. 18:74.
  • Robinson T, Singh D, Nigam P. 2001. Solid-state fermentation: a promising microbial technology for secondary metabolite production. Appl Microbiol Biotechnol. 55:284–289.
  • Sahile AA, Khan MA, Hamayun M, Imran M, Kang S-M, Lee I-J. 2021. Novel bacillus cereus strain, ALT1, enhance growth and strengthens the antioxidant system of soybean under cadmium stress. Agronomy. 11:404.
  • Saneoka H, Ishiguro S, Moghaieb REA. 2001. Effect of salinity and abscisic acid on accumulation of glycinebetaine and betaine aldehyde dehydrogenase mRNA in Sorghum leaves (Sorghum bicolor). J Plant Physiol. 158:853–859.
  • Shahbaz M, Ashraf M. 2013. Improving salinity tolerance in cereals. Crit Rev Plant Sci. 32:237–249.
  • Sheteiwy MS, Abd Elgawad H, Xiong Y-C, Macovei A, Brestic M, Skalicky M, Shaghaleh H, Alhaj Hamoud Y, El-Sawah AM. 2021. Inoculation with Bacillus amyloliquefaciens and mycorrhiza confers tolerance to drought stress and improve seed yield and quality of soybean plant. Physiol Plant. 172:2153–2169.
  • Shrivastava P, Kumar R. 2015. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci. 22:123–131.
  • Takai T, Kondo M, Yano M, Yamamoto T. 2010. A quantitative trait locus for chlorophyll content and its association with leaf photosynthesis in rice. Rice. 3:172–180.
  • Talaat NB, Shawky BT. 2014. Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exp Bot. 98:20–31.
  • Tavakkoli E, Rengasamy P, McDonald GK. 2010. High concentrations of Na+ and Cl- ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot. 61:4449–4459.
  • Tefera T, Vidal S. 2009. Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. Bio Control. 54:663–669.
  • Van Ha C, Leyva-González MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Van Dong N. 2014. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA. 111:851–856.
  • Wang W, Vinocur B, Altman A. 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 218:1–14.
  • Wang Y, Mopper S, Hasenstein KH. 2001. Effects of salinity on endogenous ABA, IAA, JA, and SA in iris hexagona. J Chem Ecol. 27:327–342.
  • Waqas M, Khan AL, Kamran M, Hamayun M, Kang S-M, Kim Y-H, Lee I-J. 2012. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules. 17:10754–10773.
  • Waqas M, Khan AL, Lee I-J. 2014. Bioactive chemical constituents produced by endophytes and effects on rice plant growth. J Plant Interact. 9:478–487.
  • Yang B, Wang X, Ma H, Yang T, Jia Y, Zhou J, Dai C. 2015. Fungal endophyte phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere. Front Microbiol. 6:982.
  • Yanwei L, Guangquan W, Qingjie M, Wenhui Z, Baoli D. 2014. Growth and physiological responses to arbuscular mycorrhizal fungi and salt stress in dioecious plant Populus tomentosa. Can J For Res. 44:1020–1031.
  • Yoon JY, Hamayun M, Lee S-K, Lee I-J. 2009. Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol. 12:63–68.
  • Yousaf MJ, Hussain A, Hamayun M, Iqbal A, Irshad M, Kim H-Y, Lee I-J. 2021. Transformation of endophytic bipolaris spp. into biotrophic pathogen under auxin cross-talk with brassinosteroids and abscisic acid. Front Bioeng Biotechnol. 9:657635.
  • Zhang S, Gan Y, 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. Front Plant Sci. 7:1405.
  • Zhao L, Wang F, Zhang Y, Zhang J. 2014. Involvement of Trichoderma asperellum strain T6 in regulating iron acquisition in plants. J Basic Microbiol. 54:S115–S124.
  • Zhou L, He H, Liu R, Han Q, Shou H, Liu B. 2014. Overexpression of GmAKT2potassium channel enhances resistance to soybean mosaic virus. BMC Plant Biol. 14:154.