Novel endophytic fungus Leptosphaeria sp. strain T-2 improves plant growth and environmental stress tolerance

Abstract

Drought and salinity stress pose threats to agricultural production in drylands. Although breeding and genetic modification techniques have been employed to develop drought- and salt-tolerant crops, these methods are costly and risky. Hence, the potential application of endophytic fungi in dryland agriculture is being explored as a novel approach in improving plant tolerance to environmental stress. In this study, endophytic fungi with growth-promoting effects were isolated, characterized, and evaluated in terms of their ability to confer drought and stress tolerance to their host plants. Seventy-seven growth-promoting endophytic fungi belonging to 20 genera were isolated from barley roots; of these, strain T-2 elicited remarkable effects on plant growth parameters. Phylogenetic analysis revealed that strain T-2 belongs to genus Leptosphaeria, whose members are generally known as plant pathogens. Thus, Leptosphaeria sp. strain T-2 is a novel endophytic fungus that promotes plant growth. Moreover, it alleviated growth inhibition caused drought and salinity stress, as evidenced by the survival and maintained health of lettuce plants inoculated with strain T-2. The results of this study suggest that strain T-2 can be applied as a biofertilizer to improve agricultural production in drylands.

References

[] Ahanger MA, Akram NA, Ashraf M et al (2017) Plant responses to environmental stresses—from gene to biotechnology. AoB PLANTS 9: plx025. https://doi.org/10.1093/aobpla/plx025

[] Arnold AE, Engelbrecht BMJ. Fungal endophytes double minimum leaf conductance in seedlings of a tropical tree. J Trop Ecol, 2007, 23: 369-372

[] Baum C, EI-Tohamy W, Gruda N. Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Sci Hortic, 2015, 187: 131-141

[] Bonfante P, Genre A. Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun, 2010, 1: 48

[] Burrell AL, Evans JP, De Kauwe MG (2020) Anthropogenic climate change has driven over 5 million km² of drylands towards desertification. Nat Commun 3853. https://doi.org/10.1038/s41467-020-17710-7

[] Ferreira FV, Musumeci MA. Trichoderma as biological agent: scope and prospects to improve efficacy. World J Microb Biot, 2021, 37: 90

[] Flowers TJ, Garcia A, Koyama M, Yeo AR. Breeding for salt tolerance in crop plants - the role of molecular biology. Acta Physiol Plant, 1997, 19: 427-433

[] Fu C, An Z. Study of aridization in northern China—a global change issue facing directly the demand of nation. Earth Sci Front, 2002, 9: 271-275

[] Gill SS, Gill R, Trivedi DK, Anjum NA, Sharma KK, Ansari MW, Ansari AA, Johri AK, Prasad R, Pereira E, Varma A, Tuteja N. Piriformospora indica: potential and significance in plant stress tolerance. Front Microbiol, 2016, 7: 332

[] Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma species opportunistic, avirulent plant symbionts. Nat Rev Microbiol, 2004, 2: 43-56

[] Hsiao TC. Plant responses to water stress. Ann Rev Plant Physiol, 1973, 24: 519-570

[] Huang J, Li Y, Fu C, Chen F, Fu Q, Dai A, Shinoda M, Ma Z, Guo W, Li Z, Zhang L, Liu Y, Yu H, He Y, Xie Y, Guan X, Ji M, Lin L, Wang S, Yan H, Wang G. Dryland climate change: recent progress and challenges. Rev Geophys, 2017, 55: 719-778

[] Iqbal M, Ashraf M. Gibberellic acid mediated induction of salt tolerance in wheat plants: Growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis. Environ Exp Bot, 2013, 86: 76-85

[] Kleczewski NM, Bauer JT, Bever JD, Clay K, Reynolds HL. A survey of endophytic fungi of switchgrass (Panicum virgatum) in the Midwest, and their putative roles in plant growth. Fungal Ecol, 2012, 5: 521-529

[] Knapp DK, Pintye A, Kovács GM. The dark side is not fastidious-dark septate endophytic fungi of native and invasive plants of semiarid sandy Areas. PLoS ONE, 2012, 7 e32570

[] Kodsueb R, Dhanasekaran V, Aptroot A, Lumyong S, McKenzie EHC, Hyde KD, Jeewon R. The family Pleosporaceae: intergeneric relationships and phylogenetic perspectives based on sequence analyses of partial 28S rDNA. Mycologia, 2006, 98(4): 571-583

[] Kumar K, Gambhir G, Dass A, Tripathi AK, Singh A, Jha AK, Yadava P, Choudhary M, Rakshit S. Genetically modified crops: current status and future prospects. Planta, 2020, 251: 91

[] Li J, Liu Z, He C, Tu W, Sun Z. Are the drylands in northern China sustainable? A perspective from ecological footprint dynamics from 1990 to 2010. Sci Total Environ, 2016, 553: 223-231

[] Maestre FT, Escolar C, de Guevara ML, Quero JL, Lázaro R, Delgado-Baquerizo M, Ochoa V, Berdugo M, Gozalo B, Gallardo A. Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Glob Chang Biol, 2013, 19: 3835-3847

[] Maity A, Sharma J, Pal RK. Novel potassium solubilizing bio-formulation improves nutrient availability, fruit yield and quality of pomegranate (Punica granatum L.) in semi-arid ecosystem. Sci Hortic, 2019, 255: 14-20

[] Michel BE. Evaluation of the Water Potentials of Solutions of Polyethylene Glycol 8000 Both in the Absence and Presence of Other Solutes. Plant Physiol, 1983, 72: 66-70

[] Ministry of Agriculture, Forestry and Fisheries n.d. Soil Diagnosis Methods and Applications https://www.maff.go.jp/j/seisan/kankyo/hozen_type/h_sehi_kizyun/pdf/tuti12.pdf/.  Accessed 30 April 2024

[] Mohamed AH, Abd El-Megeed FH, Hassanein NM, Youseif SH, Farag PF, Saleh SA, Abdel-Wahab BA, Alsuhaibani AM, Helmy YA, Abdel-Azeem AM. Native rhizospheric and endophytic fungi as sustainable sources of plant growth promoting traits to improve wheat growth under low nitrogen input. J Fungi, 2022, 8: 94

[] Ondrasek G, Rengel Z, Veres S (2011) Soil Salinisation and Salt Stress in Crop Production, in: Shanker, A. K., Venkateswarlu B. (Eds.), Abiotic Stress in Plants-Mechanisms and Adaptations, INTECH WEB. pp. 171–190.

[] Pal S, Singh HB, Farooqui A et al (2015) Fungal biofertilizers in Indian agriculture: perception, demand and promotion. J Eco-friendly Agric 10:101–113. http://ecoagrijournal.com/wp-content/uploads/2019/10/Full-Paper-102.pdf

[] Piątek M, Rodriguez-Flakus P, Domic A et al (2020) Phylogenetic placement of Leptosphaeria polylepidis, a pathogen of Andean endemic Polylepis tarapacana, and its newly discovered mycoparasite Sajamaea mycophila gen. et sp. nov.. Mycol Progress 19:1–14. https://doi.org/10.1007/s11557-019-01535-w

[] Qi W, Zhao L. Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J Basic Microbiol, 2013, 53: 355-364

[] Radhakrishnan R, Kang S-M, Baek I-Y, Lee I-J. Characterization of plant growth-promoting traits of Penicillium species against the effects of high soil salinity and root disease. J Plant Interact, 2014, 9: 754-762

[] Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM. Thermotolerance generated by plant/fungal symbiosis. Science, 2002, 298: 1581

[] Rietkerk M, Dekker SC, de Ruiter PC et al (2004) Self-organized patchiness and catastrophic shifts in ecosystems. Science 305:1926–1929. https://www.science.org/doi/full/10.1126/science.1101867

[] Rodriguez RJ, White JF Jr Arnold AE, Redman RS. Fungal endophytes: diversity and functional roles. New Phytol, 2009, 182: 314-330

[] Sallam A, Alqudah AM, Dawood MFA, Stephen Baenziger PS, Börner A. Drought stress tolerance in wheat and barley: advances in physiology, breeding and genetics research. Int J Mol Sci, 2019, 20: 3137

[] Scheffer M, Carpenter S, Foley JA et al (2001) Catastrophic shifts in ecosystems. Nature 413:591–596. https://doi.org/10.1038/35098000

[] Spatafora JW, Sung GH, Johnson D et al (2006) A five-gene phylogeny of Pezizomycotina. Mycologia 98(6):1018–1028. https://doi.org/10.1080/15572536.2006.11832630

[] Sprague SJ, Howlett BJ, Kirkegaard JA. Epidemiology of root rot caused by Leptosphaeria maculans in Brassica napus crops. Eur J Plant Pathol, 2009, 125: 189-202

[] Tsatsakis AM, Nawaz MA, Kouretas D, Balias G, Savolainen K, Tutelyan VA, Golokhvast KS, Lee JD, Yang SH, Chung G. Environmental impacts of genetically modified plants: a review. Environ Res, 2017, 156: 818-833

[] Turral H, Svendsen M, Faures JM. Investing in irrigation: reviewing the past and looking to the future. Agric Water Manag, 2010, 97: 551-560

[] Van der Weele CM, Spollen WG, Sharp RE, Baskin TI. Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. J Experimental Botany, 2000, 51: 1555-1560

[] Verma S, Varma A, Rexer K-H, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Philipp Franken P. Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia, 1998, 90: 896-903

[] Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res, 2016, 184: 13-24

[] Wahid OAA, Mehana TA. Impact of phosphate-solubilizing fungi on the yield and phosphorus-uptake by wheat and faba bean plants. Microbiol Res, 2000, 155: 221-227

[] Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, Franken P, Kogel K. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. PNAS, 2005, 102: 13386-13391

[] Waqas M, Khan AL, Kamran M, Hamayun M, Kang S-M, Kim Y-H, Lee I-J. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host–plant growth during stress. Molecules, 2012, 17: 10754-10773

[] Zhao J, Zhou L, Wang J et al (2010) Endophytic fungi for producing bioactive compounds originally from their host plants. in: Méndez-Vilas A (eds) Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, FORMATEX, Spain, pp 567–576

[] Zhou L, Chen H, Hua W, Dai Y, Wei N. Mechanisms for stronger warming over drier ecoregions observed since 1979. Clim Dyn, 2016, 47: 2955-2974