Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Diversity and Plant Growth-Promoting Effects of Fungal Endophytes Isolated from Salt-Tolerant Plants

  • Khalmuratova, Irina (School of Life Science and Biotechnology, Kyungpook National University) ;
  • Choi, Doo-Ho (School of Life Science and Biotechnology, Kyungpook National University) ;
  • Woo, Ju-Ri (School of Life Science and Biotechnology, Kyungpook National University) ;
  • Jeong, Min-Ji (School of Life Science and Biotechnology, Kyungpook National University) ;
  • Oh, Yoosun (School of Life Science and Biotechnology, Kyungpook National University) ;
  • Kim, Young-Guk (School of Life Science and Biotechnology, Kyungpook National University) ;
  • Lee, In-Jung (School of Applied Biosciences, Kyungpook National University) ;
  • Choo, Yeon-Sik (Department of Biology, College of National Sciences, Kyungpook National University) ;
  • Kim, Jong-Guk (School of Life Science and Biotechnology, Kyungpook National University)
  • Received : 2020.07.01
  • Accepted : 2020.08.28
  • Published : 2020.11.28
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Abstract

Fungal endophytes are symbiotic microorganisms that are often found in asymptomatic plants. This study describes the genetic diversity of the fungal endophytes isolated from the roots of plants sampled from the west coast of Korea. Five halophytic plant species, Limonium tetragonum, Suaeda australis, Suaeda maritima, Suaeda glauca Bunge, and Phragmites australis, were collected from a salt marsh in Gochang and used to isolate and identify culturable, root-associated endophytic fungi. The fungal internal transcribed spacer (ITS) region ITS1-5.8S-ITS2 was used as the DNA barcode for the classification of these specimens. In total, 156 isolates of the fungal strains were identified and categorized into 23 genera and two phyla (Ascomycota and Basidiomycota), with Dothideomycetes and Sordariomycetes as the predominant classes. The genus Alternaria accounted for the largest number of strains, followed by Cladosporium and Fusarium. The highest diversity index was obtained from the endophytic fungal group associated with the plant P. australis. Waito-C rice seedlings were treated with the fungal culture filtrates to analyze their plant growth-promoting capacity. A bioassay of the Sm-3-7-5 fungal strain isolated from S. maritima confirmed that it had the highest plant growth-promoting capacity. Molecular identification of the Sm-3-7-5 strain revealed that it belongs to Alternaria alternata and is a producer of gibberellins. These findings provided a fundamental basis for understanding the symbiotic interactions between plants and fungi.

Keywords

References

  1. 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. https://doi.org/10.4161/cib.1.1.6238
  2. Selosse MA, Baudoin E, Vandenkoornhuyse P. 2004. Symbiotic microorganisms, a key for ecological success and protection of plants. C. R. Biol. 327: 639-648. https://doi.org/10.1016/j.crvi.2003.12.008
  3. Rodriguez RJ, Redman RS, Henson JM. 2004. The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang 9: 261-272. https://doi.org/10.1023/B:MITI.0000029922.31110.97
  4. Thomas F, Morris JT, Wigand C, Sievert SM. 2019. Short-term effect of simulated salt marsh restoration by sand-amendment on sediment bacterial communities. PLoS One 14: e0215767. https://doi.org/10.1371/journal.pone.0215767
  5. Rodriguez RJ, Redman RS. 2008. More than 400 million years of evolution and some plants still can't make it on their own: plant stress tolerance via fungal symbiosis. J. Exp. Bot. 59: 1109-1114. https://doi.org/10.1093/jxb/erm342
  6. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, et al. 2008. Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2: 404-416. https://doi.org/10.1038/ismej.2007.106
  7. Sang-Mo K, Abdul Latif K, Young-Hyun Y, Muhammad K. 2014. Gibberellin production by newly isolated strain Leifsonia soli SE134 and its potential to promote plant growth. J. Microbiol. Biotechnol. 24: 106-112. https://doi.org/10.4014/jmb.1304.04015
  8. Nair DN, Padmavathy S. 2014. Impact of endophytic microorganisms on plants, environment and humans. ScientificWorldJournal 2014: 250693.
  9. Nalini MS, Sunayana N, Prakash HS. 2014. Endophytic fungal diversity in medicinal plants of western ghats, India. Int. J. Biodivers 2014: Doi: 10.1155/2014/494213.
  10. Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, et al. 2012. Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol. 12: 3. https://doi.org/10.1186/1471-2180-12-3
  11. Khan SA, Hamayun M, Khan AL, Lee IJ, Shinwari ZK, Kim JG. 2012. Isolation of plant growth promoting endophytic fungi from dicots inhabiting coastal sand dunes of Korea. Pak J. Botechnol. 44: 1453-1460.
  12. Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, et al. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc. Natl. Acad. Sci. USA 100: 15649-15654. https://doi.org/10.1073/pnas.2533483100
  13. Ernst M, Mendgen KW, Wirsel SG. 2003. Endophytic fungal mutualists: seed-borne Stagonospora spp. enhance reed biomass production in axenic microcosms. Mol. Plant Microbe Interact. 16: 580-587. https://doi.org/10.1094/MPMI.2003.16.7.580
  14. Kedar A, Rathod D, Yadav A, Agarkar G, Rai M. 2014. Endophytic Phoma sp. isolated from medicinal plants promote the growth of Zea mays. Nusantara Bioscie. 6: 132-139.
  15. Kim H, You YH, Yoon H, Seo Y, Kim YE, Choo YS, et al. 2014. Culturable fungal endophytes isolated from the roots of coastal plants inhabiting Korean East Coast. Mycobiol. 42: 100-108. https://doi.org/10.5941/MYCO.2014.42.2.100
  16. Tayung K, Sarkar M, Baruah P. 2012. Endophytic fungi occurring in Ipomoea carnea tissues and their antimicrobial potentials. Braz. Arch Biol. Technol. 55: 653-660. https://doi.org/10.1590/S1516-89132012000500003
  17. Redondo-Gomez S, Castillo JM, Luque CJ, Luque T, Figueroa M, Davy AJ. 2007. Fundamental niche differentiation in subspecies of Sarcocornia perennis on a salt marsh elevational gradient. Mar. Ecol. Prog. Ser. 347: 15-20. https://doi.org/10.3354/meps07041
  18. Ullah I, Khan AR, Jung BK, Khan AL, Lee IJ, Shin JH. 2014. Gibberellins synthesized by the entomopathogenic bacterium, Photorhabdus temperata M1021 as one of the factors of rice plant growth promotion. J. Plant Interact 9: 775-782. https://doi.org/10.1080/17429145.2014.942956
  19. Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR. 2011. The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81: 169-193. https://doi.org/10.1890/10-1510.1
  20. Cahoon DR, Lynch JC, Roman CT, Schmit JP, Skidds DE. 2019. Evaluating the relationship among wetland vertical development, elevation capital, sea-level rise, and tidal marsh sustainability. Estuaries Coast. 42: 1-15. https://doi.org/10.1007/s12237-018-0448-x
  21. Ahmad N, Hamayun M, Khan SA, Khan AL, Lee IJ, Shin DH. 2010. Gibberellin-producing endophytic fungi isolated from Monochoria vaginalis. J. Microbiol. Biotechnol. 20: 1744-1749. https://doi.org/10.4014/jmb.1005.05018
  22. Hamayun M, Khan SA, Khan AL, Tang DS, Hussain J, Ahmad B, et al. 2010. Growth promotion of cucumber by pure cultures of gibberellin-producing Phoma sp. GAH7. World J. Microbiol. Biotechnol. 26: 889-894. https://doi.org/10.1007/s11274-009-0248-3
  23. Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I, et al. 2010. Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp. MH-6 isolated from cucumber (Cucumis sativus L.). Mycologia 102: 989-995. https://doi.org/10.3852/09-261
  24. Yamada A, Ogura T, Degawa Y, Ohmasa M. 2001. Isolation of Tricholoma matsutake and T. bakamatsutake cultures from fieldcollected ectomycorrhizas. Mycoscience 42: 43-50. https://doi.org/10.1007/BF02463974
  25. Vazquez MM, Cesar S, Azcon R, Barea JM. 2000. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Agric., Ecosyst. Environ., Appl. Soil Ecol. 15: 261-272.
  26. You YH, Kang SM, Choo YS, Lee JM. 2012. Fungal diversity and plant growth promotion of endophytic fungi from six halophytes in Suncheon Bay. J. Microbiol. Biotechnol. 22: 1549-1556. https://doi.org/10.4014/jmb.1205.05010
  27. You YH, Yoon HJ, Seo YG, Kim MA, Shin JH, Lee IJ, et al. 2012. Analysis of Genomic Diversity of Endophytic Fungal Strains Isolated from the Roots of Suaeda japonica and S. maritima for the Restoration of Ecosystems in Buan Salt Marsh. Korean J. Microbiol. Biotechnol. 40: 287-295. https://doi.org/10.4014/kjmb.1207.07025
  28. Hill TC, Walsh KA, Harris JA, Moffett BF. 2003. Using ecological diversity measures with bacterial communities. FEMS Microbiol. Ecol. 43: 1-11. https://doi.org/10.1016/S0168-6496(02)00449-X
  29. Wearn JA, Sutton BC, Morley NJ, Gange AC. 2012. Species and organ specificity of fungal endophytes in herbaceous grassland plants. J. Ecol. 100: 1085-1092. https://doi.org/10.1111/j.1365-2745.2012.01997.x
  30. Fisher RA, Corbet AS, Williams CB. 1943. The relation between the number of species and the number of individuals in a random sample of an animal population. J. Anim. Ecol. 12: 42-58. https://doi.org/10.2307/1411
  31. Hill MO. 1973. Diversity and evenness: a unifying notation and its consequences. Ecology 54: 427-432. https://doi.org/10.2307/1934352
  32. Hughes AR, Cebrian J, Heck K, Goff J, Hanley TC, Scheffel W, et al. 2018. Effects of oil exposure, plant species composition, and plant genotypic diversity on salt marsh and mangrove assemblages. Ecosphere 9: e02207.
  33. Choi WY, Rim SO, Lee JH, Lee JM, Lee IJ, Cho KJ, et al. 2005. Isolation of gibberellins-producing fungi from the root of several Sesamum indicum plants. J. Microbiol. Biotechnol. 15: 22-28.
  34. De-Aldana BRV, Bills G, Zabalgogeazcoa I. 2013. Are endophytes an important link between airborne spores and allergen exposure?. Fungal Divers. 60: 33-42. https://doi.org/10.1007/s13225-013-0223-z
  35. Sun X, Guo LD. 2012. Endophytic fungal diversity: review of traditional and molecular techniques. Mycology 3: 65-76.
  36. Sun Y, Wang Q, Lu X, Okane I, Kakishima M. 2011. Endophytic fungi associated with two Suaeda species growing in alkaline soil in China. Mycosphere 2: 239-248.
  37. You YH, Seo YG, Yoon HJ, Kim H, Khalmuratova I, Rim SO, et al. 2013. Endophytic Fungal Diversity Associated with the Roots of Coastal Sand-dune Plants in the Sindu-ri Coastal Sand Dune, Korea. Korean J. Microbiol. Biotechnol. 41: 300-310. https://doi.org/10.4014/kjmb.1305.05003
  38. You YH, Yoon H, Kang SM, Woo JR, Choo YS, Lee IJ, et al. 2013. Cadophora malorum Cs‐8‐1 as a new fungal strain producing gibberellins isolated from Calystegia soldanella. J. Basic Microbiol. 53: 630-634. https://doi.org/10.1002/jobm.201200002
  39. De-Souza-Sebastianes FL, Romao-Dumaresq AS, Lacava PT, Harakava R, Azevedo JL, De-Melo IS, et al. 2013. Species diversity of culturable endophytic fungi from Brazilian mangrove forests. Curr. Genet. 59: 153-166. https://doi.org/10.1007/s00294-013-0396-8
  40. Colwell RK. 2009. Biodiversity: concepts, patterns, and measurement. pp.257-263. The Princeton guide to ecology.
  41. Singh LP, Gill SS, Tuteja N. 2011. Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6: 175-191. https://doi.org/10.4161/psb.6.2.14146
  42. Khan SA, Hamayun M, Yoon H, Kim HY, Suh SJ, Hwang SK, et al. 2008. Plant growth promotion and Penicillium citrinum. BMC Microbiol. 8: 231. https://doi.org/10.1186/1471-2180-8-231
  43. You YH, Hwang JS, Yoon HJ, Khan SA, Rim SO, Bae JJ, et al. 2010. Plant Growth Promotion of Calystegia soldanella and Ischaemum anthephoroides by the Strain Penicillium citrinum KACC43900. J. Life Sci. 20: 1373-1377. https://doi.org/10.5352/JLS.2010.20.9.1373
  44. Waqas M, Khan AL, Hamayun M, Shahzad R, Kim YH, Choi KS, et al. 2015. Endophytic infection alleviates biotic stress in sunflower through regulation of defence hormones, antioxidants and functional amino acids. Eur. J. Plant Pathol. 141: 803-824. https://doi.org/10.1007/s10658-014-0581-8
  45. Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S. 2004. Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16: 367-378. https://doi.org/10.1105/tpc.018143
  46. Ganley RJ, Sniezko RA, Newcombe G. 2008. Endophyte-mediated resistance against white pine blister rust in Pinus monticola. For. Ecol. Manage. 255: 2751-2760. https://doi.org/10.1016/j.foreco.2008.01.052
  47. Mejia LC, Rojas EI, Maynard Z, Van Bael S, Arnold AE, Hebbar P, et al. 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol. Control 46: 4-14. https://doi.org/10.1016/j.biocontrol.2008.01.012
  48. Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ. 2011. Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol. Biochem. 49: 852-861. https://doi.org/10.1016/j.plaphy.2011.03.005
  49. Khan AL, Waqas M, Khan AR, Hussain J, Kang SM, Gilani SA, et al. 2013. Fungal endophyte Penicillium janthinellum LK5 improves growth of ABA-deficient tomato under salinity. World J. Microbiol. Biotechnol. 29: 2133-2144. https://doi.org/10.1007/s11274-013-1378-1
  50. Teale WD, Paponov IA, Palme K. 2006. Auxin in action: signalling, transport and the control of plant growth and development. Nat. Rev. Mol. Cell Biol. 7: 847-859. https://doi.org/10.1038/nrm2020
  51. Hasan HAH. 2002. Gibberellin and auxin-indole production by plant root-fungi and their biosynthesis under salinity-calcium interaction. Acta Microbiol. Immunol. Hung. 49: 105-118. https://doi.org/10.1556/AMicr.49.2002.1.11
  52. Zhang F, Yuan J, Yang X, Cui Y, Chen L, Ran W, et al. 2013. Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil 368: 433-444. https://doi.org/10.1007/s11104-012-1519-6
  53. You YH, Kwak TW, Kang SM, Lee MC, Kim JG. 2015. Aspergillus clavatus Y2H0002 as a New Endophytic Fungal Strain Producing Gibberellins Isolated from Nymphoides peltata in Fresh Water. Mycobiology 43: 87-91. https://doi.org/10.5941/MYCO.2015.43.1.87
  54. Kawanade Y, Yamane H, Murayama T, Takahashi N, Nakamura T. 1983. Identification of gibberellin A3 in mycelia of Neurospora crassa. Agric. Biol. Chem. 47: 1693-1694. https://doi.org/10.1271/bbb1961.47.1693
  55. Hamayun M, Khan SA, Khan MA, Khan AL, Kang SM, Kim SK, et al. 2009. Gibberellin production by pure cultures of a new strain of Aspergillus fumigatus. World J. Microbiol. Biotechnol. 25: 1785-1792. https://doi.org/10.1007/s11274-009-0078-3
  56. Khan SA, Hamayun M, Kim HY, Yoon HJ, Seo JC, Choo YS, et al. 2009. A new strain of Arthrinium phaeospermum isolated from Carex kobomugi Ohwi is capable of gibberellin production. Biotechnol. Lett. 31: 283-287. https://doi.org/10.1007/s10529-008-9862-7

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