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Endophytic fungi from Himalayan silver birch as potential source of plant growth enhancement and secondary metabolite production

  • Environmental Microbiology - Research Paper
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Abstract

Mountain biodiversity is under unparalleled pressure due to climate change, necessitating in-depth research on high-altitude plant’s microbial associations which are crucial for plant survival under stress conditions. Realizing that high-altitude tree line species of Himalaya are completely unexplored with respect to the microbial association, the present study aimed to elucidate plant growth promoting and secondary metabolite producing potential of culturable endophytic fungi of Himalayan silver birch (Betula utilis D. Don). ITS region sequencing revealed that the fungal isolates belong to Penicillium species, Pezicula radicicola, and Paraconiothyrium archidendri. These endophytes were psychrotolerant in nature with the potential to produce extracellular lytic activities. The endophytes showed plant growth promoting (PGP) traits like phosphorus solubilization and production of siderophore, indole acetic acid (IAA), and ACC deaminase. The fungal extracts also exhibited antagonistic potential against bacterial pathogens. Furthermore, the fungal extracts were found to be a potential source of bioactive compounds including the host-specific compound—betulin. Inoculation with fungal suspension improved seed germination and biomass of soybean and maize crops under net house conditions. In vitro PGP traits of the endophytes, supported by net house experiments, indicated that fungal association may support the growth and survival of the host in extreme cold conditions.

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Data availability

The accession numbers MZ613188.1, MN327637.1, MN327638.1, and MN327639.1 correspond to isolates GBPI beF1, GBPI beF2, GBPI beF4, GBPI beF5 respectively and the sequencing data is accessible on NCBI.

References

  1. Vimal SR, Singh JS, Arora NK et al (2017) Soil-plant-microbe interactions in stressed agriculture management: a review. Pedosphere 27:177–192

    CAS  Google Scholar 

  2. Vincent D, Rafqi M, Job D (2020) The multiple facets of plant–fungal interactions revealed through plant and fungal secretomics. Front Plant Sci 10:1626

    PubMed  PubMed Central  Google Scholar 

  3. Prathyusha P, Rajitha SAB, Ashokvardhan T (2015) Antimicrobial and siderophore activity of the endophytic fungus Acremonium sclerotigenum inhabiting Terminalia bellerica Roxb. Int J Pharm Sci Rev Res 30:84–87

    Google Scholar 

  4. Yang B, Wang XM, Ma HY et al (2015) Fungal endophyte Phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere. Front Microbiol 6:1–15

    Google Scholar 

  5. Bader AN, Salerno GL, Covacevich F et al (2020) Native Trichoderma harzianum strains from Argentina produce indole-3 acetic acid and phosphorus solubilization, promote growth and control wilt disease on tomato (Solanum lycopersicum L.). J King Saud Univ Sci 32:867–873

    Google Scholar 

  6. Zhang S, Gan Y, Xu B (2019) Mechanisms of the IAA and ACC-deaminase producing strain of Trichoderma longibrachiatum T6 in enhancing wheat seedling tolerance to NaCl stress. BMC Plant Biol 19:1–18

    Google Scholar 

  7. Chanclud E, Morel JB (2016) Plant hormones: a fungal point of view. Mol Plant Pathol 17:1289–1297

    PubMed  PubMed Central  Google Scholar 

  8. Mishra R, Kushveer JS, Revanthbabu P et al (2019) Endophytic fungi and their enzymatic potential. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer Intesrnational Publishing, Cham, pp 283–337

    Google Scholar 

  9. Jia M, Chen L, Xin HL et al (2016) A friendly relationship between endophytic fungi and medicinal plants: a systematic review. Front Microbiol 7:906

    PubMed  PubMed Central  Google Scholar 

  10. Strobel G, Daisy B, Castillo U et al (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268

    CAS  PubMed  Google Scholar 

  11. Rodriguez R, Durán P (2020) Natural holobiome engineering by using native extreme microbiome to counteract the climate change effects. Front Bioeng Biotechnol 8:568

    PubMed  PubMed Central  Google Scholar 

  12. Suryanarayanan TS, Shanker RU (2021) Can fungal endophytes fast-track plant adaptations to climate change? Fungal Ecol 50:101039

    Google Scholar 

  13. Rashmi M, Kushveer JS, Sarma VV (2019) A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10:798–1079

    Google Scholar 

  14. Qadri M, Johri S, Shah BA et al (2013) Identification and bioactive potential of endophytic fungi isolated from selected plants of the Western Himalayas. Springerplus 2:1–14

    Google Scholar 

  15. Adhikari P, Pandey A (2019) Phosphate solubilization potential of endophytic fungi isolated from Taxus wallichiana Zucc roots. Rhizosphere 9:2–9

    Google Scholar 

  16. Fatima N, Kondratyuk TP, Park EJ et al (2016) Endophytic fungi associated with Taxus fuana (West Himalayan Yew) of Pakistan: potential bio-resources for cancer chemopreventive agents. Pharm Biol 54:2547–2554

    CAS  PubMed  Google Scholar 

  17. Yuan Z, Tian Y, He F et al (2019) Endophytes from Ginkgo biloba and their secondary metabolites. Chin Med 14:1–40

    Google Scholar 

  18. Jain R, Bhardwaj P, Pandey SS et al (2021) Arnebia euchroma, a plant species of cold desert in the Himalayas, harbors beneficial cultivable endophytes in roots and leaves. Front Microbiol 12:1–16

    CAS  Google Scholar 

  19. Shaw K, Roy S, Wilson B (2014) Betula utilis. The IUCN red list of threatened species 2014:e.T194535A2346136. https://doi.org/10.2305/IUCN.UK.2014-3.RLTS.T194535A2346136.en

  20. Pandey A, Palni LMS (2007) The rhizosphere effect in trees of the Indian Central Himalaya with special reference to altitude. Appl Eco Env Res 5:93–102

    Google Scholar 

  21. Dasila K, Pandey A, Samant SS et al (2020) Endophytes associated with Himalayan silver birch (Betula utilis D. Don) roots in relation to season and soil parameters. Appl Soil Ecol 149:103513

    Google Scholar 

  22. Pandey A, Trivedi P, Kumar B et al (2006) Characterization of a phosphate solubilizing and antagonistic strain of Pseudomonas putida (B0) isolated from a sub-alpine location in the Indian Central Himalaya. Curr Microbiol 53:102–107

    CAS  PubMed  Google Scholar 

  23. Dos Santos RMG, Rodrigues-Fo E, Rocha WC et al (2003) Endophytic fungi from Melia azedarach. World J Microbiol Biotechnol 19:767–770

    Google Scholar 

  24. Woo PC, Ngan AH, Chui HK et al (2010) Agar block smear preparation: a novel method of slide preparation for preservation of native fungal structures for microscopic examination and long-term storage. J Clin Microbiol 48:3053–3061

    PubMed  PubMed Central  Google Scholar 

  25. Fauda AH, Hassan SE, Eid AM et al (2015) Biotechnological applications of fungal endophytes associated with medicinal plant Asclepias sinaica (Bioss). Ann Agric Sci 60:95–104

    Google Scholar 

  26. Dhakar K, Pandey A (2013) Laccase production from a temperature and pH tolerant fungal strain of Trametes hirsuta (MTCC 11397). Enzyme Res 2013:9

  27. Jani K, Bandal J, Rale V et al (2019) Antimicrobial resistance pattern of microorganisms isolated and identified from Godavari River across the mass gathering event. J Biosci 44:1–6

    CAS  Google Scholar 

  28. White TJ, Bruns T, Lee SJWT et al (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc: a guide to methods and applications 18:315–322

    Google Scholar 

  29. Kajale SC, Sonawane MS, Sharma R et al (2015) Leptoxyphium kurandae – new record of insect gut associated sooty mold fungus from India. Mycosphere 6:133–138

    Google Scholar 

  30. Sharma A, Jani K, Feng GD et al (2018) Subsaxibacter sediminis sp. nov., isolated from arctic glacial sediment and emended description of the genus Subsaxibacter. Int J Syst Evol Microbiol 68:1678–1682

    CAS  PubMed  Google Scholar 

  31. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  32. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  PubMed  ADS  Google Scholar 

  33. Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  35. Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270

    CAS  PubMed  Google Scholar 

  36. Ahmad F, Ahmad I, Khan MS (2005) Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk J Biol 29:29–34

    CAS  Google Scholar 

  37. Schwyn A, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    CAS  PubMed  Google Scholar 

  38. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase containing plant growth promoting rhizobacteria. Physiol Plant 118:10–15

    CAS  PubMed  Google Scholar 

  39. Singh P, Kumar V, Agrawal S (2014) Evaluation of phytase producing bacteria for their plant growth promoting activities. Int J Microbiol 2014:7

  40. Bakker AW, Shippers B (1887) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp. mediated plant growth stimulation. Soil Biol Biochem 19:451–457

    Google Scholar 

  41. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters, Analytica. Chimica Acta 27:31–36

    CAS  Google Scholar 

  42. Kerovuo J, Lauraeus M, Nurminen P, Kalkkinen N, Apajalahti J (1998) Isolation, characterization, molecular gene cloning, and sequencing of a novel phytase from Bacillus subtilis. Appl Environ Microbiol 64(6):2079–2085

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  43. Arnow LE (1937) Colorimetric determination of the components of 3, 4-dihydroxyphenylalanine–tyrosine mixtures. J Biol Chem 118:531–537

    CAS  Google Scholar 

  44. Neilands JB (1981) Microbial iron transport compounds (siderophores) as chelating agents. In: Anderson WF, Badman DG (eds) Martell E. Development of iron chelators for clinical use, Elsevier Amsterdam, pp 13–31

    Google Scholar 

  45. Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831

    CAS  Google Scholar 

  46. Jasim B, John Jimtha C, Jyothis M et al (2013) Plant growth promoting potential of endophytic bacteria isolated from Piper nigrum. Plant Growth Regul 71:1–11

    CAS  Google Scholar 

  47. Dasila K, Singh M (2022) Bioactive compounds and biological activities of Elaegnus latifolia L.: an underutilized fruit of North-East Himalaya, India. S Afr J Bot 45:177–185

    Google Scholar 

  48. Kirk PM, Cannon PF, Minter DW et al (2008) Dictionary of the fungi Wallingford. CABI, UK, p 335

    Google Scholar 

  49. Dhakar K, Sharma A, Pandey A (2014) Cold, pH and salt tolerant Penicillium spp. inhabit the high-altitude soils in Himalaya, India. World J Microbiol Biotechnol 30:1315–1324

    CAS  PubMed  Google Scholar 

  50. Nicoletti R, Fiorentino A, Scognamiglio M (2014) Endophytism of Penicillium species in woody plants. Open Mycol J 8:1–26

    Google Scholar 

  51. Hassan SED (2017) (2017) Plant growth-promoting activities for bacterial and fungal endophytes isolated from medicinal plant of Teucrium polium L. J Adv Res 8:687–695

    PubMed  PubMed Central  Google Scholar 

  52. Pombeiro-Sponchiado SR, Sousa GS, Andrade JC et al (2017) Production of melanin pigment by fungi and its biotechnological applications. Melanin 1(4):47–75

  53. Perez-Cuesta U, Aparicio-Fernandez L, Guruceaga X et al (2020) Melanin and pyomelanin in Aspergillus fumigatus: from its genetics to host interaction. Int Microbiol 23:55–63

    CAS  PubMed  Google Scholar 

  54. Krain A, Siupka P (2021) Fungal guttation, a source of bioactive compounds, and its ecological role- a review. Biomolecules 11(9):1270

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Farrar K, Bryant D, Cope-Selby N (2014) Understanding and engineering beneficial plant–microbe interactions: plant growth promotion in energy crops. Plant Biotechnol J 12:1193–1206

    PubMed  PubMed Central  Google Scholar 

  56. Jhala YK, Panpatte DG, Adetunji CO et al (2020) Management of biotic and abiotic stress affecting agricultural productivity using beneficial microorganisms isolated from higher altitude agro-ecosystems: a remedy for sustainable agriculture. In: Goel R, Soni R, Suyal DH (eds) Microbiological advancements for higher altitude agro-ecosystems & sustainability. Springer, Singapore, pp 113–134

    Google Scholar 

  57. Wang M, Tian J, Xiang M et al (2017) Living strategy of cold-adapted fungi with the reference to several representative species. Mycology 8:178–188

    PubMed  PubMed Central  Google Scholar 

  58. Moghaddam MSH, Soltani J (2014) Psychrophilic endophytic fungi with biological activity inhabit Cupressaceae plant family. Symbiosis 63:79–86

    Google Scholar 

  59. Li HY, Li DW, He CM et al (2012) Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb–Zn mine wasteland in China. Fungal Ecol 5:309–315

    Google Scholar 

  60. Hoshino T, Xiao N, Tkachenko OB (2009) Cold adaptation in the phytopathogenic fungi causing snow molds. Mycoscience 50:26–38

    Google Scholar 

  61. Dhakar K, Pandey A (2016) Wide pH range tolerance in extremophiles: towards understanding an important phenomenon for future biotechnology. Appl Microbiol Biotechnol 100:2499–2510

    CAS  PubMed  Google Scholar 

  62. Gupta A, Singh SK, Singh MK et al (2019) Plant growth-promoting rhizobacteria and their functional role in salinity stress management. In: Singh P, Kumar A, Borthakur A (eds). Abatement of environmental pollutants: trends and strategies, Elsevier, Cambridge: MA, USA, 151–60

  63. Bal HB, Nayak L, Das S et al (2013) Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil 366:93–105

    CAS  Google Scholar 

  64. Toghueo RMK, Zabalgogeazcoa I, de Aldana BV et al (2017) Enzymatic activity of endophytic fungi from the medicinal plants Terminalia catappa, Terminalia mantaly and Cananga odorata. S Afr J Bot 109:146–153

    CAS  Google Scholar 

  65. Choudhary DK, Prakash A, John BN (2007) Induced systemic resistance (ISR) in plants: mechanism of action. Indian J Microbiol 47(4):289–297

    CAS  PubMed  Google Scholar 

  66. Etemadi M, Gutjahr C, Couzigou JM et al (2014) Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol 166:281–292

    PubMed  PubMed Central  Google Scholar 

  67. Chand K, Shah S, Sharma J et al (2020) Isolation, characterization, and plant growth-promoting activities of endophytic fungi from a wild orchid Vanda cristata. Plant Signal Behav 15:1744294

    PubMed  PubMed Central  Google Scholar 

  68. Yadav AN (2021) Beneficial plant-microbe interactions for agricultural sustainability. J Appl Biol Biotechnol 9:1–4

    Google Scholar 

  69. Saeed S, Barozai MYK, Ahmad A et al (2014) Impact of altitude on soil physical and chemical properties in SraGhurgai (Takatu mountain range) Quetta, Balochistan. Int J Sci Eng Res 5:730–735

    Google Scholar 

  70. Goswami D, Thakker JN, Dhandhukia PN (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500

    Google Scholar 

  71. Sharma A, Johri B, Sharma A et al (2003) Plant growth-promoting bacterium Pseudomonas sp. strain GRP3 influences iron acquisition in mung bean (Vigna radiata L. Wilzeck). Soil Biol Biochem 35:887–894

    CAS  Google Scholar 

  72. Sessitsch A, Kuffner M, Kidd P et al (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Glick BR, Todorovic B, Czarny J et al (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242

    CAS  Google Scholar 

  74. Hardoim P, Van-Overbeek L, Van-Elsas J (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    CAS  PubMed  Google Scholar 

  75. Chen X, Sang X, Li S et al (2010) Studies on a chlorogenic acid-producing endophytic fungi isolated from Eucommia ulmoides Oliver. J Ind Microbiol Biotechnol 37:447–454

    CAS  PubMed  Google Scholar 

  76. Thalavaipandian B, Ramesh V, Arivudainambi USE et al (2012) A novel endophytic fungus Pestalotiopsis sp. inhabiting Pinus caneriensis with antibacterial and antifungal potential. Int J Adv Life Sci 2:1–7

    Google Scholar 

  77. Gherbawy YA, Elhariry HM (2016) Endophytic fungi associated with high-altitude Juniperus trees and their antimicrobial activities. Plant Biosyst 150:131–140

    Google Scholar 

  78. Bhardwaj A, Sharma D, Jadon N et al (2015) Antimicrobial and phytochemical screening of endophytic fungi isolated from spikes of Pinus roxburghii. Arch Clin Microbiol 6:1–9

    Google Scholar 

  79. Gauchan DP, Kandel P, Tuladhar A et al (2020) Evaluation of antimicrobial, antioxidant and cytotoxic properties of bioactive compounds produced from endophytic fungi of Himalayan yew (Taxuswallichiana) in Nepal. F1000Research 9:379

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Moghaddam MG, Ahmad FBH, Samzadeh-Kermani A (2012) Biological activity of betulinic acid: a review. Pharmacol Pharm 3:1–5

    Google Scholar 

  81. Stierle A, Strobel G, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260:214–216

    CAS  PubMed  ADS  Google Scholar 

  82. Yang X, Guo S, Zhang L et al (2003) Select of producing podophyllotoxin endophytic fungi from podophyllin plant. Nat Prod Res Dev 12:419–422

    Google Scholar 

  83. Cui Y, Yi D, Bai X et al (2012) Ginkgolide B produced endophytic fungus (Fusarium oxysporum) isolated from Ginkgo biloba. Fitoterapia 83:913–920

    CAS  PubMed  Google Scholar 

  84. Wang Y, Dai CC (2011) Endophytes: a potential resource for biosynthesis, biotransformation, and biodegradation. Ann Microbiol 61:207–215

    CAS  Google Scholar 

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Acknowledgements

Director, G. B. Pant National Institute of Himalayan Environment, India, is acknowledged for providing the facilities. Advance Instrumentation Research Facility (AIRF)- Jawaharlal Nehru University (JNU), India, is acknowledged for extending the GC/MS facilities. Sequencing was performed at Centre for Excellence, National Centre for Microbial Resource, NCCS, Pune.

Funding

The work was supported by the National Mission on Himalayan Studies (NMHS Reference No.: GBPNI/NMHS- 2018/NSMW/SG29).

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Authors and Affiliations

  1. Center for Environmental Assessment and Climate Change, G.B. Pant National Institute of Himalayan Environment, Kosi-Katarmal, Almora, 263643, Uttarakhand, India

    Khashti Dasila, Anita Pandey & Mithilesh Singh

  2. Department of Biotechnology, Graphic Era (Deemed to Be University), Bell Road, Clement Town, Dehradun, 248002, Uttarakhand, India

    Anita Pandey

  3. National Centre for Microbial Resource, National Centre for Cell Science, Pune, 41107, Maharashtra, India

    Avinash Sharma

  4. School of Agriculture, Graphic Era Hill University, Dehradun, 248002, India

    Avinash Sharma

  5. Himalayan Forest Research Institute, Conifer Campus, Panthaghati, Shimla, 171013, Himachal Pradesh, India

    Sher S. Samant

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  1. Khashti Dasila
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Contributions

KD: conceptualization, methodology, experimentation, analysis, writing; AP: conceptualization, investigation, supervision, validation, review, editing; AS: molecular identification and phylogeny; MS: review; SSS: plant identification and sample collection; MS: review; MS: supervision, review, editing.

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Correspondence to Anita Pandey or Mithilesh Singh.

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Dasila, K., Pandey, A., Sharma, A. et al. Endophytic fungi from Himalayan silver birch as potential source of plant growth enhancement and secondary metabolite production. Braz J Microbiol 55, 557–570 (2024). https://doi.org/10.1007/s42770-024-01259-4

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