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Diversity of root-endophytic Trichoderma from Malaysian Borneo

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Abstract

Trichoderma species form endophytic associations with plant roots and may provide a range of benefits to their hosts. However, few studies have systematically examined the diversity of Trichoderma species associated with plant roots in tropical regions. During the evaluation of Trichoderma isolates for use as biocontrol agents, root samples were collected from more than 58 genera in 35 plant families from a range of habitats in Malaysian Borneo. Trichoderma species were isolated from surface-sterilised roots and identified following analysis of partial translation elongation factor-1α (tef1) sequences. Species present included Trichoderma afroharzianum, Trichoderma asperelloides, Trichoderma asperellum, Trichoderma guizhouense, Trichoderma reesei, Trichoderma strigosum and Trichoderma virens. Trichoderma asperellum/T. asperelloides, Trichoderma harzianum s.l. and T. virens were the most frequently isolated taxa. tef1 sequence data supported the recognition of undescribed species related to the T. harzianum complex. The results suggest that tropical plants may be a useful source of novel root-associated Trichoderma for biotechnological applications.

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References

  • Asis A, Siddiquee S (2015) Identification of Trichoderma species from wet paddy field soil samples. Trans Sci Technol (In press)

  • Atanasova L, Jaklitsch WM, Komoń-Zelazowska M, Kubicek CP, Druzhinina IS (2010) Clonal species Trichoderma parareesei sp. nov. likely resembles the ancestor of the cellulase producer Hypocrea jecorina/T. reesei. Appl Environ Microbiol 76:7259–7267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey BA, Melnick RL (2013) The endophytic Trichoderma. In: Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M (ed) Trichoderma: biology and applications. CABI, Wallingford, pp 52–172

    Google Scholar 

  • Benítez T, Rincón AM, Limón MC, Codón AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260

    PubMed  Google Scholar 

  • Bissett J (1991) A revision of the genus Trichoderma. III. Section Pachybasium. Can J Bot 69:2373–2417

    Article  Google Scholar 

  • Bissett J, Gams W, Jaklitsch W, Samuels GJ (2015) Accepted Trichoderma names in the year 2015. IMA Fungus 6:263–295

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaverri P, Samuels GJ (2013) Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of interkingdom host jumps and major shifts in ecology. Evolution 67:2823–2837

    PubMed  Google Scholar 

  • Chaverri P, Castlebury LA, Samuels GJ, Geiser DM (2003) Multilocus phylogenetic structure within the Trichoderma harzianum/Hypocrea lixii complex. Mol Phylogenet Evol 27:302–313

    Article  CAS  PubMed  Google Scholar 

  • Chaverri P, Gazis RO, Samuels GJ (2011) Trichoderma amazonicum, a new endophytic species on Hevea brasiliensis and H. guianensis from the Amazon basin. Mycologia 103:139–151

    Article  PubMed  Google Scholar 

  • Chaverri P, Branco-Rocha F, Jaklitsch W, Gazis R, Degenkolb T, Samuels GJ (2015) Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia 107:558–590

    Article  CAS  PubMed  Google Scholar 

  • Dang L, Li G, Yang Z, Luo S, Zheng X, Zhang K (2010) Chemical constituents from the endophytic fungus Trichoderma ovalisporum isolated from Panax notoginseng. Ann Microbiol 60:317–320

    Article  CAS  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Respinis S, Vogel G, Benagli C, Tonolla M, Petrini O, Samuels GJ (2010) MALDI-TOF MS of Trichoderma: a model system for the identification of microfungi. Mycol Prog 9:79–100

    Article  Google Scholar 

  • Druzhinina I, Kubicek CP (2005) Species concepts and biodiversity in Trichoderma and Hypocrea: from aggregate species to species clusters. J Zhejiang Univ Sci B 6:100–112

    Article  PubMed  PubMed Central  Google Scholar 

  • Druzhinina IS, Kopchinskiy AG, Komoń M, Bissett J, Szakacs G, Kubicek CP (2005) An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet Biol 42:813–828

    Article  CAS  PubMed  Google Scholar 

  • Druzhinina IS, Komoń-Zelazowska M, Atanasova L, Seidl V, Kubicek CP (2010a) Evolution and ecophysiology of the industrial producer Hypocrea jecorina (Anamorph Trichoderma reesei) and a new sympatric agamospecies related to it. PLoS One 5:e9191

    Article  PubMed  PubMed Central  Google Scholar 

  • Druzhinina IS, Kubicek CP, Komoń-Zelazowska M, Mulaw TB, Bissett J (2010b) The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages. BMC Evol Biol 10:94

    Article  PubMed  PubMed Central  Google Scholar 

  • Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elad Y (1996) Mechanisms involved in the biological control of Botrytis cinerea incited diseases. Eur J Plant Pathol 102:719–732

    Article  Google Scholar 

  • Gherbawy Y, Druzhinina I, Shaban GM, Wuczkowsky M, Yaser M, El-Naghy MA, Prillinger H-J, Kubicek CP (2004) Trichoderma populations from alkaline agricultural soil in the Nile valley, Egypt, consist of only two species. Mycol Prog 3:211–218

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) PhyML: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Harman GE (2000) Myths and dogmas of biocontrol changes in perceptions derived from research on Trichoderma harzinum T-22. Plant Dis 84:377–393

    Article  Google Scholar 

  • Harman GE (2011) Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytol 189:647–649

    Article  PubMed  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  PubMed  Google Scholar 

  • Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25

    Article  CAS  PubMed  Google Scholar 

  • Hill RA, Ambrose A, Sajali NA, Yatim M, Valdez RB, Agbayani F, Bungang J, Minchin R, Stewart A (2010) Bioprotection of Acacia mangium using Trichoderma in Malaysia. In: Zydenbos SM, Jackson TA (eds) Microbial products: exploiting microbial diversity for sustainable plant production. New Zealand Plant Protection Society, Christchurch, pp 51–55

    Google Scholar 

  • Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10

    Article  Google Scholar 

  • Hoyos-Carvajal L, Bissett J (2011) Biodiversity of Trichoderma in neotropics. In: Grillo O, Venora G (eds) The dynamical processes of biodiversity—case studies of evolution and spatial distribution. InTech, Rijeka, pp 303–320

    Google Scholar 

  • Hoyos-Carvajal L, Orduz S, Bissett J (2009) Genetic and metabolic biodiversity of Trichoderma from Colombia and adjacent neotropic regions. Fungal Genet Biol 46:615–631

    Article  CAS  PubMed  Google Scholar 

  • Jaklitsch WM (2009) European species of Hypocrea part I. The green-spored species. Stud Mycol 63:1–91

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaklitsch WM (2011) European species of Hypocrea part II: species with hyaline ascospores. Fungal Divers 48:1–250

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaklitsch WM, Voglmayr H (2015) Biodiversity of Trichoderma (Hypocreaceae) in Southern Europe and Macaronesia. Stud Mycol 80:1–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamala T, Indira Devi S, Chandradev Sharma K, Kennedy K (2015) Phylogeny and taxonomical investigation of Trichoderma spp. from Indian region of Indo-Burma biodiversity hot spot region with special reference to Manipur. BioMed Res Int 2015; 285261

    Article  PubMed  PubMed Central  Google Scholar 

  • Kubicek CP, Bissett J, Druzhinina I, Kullnig-Gradinger C, Szakacs G (2003) Genetic and metabolic diversity of Trichoderma: a case study on South-East Asian isolates. Fungal Genet Biol 38:310–319

    Article  CAS  PubMed  Google Scholar 

  • Kubicek CP, Komon-Zelazowska M, Druzhinina IS (2008) Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J Zhejiang Univ Sci B 9:753–763

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuhls K, Lieckfeldt E, Samuels GJ, Kovacs W, Meyer W, Petrini O, Gams W, Börner T, Kubicek CP (1996) Molecular evidence that the asexual industrial fungus Trichoderma reesei is a clonal derivative of the ascomycete Hypocrea jecorina. Proc Natl Acad Sci U S A 93:7755–7760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kullnig C, Szakacs G, Kubicek CP (2000) Molecular identification of Trichoderma species from Russia, Siberia and the Himalaya. Mycol Res 104:1117–1125

    Article  CAS  Google Scholar 

  • Lee SS, Alias SA, Jones EBG, Zainuddin N, Chan HT (2012) Checklist of fungi of Malaysia (research pamphlet no. 132). Forest Research Institute Malaysia, Kepong, 527 pp

    Google Scholar 

  • Li Q-R, Tan P, Jiang Y-L, Hyde KD, Mckenzie EHC, Bahkali AH, Kang J-C, Wang Y (2013) A novel Trichoderma species isolated from soil in Guizhou, T. guizhouense. Mycol Prog 12:167–172

    Article  Google Scholar 

  • Lieckfeldt E, Cavignac Y, Fekete C, Börner T (2000a) Endochitinase gene-based phylogenetic analysis of Trichoderma. Microbiol Res 155:7–15

    Article  CAS  PubMed  Google Scholar 

  • Lieckfeldt E, Kullnig C, Samuels GJ, Kubicek CP (2000b) Sexually competent, sucrose- and nitrate-assimilating strains of Hypocrea jecorina (Trichoderma reesei) from South American soils. Mycologia 92:374–380

    Article  Google Scholar 

  • López-Quintero CA, Atanasova L, Franco-Molano AE, Gams W, Komon-Zelazowska M, Theelen B, Müller WH, Boekhout T, Druzhinina I (2013) DNA barcoding survey of Trichoderma diversity in soil and litter of the Colombian lowland Amazonian rainforest reveals Trichoderma strigosellum sp. nov. and other species. Antonie van Leeuwenhoek 104:657–674

    Article  PubMed  PubMed Central  Google Scholar 

  • Migheli Q, Balmas V, Komoñ-Zelazowska M, Scherm B, Fiori S, Kopchinskiy AG, Kubicek CP, Druzhinina IS (2009) Soils of a Mediterranean hot spot of biodiversity and endemism (Sardinia, Tyrrhenian Islands) are inhabited by pan-European, invasive species of Hypocrea/Trichoderma. Environ Microbiol 11:35–46

    Article  CAS  PubMed  Google Scholar 

  • Mpika J, Kébé IB, Issali AE, N’Guessan FK, Druzhinina S, Komon-Zélazowska M, Kubicek CP, Aké S (2009) Antagonist potential of Trichoderma indigenous isolates for biological control of Phytophthora palmivora the causative agent of black pod disease on cocoa (Theobroma cacao L.) in Côte d’Ivoire. Afr J Biotechnol 8:5280–5293

    Google Scholar 

  • Mulaw TB, Druzhinina IS, Kubicek CP, Atanasova L (2013) Novel endophytic Trichoderma spp. isolated from healthy Coffea arabica roots are capable of controlling coffee tracheomycosis. Diversity 5:750–766

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Naeimi S, Khodaparast S, Javan-Nikkhah M, Vágvölgyi C, Kredics L (2011) Species pattern and phylogenetic relationships of Trichoderma strains in rice fields of southern Caspian Sea, Iran. Cereal Res Commun 39:560–568

    Article  Google Scholar 

  • Naik BS, Shashikala J, Krishnamurthy YL (2009) Study on the diversity of endophytic communities from rice (Oryza sativa L.) and their antagonistic activities in vitro. Microbiol Res 164:290–296

    Article  CAS  PubMed  Google Scholar 

  • Narisawa K, Kawamata H, Currah RS, Hashiba T (2002) Suppression of Verticillium wilt in eggplant by some fungal root endophytes. Eur J Plant Pathol 108:103–109

    Article  Google Scholar 

  • Park YH, Lee SG, Ahn DJ, Kwon TR, Park SU, Lim HS, Bae H (2012) Diversity of fungal endophytes in various tissues of Panax ginseng Meyer cultivated in Korea. J Ginseng Res 36:211–217

    Article  PubMed  PubMed Central  Google Scholar 

  • Quilliam RS, Jones DL (2010) Fungal root endophytes of the carnivorous plant Drosera rotundifolia. Mycorrhiza 20:341–348

    Article  PubMed  Google Scholar 

  • Quilliam RS, Jones DL (2012) Evidence for host-specificity of culturable fungal root endophytes from the carnivorous plant Pinguicula vulgaris (Common Butterwort). Mycol Prog 2:583–585

    Article  Google Scholar 

  • Reino JL, Guerrero RF, Hernández-Galán R, Collado IG (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7:89–123

    Article  CAS  Google Scholar 

  • Samuels GJ, Hebbar PK (2015) Trichoderma: identification and agricultural applications. American Phytopathological Society Press, St. Paul, MN, 204 pp

    Google Scholar 

  • Samuels GJ, Lieckfeldt E, Nirenberg HI (1999) Trichoderma asperellum, a new species with warted conidia, and redescription of T. viride. Sydowia 51:71–88

    Google Scholar 

  • Samuels GJ, Ismaiel A, Bon MC, De Respinis S, Petrini O (2010) Trichoderma asperellum sensu lato consists of two cryptic species. Mycologia 102:944–966

    Article  CAS  PubMed  Google Scholar 

  • Samuels GJ, Ismaiel A, Mulaw TB, Szakacs G, Druzhinina IS, Kubicek CP, Jaklitsch WM (2012) The Longibrachiatum clade of Trichoderma: a revision with new species. Fungal Divers 55:77–108

    Article  PubMed  PubMed Central  Google Scholar 

  • Sato H, Tanabe AS, Toju H (2015) Contrasting diversity and host association of ectomycorrhizal basidiomycetes versus root-associated ascomycetes in a dipterocarp rainforest. PLoS One 10; e0125550

    Article  PubMed  PubMed Central  Google Scholar 

  • Saw LG, Chung RCK (2005) Towards the flora of Malaysia. In: Chua LSL, Kirton LG, Saw LG (eds) Proceedings of the seminar and workshop: status of biological diversity in Malaysia and threat assessment of plant species in Malaysia. Forest Research Institute Malaysia, Kepong, pp 211–227

    Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW, Miller AN (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109:6241–6246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shoukouhi P, Bissett J (2009) Preferred primers for sequencing the 5′ end of the translation elongation factor 1-alpha gene (eEF1a1). International Subcommission on Trichoderma and Hypocrea Taxonomy. http://www.isth.info/methods (accessed 1/2/2015)

  • Sieber TN (2002) Fungal root endophytes. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 887–917

    Google Scholar 

  • Stewart A, Hill R (2014) Applications of Trichoderma in plant growth promotion. In: Gupta VK, Schmoll M, Herrera-Estrella A, Upadhyay RS, Druzhinina I, Tuohy MG (ed) Biotechnology and biology of Trichoderma. Elsevier, Amsterdam, pp 415–428

    Chapter  Google Scholar 

  • Sun RY, Liu ZC, Fu K, Fan L, Chen J (2012) Trichoderma biodiversity in China. J Appl Genet 53:343–354

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor JW, Jacobson DJ, Fisher MC (1999) The evolution of asexual fungi: reproduction, speciation and classification. Annu Rev Phytopathol 37:197–246

    Article  CAS  PubMed  Google Scholar 

  • Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21–32

    Article  CAS  PubMed  Google Scholar 

  • Toju H, Yamamoto S, Sato H, Tanabe AS (2013) Sharing of diverse mycorrhizal and root-endophytic fungi among plant species in an oak-dominated cool–temperate forest. PLoS One 8; e78248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma VC, Gond SK, Kumar A, Kharwar RN, Boulanger L-A, Strobel GA (2011) Endophytic fungal flora from roots and fruits of an Indian Neem plant Azadirachta indica A. Juss., and impact of culture media on their isolation. Indian J Microbiol 51:469–476

    Article  PubMed  PubMed Central  Google Scholar 

  • Wuczkowski M, Druzhinina I, Gherbawy Y, Klug B, Prillinger H, Kubicek CP (2003) Species pattern and genetic diversity of Trichoderma in a mid-European, primeval floodplain-forest. Microbiol Res 158:125–133

    Article  CAS  PubMed  Google Scholar 

  • Xia X, Lie TK, Qian X, Zheng Z, Huang Y, Shen Y (2011) Species diversity, distribution, and genetic structure of endophytic and epiphytic Trichoderma associated with banana roots. Microb Ecol 61:619–625

    Article  PubMed  Google Scholar 

  • Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zachow C, Berg C, Müller H, Meincke R, Komon-Zelazowska M, Druzhinina IS, Kubicek CP, Berg G (2009) Fungal diversity in the rhizosphere of endemic plant species of Tenerife (Canary Islands): relationship to vegetation zones and environmental factors. ISME J 3:79–92

    Article  CAS  PubMed  Google Scholar 

  • Zhang CL, Druzhinina IS, Kubicek CP, Xu T (2005) Trichoderma biodiversity in China: evidence for a North to South distribution of species in East Asia. FEMS Microbiol Lett 251:251–257

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was funded in part by: The Royal Society of New Zealand International Mobility Fund (IMF10-B38), Lincoln University Research Fund (LURF2009-26) and the Tertiary Education Commission (Bio-Protection Research Centre). We wish to thank Mahmad Yatim for supplying the samples from Sabah.

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Authors and Affiliations

  1. Bio-Protection Research Centre, Lincoln University, P.O. Box 85084, Lincoln, 7647, New Zealand

    N. J. Cummings, M. Braithwaite, A. Stewart, J. Steyaert & R. A. Hill

  2. Sarawak Forestry Corporation, Lot 218, KLCD, Jalan Tapang, Kota Sentosa, 93250, Kuching, Sarawak, Malaysia

    A. Ambrose & J. Abdullah

  3. Agriculture and Agri-Food Canada, 960 Carling Ave., Ottawa, Ontario, K1A 0C6, Canada

    J. Bissett

  4. Department of Molecular Biology, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia

    H. A. Roslan

  5. Grand Perfect Sdn Bhd, Bintulu, Sarawak, Malaysia

    F. V. Agbayani

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  1. N. J. Cummings
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  2. A. Ambrose
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Cummings, N.J., Ambrose, A., Braithwaite, M. et al. Diversity of root-endophytic Trichoderma from Malaysian Borneo. Mycol Progress 15, 50 (2016). https://doi.org/10.1007/s11557-016-1192-x

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