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Isolation and molecular characterization of the fungal endophytic microbiome from conventionally and organically grown avocado trees in South Florida

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An Erratum to this article was published on 13 September 2016

Abstract

Fungal endophytes are the most ubiquitous and highly diverse microorganisms that inhabit the interior of healthy plants. They are important in plant ecology and offer untapped potential to improve plant health and productivity in agroecosystems. The endophytic assemblage of avocado is poorly understood; therefore, surveys of fungal endophytes of Persea americana Mill. (Avocado) in South Florida organic and conventional orchards were conducted. A total of 17 endophytic fungal species were recovered from healthy avocado terminal branches. Endophytic fungal species were identified by rDNA sequencing of the internal transcribed spacer (ITS) region, using UNITE Species Hypotheses to reliably assign a taxon name, and determined as belonging to the genera Alternaria, Cladosporium, Colletotrichum, Corynespora, Diaporthe, Lasiodiplodia, Neofusicoccum, Neopestalotiopsis, Phyllosticta, and Strelitziana. Endophyte community assemblage differed between organic and conventional agroecosystems. This is the first report of Alternaria eichhorniae, Cladosporium tenuissimum, Corynespora cassiicola, Colletotrichum alatae, Diaporthe fraxini-angustifoliae, Lasiodiplodia gonubiensis, Neofusicoccum algeriense, Neofusicoccum andinum, Neopestalotiopsis foedans, Phyllosticta capitalensis, and Strelitziana africana as endophytes of avocado. Evaluation using pathogenicity tests on avocado leaves and terminal branches showed that endophytic fungal isolates did not cause disease symptoms.

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References

  • Afkhami ME, Strauss SY (2016) Native fungal endophytes suppress an exotic dominant and increase plant diversity over small and large spatial scales. Ecology 97:1159–1169

    Article  PubMed  Google Scholar 

  • Alfieri SA Jr, Langdon KR, Wehlburg C, Kimbrough JW (1984) Index of Plant Diseases in Florida (Revised). Florida Dept. Agric. and Consumer Serv., Div. Plant Ind Bull 11:1–389

    Google Scholar 

  • Arzanlou M, Crous PW (2006) Strelitziana africana. Fungal Planet 8:2

    Google Scholar 

  • Ayoubi N, Soleimani MJ (2015) Strawberry fruit rot Caused by Neopestalotiopsis iranensis sp. nov., and N. mesopotamica. Curr Microbiol 72:329–336

    PubMed  Google Scholar 

  • Azad K, Kaminskyj S (2016) A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis 68:73–78

    Article  CAS  Google Scholar 

  • Bacon CW, White JF (2000) Microbial endophytes. Marcel Dekker, New York

    Google Scholar 

  • Berg G, Rybakova D, Grube M, Köberl M (2016) The plant microbiome explored: implications for experimental botany. J Exp Bot 67:995–1002

    Article  PubMed  Google Scholar 

  • Bergh BO (1995) Avocado. In: Smartt J, Simmonds NW (eds) Evolution of crop plants. Longman Scientific & Technical, Harlow, pp 240–245

    Google Scholar 

  • Berraf-Tebbal A, Guerreiro MA, Phillips AJL (2014) Phylogeny of Neofusicoccum species associated with grapevine trunk diseases in Algeria, with description of Neofusicoccum algeriense sp. nov. Phytopathol Mediterr 53:416–427

    CAS  Google Scholar 

  • Busby PE, Ridout M, Newcombe G (2016) Fungal endophytes: modifiers of plant disease. Plant Mol Biol 90:645–655

    Article  CAS  PubMed  Google Scholar 

  • Camatti-Sartori V, da Silva-Ribeiro RT, Valdebenito-Sanhueza RM, Pagnocca FC, Echeverrigaray S, Azevedo JL (2005) Endophytic yeasts and filamentous fungi associated with southern Brazilian apple (Malus domestica) orchards subjected to conventional, integrated or organic cultivation. J Basic Microbiol 45:397–402

    Article  PubMed  Google Scholar 

  • Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum—current status and future directions. Stud Mycol 73:181–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll GC (1990) Fungal endophytes in vascular plants: mycological research opportunities in Japan. Trans Mycol Soc Jpn 31:103–116

    Google Scholar 

  • Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth

  • Crous PW, Slippers B, Wingfield MJ, Rheeder J, Marasas WFO, Philips AJL, Alves A, Burgess T, Barber P, Groenewald JZ (2006) Phylogenetic lineages in the Botryosphaeriaceae. Stud Mycol 55:235–253

    Article  PubMed  PubMed Central  Google Scholar 

  • Daisy BH, Strobel GA, Castillo U, Ezra D, Sears J, Weaver DK, Runyon JB (2002) Naphthalene, an insect repellent, is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology 148:3737–3741

    Article  CAS  PubMed  Google Scholar 

  • Déon M, Scomparin A, Tixier A, Mattos CRR, Leroy T, Seguin M, Roeckel-Drevet P, Pujade-Renaud V (2012) First characterization of endophytic Corynespora cassiicola isolates with variant cassiicolin genes recovered from rubber trees in Brazil. Fungal Divers 54:87–99

    Article  Google Scholar 

  • Ek-Ramos MJ, Zhou W, Valencia CU, Antwi JB, Kalns LL, Morgan GD, Kerns DL, Sword GA (2013) Spatial and temporal variation in fungal endophyte communities isolated from cultivated cotton (Gossypium hirsutum). PLoS One 8:e66049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans EA, Lozano IB (2014) Sample avocado production costs and profitability analysis for Florida. EDIS #FE837. UF/IFAS Extension, Gainesville, FL

  • Farr DF, Bills GF, Chamuris GP, Rossman AY (1989) Fungi on plants and plant products in the United States. APS Press, St. Paul

    Google Scholar 

  • Farr DF, Rossman AY (2011) Fungal databases. Systematic Mycology and Microbiology Laboratory, ARS, USDA. http://nt.ars-grin.gov/fungaldatabases/

  • Fraedrich SW, Harrington TC, Rabaglia RJ, Ulyshen MD, Mayfield AE III, Hanula JL, Eickwort JM, Miller DR (2008) A fungal symbiont of the redbay ambrosia beetle causes a lethal wilt in redbay and other Lauraceae in the southeastern United States. Plant Dis 92:215–224

    Article  Google Scholar 

  • Gao YH, Su YY, Sun W, Cai L (2015) Diaporthe species occurring on Lithocarpus glabra in China, with descriptions of five new species. Fungal Biol 119:295–309

    Article  PubMed  Google Scholar 

  • García A, Rhoden SA, Rubin Filho CJ, Nakamura CV, Pamphile JA (2012) Diversity of foliar endophytic fungi from the medicinal plant Sapindus saponaria L. and their localization by scanning electron microscopy. Biol Res 45:139–148

    Article  PubMed  Google Scholar 

  • Gomes RR, Glienke C, Videira SIR, Lombard L, Groenewald JZ, Crous PW (2013) Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31:1–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillén-Sánchez D, de Jesús Yañez-Morales M, Téliz-Ortíz D, Siebe-Grabach C, Bautista-Baños S (2007) Morphological and molecular characterization of Cladosporium tenuissimum Cooke (Deuteromycotina: Hyphomycetes) on mango tree panicles: symptoms, pathogenicity and severity of the fungus. Fruits 62:361–368

    Article  Google Scholar 

  • Hakizimana JD, Gryzenhout M, Coutinho TA, van den Berg N (2011) Endophytic diversity in Persea americana (avocado) trees and their ability to display biocontrol activity against Phytophthora cinnamomi. In: Proceedings of the VII World Avocado Congress 2011, Cairns, Australia, 5–9 September 2011

  • Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed  PubMed Central  Google Scholar 

  • Hata K, Futai K (1995) Endophytic fungi associated with healthy pine needles and needles infested by the pine needle gall midge, Thecodiplosis japonensis. Can J Botany 73:384–390

    Article  Google Scholar 

  • Hubbard M, Germida JJ, Vujanovic V (2014) Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second-generation seed viability. J Appl Microbiol 116:109–122

    Article  CAS  PubMed  Google Scholar 

  • Jayawardena RS, Zhang W, Liu M, Maharachchikumbura SS, Zhou Y, Huang J, Nilthong S, Wang Z, Li X, Yan J, Hyde KD (2015) Identification and characterization of Pestalotiopsis-like fungi related to grapevine diseases in China. Fungal Biol 119:348–361

    Article  PubMed  Google Scholar 

  • Kim CK, Eo JK, Eom AH (2013) Diversity and seasonal variation of endophytic fungi isolated from three conifers in Mt. Taehwa, Korea. Mycobiology 41:82–85

    Article  PubMed  PubMed Central  Google Scholar 

  • Ko TWK, Stephenson SL, Bahkali AH, Hyde KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers 50:113–120

    Article  Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martin MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Wei M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Article  PubMed  Google Scholar 

  • Lebeis SL, Rott M, Dangl JL, Schulze-Lefert P (2012) Culturing a plant microbiome community at the cross-Rhodes. New Phytol 196:341–344

    Article  PubMed  Google Scholar 

  • Lima NB, Batista MVdeA, de Morais MA Jr, Barbosa MAG, Michereff SJ, Hyde KD, Câmara MPS (2013) Five Colletotrichum species are responsible for mango anthracnose in northeastern Brazil. Fungal Divers 61:75–88

    Article  Google Scholar 

  • Martín JA, Witzell J, Blumenstein K, Rozpedowska E, Helander M, Sieber TN, Gil L (2013) Resistance to Dutch elm disease reduces presence of xylem endophytic fungi in elms (Ulmus spp.). PLoS One 8(2):e56987

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayfield AE III, Smith JA, Hughes M, Dreaden T (2008) First report of Laurel wilt disease caused by a Raffaelea sp. on avocado in Florida. Plant Dis 92:976

    Article  Google Scholar 

  • McDonald V, Eskalen A (2011) Botryosphaeriaceae species associated with avocado branch cankers in California. Plant Dis 95:1465–1473

    Article  Google Scholar 

  • Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43:145–155

    Article  Google Scholar 

  • Mohali SR, Slippers B, Wingfield MJ (2009) Pathogenicity of seven species of the Botryosphaeriaceae on Eucalyptus clones in Venezuela. Australas Plant Pathol 38:135–140

    Article  Google Scholar 

  • O’Brien D (2012) Addressing a new threat to avocado: laurel wilt. http://agresearchmag.ars.usda.gov/2012/oct/avocado. Accessed 6 January 2016

  • Pavlic D, Slippers B, Coutinho TA, Gryzenhout M, Wingfield MJ (2004) Lasiodiplodia gonubiensis sp. nov., a new Botryosphaeria anamorph from native Syzygium cordatum in South Africa. Stud Mycol 50:313–322

    Google Scholar 

  • Paz-Vega R (2015) Avocado production, marketing and consumption: a global perspective. In: Proceedings of the VIII World Avocado Congress, Lima, Peru, 13–18 September 2015. http://industry.nzavocado.co.nz/resources/4564754/Avocado_production__marketing_and_consumption_presentation.pdf. Accessed June 10, 2016

  • Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer-Verlag, New York, NY, pp 179–197

    Chapter  Google Scholar 

  • Ploetz RC, Benscher D, Vazquez A, Colls A, Nagel J, Schaffer B (1996) A reexamination of mango decline in Florida. Plant Dis 80:664–668

    Article  Google Scholar 

  • Ploetz RC, Peña JE, Smith JA, Dreaden TJ, Crane JH, Schubert T, Dixon W (2011) Laurel wilt, caused by Raffaelea lauricola, is confirmed in Miami-Dade County, center of Florida’s commercial avocado production. Plant Dis 95:1589

    Article  Google Scholar 

  • Ploetz RC, Pérez-Martínez JM, Smith JA, Hughes M, Dreaden TJ, Inch SA, Fu Y (2012) Responses of avocado to laurel wilt, caused by Raffaelea lauricola. Plant Pathol 61:801–808

    Article  Google Scholar 

  • Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopath 49:291–315

    Article  CAS  Google Scholar 

  • Punithalingam E (1980) Plant diseases attributed to Botryodiplodia theobromae Pat (Bibliotheca Mycologica). J Cramer, Vaduz Berlin

    Google Scholar 

  • Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716

    Article  Google Scholar 

  • Rodriguez R, Redman R (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

    Article  CAS  PubMed  Google Scholar 

  • Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331

    Article  PubMed  Google Scholar 

  • Rossman AY, Farr DF, Castlebury LA (2007) A review of the phylogeny and biology of the Diaporthales. Mycoscience 48:135–144

    Article  Google Scholar 

  • Rozpądek P, Wężowicz K, Nosek M, Ważny R, Tokarz K, Lembicz M, Miszalski Z, Turnau K (2015) The fungal endophyte Epichloë typhina improves photosynthesis efficiency of its host orchard grass (Dactylis glomerata). Planta 242:1025–1035

    Article  PubMed  PubMed Central  Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  • Shabana YM, Baka ZA, Abdel-Fattah GM (1997) Alternaria eichhorniae, a biological control agent for waterhyacinth: mycoherbicidal formulation and physiological and ultrastructural host responses. Eur J Plant Pathol 103:99–111

    Article  CAS  Google Scholar 

  • Sharma JK, Heather WA (1978) Parasitism of uredospores of Melampsora larici-populina Kleb. by Cladosporium sp. Eur J Forest Pathol 8:48–54

    Article  Google Scholar 

  • Singh B, Kaur T, Kaur S, Manhas RK, Kaur A (2016) Insecticidal potential of an endophytic Cladosporium velox against Spodoptera litura mediated through inhibition of alpha glycosidases. Pestic Biochem Physiol 131:46–52

    Article  CAS  PubMed  Google Scholar 

  • Tan YP, Edwards J, Grice KR, Shivas RG (2013) Molecular phylogenetic analysis reveals six new species of Diaporthe from Australia. Fungal Divers 61:251–260

    Article  Google Scholar 

  • Tkacz A, Poole P (2015) Role of root microbiota in plant productivity. J Exp Bot 66:2167–2175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Twizeyimana M, Förster H, McDonald V, Wang DH, Adaskaveg JE, Eskalen A (2013) Identification and pathogenicity of fungal pathogens associated with stem-end rot of avocado in California. Plant Dis 97:1580–1584

    Article  Google Scholar 

  • Udayanga D, Liu X, McKenzie EHC, Chukeatirote E, Bahkali AHA, Hyde KD (2011) The genus Phomopsis: biology, applications, species concepts and names of common phytopathogens. Fungal Divers 50:189–225

    Article  Google Scholar 

  • United States Department of Agriculture (USDA)/National Agricultural Statistics Service (NASS) (2015) Noncitrus fruits and nuts: 2014 Summary. July 2015. ISSN: 1948–2698. USDA/NASS, Washington, DC. http://www.usda.gov/nass/PUBS/TODAYRPT/ncit0715.pdf. Accessed 12 June 2016

  • Vieira WA, Michereff SJ, de Morais MA Jr, Hyde KD, Câmara MPS (2014) Endophytic species of Colletotrichum associated with mango in northeastern Brazil. Fungal Divers 67:181–202

    Article  Google Scholar 

  • Walker DM, Castlebury LA, Rossman AY, Sogonov MV, White JF (2010) Systematics of genus Gnomoniopsis (Gnomoniaceae, Diaporthales) based on a three gene phylogeny, host associations and morphology. Mycologia 102:1479–1496

    Article  PubMed  Google Scholar 

  • Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99:2955–296

    Article  CAS  PubMed  Google Scholar 

  • Watling R, Turnbull E (1998) Cantharellaceae, Gomphaceae and amyloid-spored and xeruloid members of Tricholomataceae (excl. Mycena). In: Henderson DM, Orton PD, Watling R, Gregory NM, Howell KMR (eds) British fungus flora 8. Alden, United Kingdom. 189 pp

    Google Scholar 

  • Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Wikee S, Lombard L, Crous PW, Nakashima C, Motohashi K, Chukeatirote E, Alias SA, McKenzie EHC, Hyde KD (2013) Phyllosticta capitalensis, a widespread endophyte of plants. Fungal Divers 60:91–105

    Article  Google Scholar 

  • Wilson D (1995) Endophyte: The evolution of a term, and clarification of its use and definition. Oikos 73:274–276

    Article  Google Scholar 

  • Yahia EM (2012) Avocado. In: Rees D, Farrell G, Orchard J (eds) Crop post-harvest: science and technology: perishables. Wiley-Blackwell, Oxford, UK, pp 159–179

    Chapter  Google Scholar 

  • Yang SM, Dowler WM, Johnson DR (1991) Comparison of methods for selecting fungi pathogenic to leafy spurge. Plant Dis 75:1201–1203

    Article  Google Scholar 

  • Yao X, Christensen MJ, Bao G, Zhang C, Li X, Li C, Nan Z (2015) A toxic endophyte-infected grass helps reverse degradation and loss of biodiversity of over-grazed grasslands in northwest China. Sci Rep 5:18527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeilinger S, Gupta VK, Dahms TE, Silva RN, Singh HB, Upadhyay RS, Gomes EV, Tsui CK, Nayak SC (2016) Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiol Rev 40:182–207

    Article  PubMed  Google Scholar 

  • Zhang JX, Xu T, Ge QX (2003) Notes on Pestalotiopsis from Southern China. Mycotaxon 85:91–92

    Google Scholar 

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Acknowledgments

DMW would like to thank Lucy Yanckello for help with microscopy. DVR would like to acknowledge partial funding by USDA-NIFA Hispanic Serving Institutions Grant 2011-38422-30804. The authors are grateful to Mr. Robert Barnum (Possum trot tropical nursery) for helping with the sample collection and also Madora Krome Farm for allowing us to collect samples and for sharing information on their farming practices.

The authors would like to thank the two anonymous reviewers for their helpful comments to improve this manuscript.

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  1. Department of Earth and Environment, Florida International University, Miami, FL, 33199, USA

    Kateel G. Shetty, Diana V. Rivadeneira & Krish Jayachandran

  2. Department of Biology, Tennessee Technological University, Cookeville, TN, 38505, USA

    Donald M. Walker

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  1. Kateel G. Shetty
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An erratum to this article can be found at http://dx.doi.org/10.1007/s11557-016-1226-4.

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Shetty, K.G., Rivadeneira, D.V., Jayachandran, K. et al. Isolation and molecular characterization of the fungal endophytic microbiome from conventionally and organically grown avocado trees in South Florida. Mycol Progress 15, 977–986 (2016). https://doi.org/10.1007/s11557-016-1219-3

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