Comunidades fúngicas aisladas de hojas sintomáticas de naranjilla (Solanum quitoense Lam.) en la región amazónica ecuatoriana
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Se recuperaron aislados de tejidos sintomáticos de hojas de naranjilla Solanum quitoense Lam. en la provincia de Pastaza, una región de producción importante de la región amazónica del Ecuador. Se identificaron hongos filamentosos por medio de técnicas moleculares basados en la región ITS y secuenciamiento de ADN ribosomal. De un total de 68 hongos, se recuperaron 14 taxa. La mayor cantidad de registros pertenecieron a las especies Diaporthe citri, D. schini, y Xylaria berteri. Según lo que conocemos, más del 90% de los taxones recuperados en este estudio se reportan por primera vez en S. quitoense. Los indices de diversidad sugieren que los tejidos sintomáticos representan un reservorio moderadamente diverso para especies de hongos. Por lo tanto, dichas lesiones representan una fuente significativa de moléculas con propiedades agronómicas y farmacéuticas, considerando su capacidad para sobrevivir en tejidos foliares sintomáticos. Esperamos que este estudio facilite las medidas de control biológica en cultivos neotropicales de interés comercial.
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Acosta A, Perez F, Vaillant F. 2009. Chemical characterization, antioxidant properties, and volatile constituents of naranjilla (Solanum quitoense Lam.) cultivated in Costa Rica. Arch Latinoam Nutr. 59: 88-94.
Aegerter BJ, Gordon TR, Davis RM. 2000. Occurrence and pathogenicity of fungi associated with melon root rot and vine decline in California. Plant Dis. 84: 224-230.
Agrios GN. 2005. Plant Pathology, 5th edition. London: Elsevier Academic Press. 922 p.
Álvarez E, Gañán L, Rojas-Trivino A, Mejia JF, Llano GA, González A. 2014. Diversity andpathogenicity of Colletotrichum species isolated from soursop in Colombia. Eur J Plant Pathol. 139: 325-338.
Andersen RN, Walker HL. 1985. Colletotrichum coccodes: A pathogen of eastern black nightshade (Solanum ptycanthum). Weed Sci. 33: 902-905.
Arnold AE. 2007. Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev. 21: 51-66.
Arnold AE, Herre EA. 2003. Canopy cover and leaf age affect colonization by tropical fungal endophytes: ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia. 95:388-398.
Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA. 2003. Fungal endophytes limit pathogen damage in a tropical tree. PNAS. 26: 15649-15654.
Arnold AE, Lutzoni F. 2007. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology. 88: 541-549.
Asiegbu FO, Adomas A, Stenlid JA. 2005. Conifer root and butt rot caused by Heterobasidion annosum (Fr.) Bref. sl. Mol Plan Pathol. 6: 395-409.
Backman PA, Sikora RA. 2008. Endophytes: an emerging tool for biological control. Biol Control. 46:1-3.
Bills GF. 1996. Isolation and analysis of endophytic fungal communities from woody plants. In: Redlin S, LM Carris, editors. Systematics, Ecology and Evolution of Endophytic Fungi in Grasses and Woody Plants. St Paul, USA: MNAPS Press. p. 31-65
Bruez E, Vallance J, Gerbore J, Lecomte P, Da Costa JP, Guerin-Dubrana L, Rey P. 2014. Analyses of the temporal dynamics of fungal communities colonizing healthy wood tissues of esca leaf-symptomatic and asymptomatic vines. Plos One. 9: e95928.
Brum MCP, Araujo WL, Maki CS, Azevedo JLD. 2012. Endophytic fungi from Vitis labrusca L. ('Niagara Rosada') and its potential for the biological control of Fusarium oxysporum. Genet Mol Res. 11: 4187-4197.
Cai L, Jeewon R, Hyde KD. 2006. Phylogenetic investigations of Sordariaceae based on multiple gene sequences and morphology. Mycol Res. 110: 137-150.
Cakmak I. 2005. The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci. 168: 521-530.
Cannon PF, Damm U, Johnston PR, Weir BS. 2012. Colletotrichum – current status and future directions. Stud Mycol. 73: 181-213.
Carroll GC. 1986. The biology of endophytism in plants with particular reference to woody perennials. In: Fokkema NJ, van den Heuvel J, editors. Microbiology of phyllosphere. London: Cambridge University Press. p. 205-222.
Casierra-Posada F, García EJ, Ludders P. 2004. Determinación del punto óptimo de cosecha en el lulo (Solanum quitoense Lam.) var. quitoense y septentrionale. Agron. Colomb. 2: 32-39.
Cerkauskas RF. 1988. Latent colonization by Colletotrichum spp.: epidemiological considerations and implications for mycoherbicides. Can J Plant Pathol. 10: 297-310.
Crouch JA, Clarke BB, Hillman BI. 2009. What is the value of ITS sequence data in Colletotrichum systematics and species diagnosis? A case study using the falcate-spored graminicoulous Colletotrichum group. Mycologia. 101: 648-656.
Crous PW, Verkley GJ, Groenewald E, Samson RA. 2009. CBS Laboratory Manual Series 1: Fungal Biodiversity. The Netherlands, Central Bureau voor Schimmelcultures.
Crozier J, Thomas SE, Aime MC, Evans HC, Holmes KA. 2006. Molecular characterization of fungal endophytic morphospecies isolated from stems and pods of Theobroma cacao. Plant Pathol. 55: 783-791.
Das M, Rover TV, Left LG. 2007. Diversity of fungi, and actinomycetes on leaves decomposing in a stream. Appl. Environ. Microbiol. 73: 756-767.
De Lucca AJ. 2007. Harmful fungi in both agriculture and medicine. Rev Iberoam Micol. 24: 3-13.
Del-Prado R, Cubas P, Lumbsch HT, Divakar PK, Blanco O, de Paz GA, Molina MC, Crespo A. 2010. Genetic distances within and among species in monophyletic lineages of Parmeliaceae (Ascomycota) as a tool for taxon delimitation. Mol Phylogenet Evol. 56: 125-133.
Dettrakul S, Kittakoop P, Isaka M, Nopuchal S, Suyarnsestakorn C, Tanticharoen M, Thebtaranonth Y. 2003. Antimycobacterial pimarane diterpenes from the Fungus Diaporthe sp. Bioorg Med Chem Lett. 13:1253-1255
Dreyfuss MM, Chapela IH. 1994. Potential of fungi in the discovery of novel, low-molecular weight pharmaceuticals. In: Gullo V, editor. Discovery of Novel Natural Products with Therapeutic Potential. Newnes. p. 49-80.
Fierer N, Breitbart M, Nulton J, Salamon P, Lozupone C, Jones R, Robeson M, Edwards RA, Felts B, Rayhwak S, Knight R. 2007. Metagenomic and smallsubunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl Environ Microbiol. 73: 7059-7066.
Flórez SL, Lastrilla DM, Chaves B, Fisher G, Magnitskiy S. 2008. Growth of lulo (Solanum quitoense L.) plants affected by salinity and substrate. Rev Bras Frutic. 30: 402-408.
Frohlich J, Hyde KD, Petrini O. 2000. Endophytic fungi associated with palms. Mycol Res. 104: 1201-1212.
Frohlich-Nowoisky J, Pickersqill DA, Després VR, Poschl u. 2009. High diversity of fungi in air particulate matter. Proc. Natl. Acad. Sci. USA. 106: 12814-9.
Gazis R, Chaverri P. 2010. Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol. 3: 240-254.
Ghimire SR, Charlton ND, Bell JD, Krishnamurthy YL, Craven KD. 2011. Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L.) growing in the native tallgrass prairie of northern Oklahoma. Fungal Divers. 47: 19-27.
Gomes RR, Glienke C, Videira SI, Lombard L, Groenewald JZ, Crous PW. 2013. Diaporthe: a genus of endophytic, saprobic, and plant pathogenic fungi. Persoonia. 31: 1-41.
González V, Tello ML. 2011. The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers. 47: 29-42.
Granados C, Torrenegra ME, Acevedo D, Romero P. 2013. Evaluación fisicoquímica y microbiolpogica del aperitivo vínico de lulo (Solanum quitoense L.). Inf. Tecnol. 24: 35-40.
Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW. 1997. Bacterial endophytes in agricultural crops. Can J Microbiol. 43: 895-914.
Hammer Ø, Harper DAT, Ryan PD. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron. 4: 9.
Hata K, Futai K. 1995. Endophytic fungi associated with healthy pine needles and needles infested by the pine needle gall midge, Thecodiplosis japonensis. Cana J Bot. 73: 384-390.
Hsieh HM, Lin CR, Fang MJ, Rogers JD, Fournier J, Lechat C, Ju YM. 2010. Phylogenetic status of Xylaria subgenus Pseudoxylaria among taxa of the subfamily Xylarioideae (Xylariaceae) and phylogeny of the taxa involved in the subfamily. Mol Phylogenet Evol. 54: 957-969.
Hyde KD, Soytong K. 2008. The fungal endophyte dilemma. Fungal Divers. 33: 163-173.
Hyde KD, Cai L, Cannon PF, Crouch J, Crous PW, Damn U, Goodwin PH, Chen H, Johnston PR,
Jones EBG, et al. 2009. Colletotrichum – names in current use. Fungal Divers. 39: 147-182.
Johnston PR, Sutherland PW, Joshee S. 2006. Visualizing endophytic fungi within leaves by detection of (1-3) B-D-glucans in fungal cell walls. Mycologist 20: 159-162.
Jumpponen A, Jones KL. 2009. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol. 184: 438-448.
Kharwar RN, Mishra A, Gond SK, Stierle A, Stierle D. 2011. Anticancer compounds derived from fungal endophytes: their importance and future challenges. Nat Prod Rep. 28:1208-28.
Kobayashi H, Meguro S, Yoshimoto T, Namikoshi M. 2003.Absolute structure, biosynthesis, and anti-microtubule activity of phomopsidin, isolated from a marine derived fungus Phomopsis sp. Tetrahedron. 59: 455-459.
Koh YJ, Hur JS, Jung JS. 2005. Postharvest fruit rot of kiwifruit (Actinidia deliciosa) in Korea. N Z J Crop Hortic Sci. 3: 303-310.
Koukol O, Kolarik M, Kolarova Z, Baldrian P. 2012. Diversity of foliar endophytes in wind-fallen Picea abies trees. Fungal Divers. 54: 69-77.
León J. 2000. Botánica de los cultivos tropicales, 3rd Edition. Costa Rica: Agroamérica. 522 p.
Millar CS. 1980. Infection processes on conifer needles. In: Blakeman JP, editor. Microbial ecology of the phylloplane. London: Academic Press. p 185-209.
Mohamed R, Jong PL, Zali MS. 2010. Fungal diversity in wounded stems of Aquilaria malaccensis. Fungal Divers. 43: 67-74.
Mondal SN, Vicent A, Reis RF, Timmer LW. 2007. Saprophytic colonization of citrus twigs by Diaporthe citri and factors affecting pycnidial production and conidial survival. Plant Dis. 91: 387-392.
Montes-Rojas C, Muñoz LA, Terán VF, Prado FA, Quinónez MA. 2010. Pathogenity evaluation on Solanum quitoense Lam. Clones. Acta Agron. 59: 144-154.
Okane I, Srikitikulchai P, Tabuchi Y, Sivichai S, Nakagiri A. 2012. Recognition and characterization of four Thai xylariaceous fungi inhabiting various tropical foliages as endophytes by DNA sequences and host plant preference. Mycoscience 53: 122-132.
Omacini M, Chaneton EJ, Ghersa CM, Müller CB. 2001. Symbiotic fungal endophytes control insect host–parasite interaction webs. Nature. 409:78.
Oono R, Lefevre E, Simha A, Lutzoni F. 2015. A comparison of the community diversity of foliar fungal endophytes between seedling and adult loblolly pines (Pinus taeda). Fungal Biol. 119: 917-928.
Opik M, Moora M, Liira J, Zobel M. 2006. Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J. Ecol. 94: 778-790
Osono T, Hirose D. 2001. Colonization and lignin decomposition of pine needle littler by Lophodermium pinastri. For. Pathol. 41: 156-162.
Peay KG, Kennedy PG, Talbot JM. 2016. Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol. 14:434.
Petrini O. 1991. Fungal endophytes of tree leaves. In: Andrews J, Hirano SS, editors. Microbial ecology of leaves. New York: Springer-Verlag. p. 179-197.
Petrini O. 1996. Ecological and physiological aspects of host specificity in endophytic fungi. In: Redlin SC, Carris LM, editors. Endophytic Fungi of Grasses and Woody Plants. St Paul, MN: American Phytopathological Society. p. 87-100.
Phongpaichit S, Rungjindamai N, Rukachaisirikul V, Sakayaroj J. 2006. Antimicrobial activity in cultures of endophytic fungi isolated from Garcinia species. FEMS Immunol Med Microbiol. 48: 367-372.
Photita W, Lumyong S, Lumyong P, Hyde KD. 2001. Endophytic fungi of wild banana (Musa acuminate) at Doi Suthep Pui National Park, Thailand. Mycol Res. 105: 1508-1513.
Photita W, Lumyong S, Lumyong P, McKenzie EHC, Hyde KD. 2004. Are some endophytes of Musa acuminata latent pathogens? Fungal Divers. 16: 131-140.
Prihastuti H, Cai L, Chen H, Hyde KD. 2009. Characterization of Colletotrichum species associated with coffee berries in Chiang Mai, Thailand. Fungal Divers. 39: 89-109.
Promputtha L, Lumyong S, Dhanasekaran V, McKenzie E, Hyde K, Jeewon R. 2007. A Phylogenetic Evaluation of Whether Endophytes Become Saprotrophs at Host Senescense. Microb. Ecol. 53: 579-590.
Pulido CR, Bojaca C, Salazar MR, Chaves B. 2008. Node appearance model for Lulo (Solanum quitoense L.) in the high altitude tropics. Biosyst Eng. 101: 383-387.
Quinchia CF, Cabrera CA. 2006. Manual técnico del cultivo del Lulo (Solanum quitoense Lam.) en el departamento de Huila. Gobernación del Huila. Neiva, Huila. Colombia.
Reis BMS, Silva A, Alvarez MR, Oliveira TB, Rodrigues A. 2015. Fungal communities in garden of leafcutter ant Atta cephalotes in forest and cabruca agrosystems of southern Bahia State (Brazil). Fungal Biol. 119: 1170-1178.
Revelo J, Viteri P, Vásquez W, Valverde F, León J, Gallegos P. 2010. Manual del Cultivo Ecológico de la Naranjilla. INIAP, Ecuador.
Rivera-Ordoña FN, Suárez-Sánchez RA, Flores-Bustamante ZR, Gracida-Rodriguez JN, Flores-Cotera LB. 2011. Diversity of endophytic fungi of Taxus globosa (Mexican yew). Fungal Divers. 47: 65-74.
Rogg H. 2000. Manejo integrado de plagas en cultivos de la Amazonía Ecuatoriana. Editorial Abya Yala, Quito, Ecuador.
Rungjindamai N, Pinruan U, Choeyklin R, Hattori T, Jones EBG. 2008. Molecular characterization of basidiomycetous endophytes isolated from leaves, rachis and petioles of the oil palm, Elaeis guineensis, in Thailand. Fungal Divers. 33: 139-161.
Saikkonen K, Wali P, Helander M, Faeth SH. 2004. Evolution of endophyte-plant symbioses. Trends Plant Sci. 9: 275-280.
Sánchez Márquez S, Bills GF, Zabalgogeazcoa I. 2007. The endophytic mycobiota of the grass Dactylis glomerata. Fungal Divers. 27:171-195.
Sánchez Márquez S, Bills GF, Domínguez-Acuña L, Zabalgogeazcoa I. 2010. Endophytic mycobiota of leaves and roots of the grass Holcus lanatus. Fungal Divers. 41: 115-123.
Santos JM, Vrandečić K, Ćosić J, Duvnjak T, Phillips AJL. 2011. Resolving the Diaporthe species occurring on soybean in Croatia. Persoonia. 27: 9-19.
Santos TT, Leite TS, Queiroz CB, Araujo EF, Pereira OL, Queiroz MV, 2015. High genetic variability in endophytic fungi from the genus Diaporthe isolated from common bean (Phaseolus vulgaris L.) in Brazil. J Appl Microbiol. 120: 388-401.
Schadt CW, Martin AP, Lipson DA, Schmidt SK. 2003. Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science. 301:1359-61.
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW, et al. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad. Sci. 109: 6241-6.
Schulz B, Boyle C, Draeger S, Rommert AK, Krohn K. 2002. Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res. 106: 996-1004.
Schulz B, Boyle C. 2006. What are endophytes? In: Schulz B, Boyle CJ, Sieber TN, editors. Microbial root endophytes. Berlin: Springer. p. 1-13.
Sebastianes FLS, Lacava PT, Fávaro LCL, Rodrigues MBC, Araújo WL, Azevedo JL, Pizzirani-Kleiner AA. 2011. Genetic transformation of Diaporthe phaseolorum, an endophytic fungus found in mangrove forests, mediated by Agrobacterium tumefaciens. Curr Genet. 58: 21-33.
Sebastianes FL, Cabedo N, El Aouad N, Valente AM, Lacava PT, Azevedo JL, Cortes D. 2012. 3-Hydroxypropionic acid as an antibacterial agent from endophytic fungi Diaporthe phaseolorum. Curr Microbiol. 65: 622-632.
Shannon CE, Weaver W. 1963. The Mathematical Theory of Communication. Urbana, IL: University of Illinois Press. 144 p.
Sieber T. 2007. Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev. 21: 75-89.
Simpson EH. 1949. Measurement of diversity. Nature. 163: 688.
Strobel GA. 2002. Rainforest endophytes and bioactive products. Crit Rev Biotechnol. 22:315-33.
Suryanarayanan TS, Wittlinger SK, Faeth SH. 2005. Endophytic fungi associated with cacti in Arizona. Mycol Res. 109: 635-639.
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.
Tejesvi MV, Kini KR, Prakash HS, Subbiah V, Shetty HS. 2007. Genetic diversity and antifungal activity of species of Pestalotiopsis isolated as endophytes from medicinal plants. Fungal Divers. 24: 37-54.
Thomas SE, Crozier J, Aime MC, Evans HC, Holmes KA. 2008. Molecular characterization of fungal endophytic morphospecies associated with the indigenous forest tree, Theobroma gileri, in Ecuador. Mycol Res. 112: 852-860.
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-80.
U’Ren JM, Lutzoni F, Miadlikowska J, Arnold AE. 2010. Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol. 60: 340-353.
U’Ren JM, Arnold AE. 2016. Diversity, taxonomic composition, and functional aspects of fungal communities in living, senesced, and fallen leaves at five sites across North America. Peer J 4: e2768.
Vaz ABM, Da Costa AGFC, Raad LVV, Góes-Neto A. 2014. Fungal endophytes associated with three South American Myrtae (Myrtaceae) exhibit preferences in the colonization at leaf level. Fungal Biol. 118: 277-286.
Vega FE, Simpkins A, Aime MC, Posada F, Peterson SW, Rehner SA, Infante F, Castillo A, Arnold AE. 2010. Fungal endophyte diversity in coffee plants from Colombia, Hawaii, Mexico, and Puerto Rico. Fungal Ecol. 3: 122-138.
Viret O, Petrini O. 1994. Colonisation of beech leaves (Fagus sylvatica) by the endophytes Discula umbrinella (Teleomorph: Apiognomonia errabunda). Mycol Res. 98: 423-432.
White TF, Brunus T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,. In: Innis MA, Gelfand DH, Sninsnky FS, White TT, editors. PCR Protocol: A guide to methods and applications. San Diego: Academic Press. p. 315-322.
Wikee S, Cai L, Pairin N, McKenzie EHC, Su YY, Chukeatirote E, Thi HN, Bahkali AH, Moslem MA, Abdelsalam K, Hyde KD. 2011. Colletotrichum species from Jasmine (Jasminum sambac). Fungal Divers. 46: 171-182.
Williamson B. 1994. Latency and quiescence in survival and success of fungal plant pathogens. In: Blackeman JP, Williamson B, editors. Ecology of plant pathogens. Oxford: CAB International. p. 187-207.
Wilson D. 1995. Endophyte: the evolution of a term, and clarification of its use and definition. Oikos. 73: 274-276.
Yuan Z, Chen L. 2014. The role of endophytic fungal individuals and communities in the decomposition of Pinus massoniana needle litter. PLoS ONE. 9: e105911.
Zhang AW, Hartman GL, Curio-Penny B, Pedersen WL, Becker KB. 1999. Molecular detection of Diaporthe phaseolorum and Phomopsis longicolla from soybean seeds. Phytopathol. 89: 796-804.
Zhu Y, Chen H, Fan J, Wang Y, Li Y, Chen J, Fan J, Yang S, Hu L, Leung H, et al. 2000. Genetic diversity and disease control in rice. Nature. 406:718.