Ascomycete; Basidiomycete; coffee rust; fungal diversity; mycoparasites; OTUs; Ecology; Ecological Modeling; Agricultural and Biological Sciences (miscellaneous); Nature and Landscape Conservation
Abstract :
[en] Coffee production worldwide is affected by the pathogen Hemileia vastatrix, which causes the “coffee rust” disease and may be associated with other fungi. Ecuador lacks studies on fungal diversity associated with coffee rust, which could potentially control or escalate pathogen activity. Using the ITS-5.8S nrDNA region, we randomly detected a small preliminary fungi diversity related to coffee rust in Ecuador, which we report here for the first time. Ten coffee farms (four in Loja, three in Calvas, and three in Quilanga) from the Loja Province were sampled to analyze the genetic diversity of the pathogen Hemileia vastatrix in rust lesions on coffee leaves. A high number of selected sequences (Sanger sequencing) showed the presence of 48 OTUs (Operational Taxonomic Units) or “hypothetical species” of Ascomycetes and Basidiomycetes distributed across all the sampled farms. The genera Akanthomyces, Ceramothyrium, Cladosporium, Didymella, Fusarium, Mycosphaerella, Neoceratosperma, and Trichothecium of Ascomycetes, as well as Bulleribasidium, Hannaella, and Meira of Basidiomycetes, were the most abundant. To avoid taxonomic conflict, some sequences were placed into Capnodiales (Ascomycetes) and Tremelalles (Basidiomycetes) without a genus definition. A new phylogenetic group of sequences is considered Incertae Sedis from Basidiomycetes. Additionally, morphospecies of Akanthomyces (synonymous with some Lecanicillium species) and Colletotrichum were observed macroscopically and microscopically growing closely with rust. Most of the OTUs probably correspond to rust mycoparasites, as previously reported in the literature. However, this study is limited by the number of sequences analyzed phylogenetically, which may hinder the discovery of significant insights. Future studies are needed to determine whether this preliminary fungal diversity is associated with the rust fungus or corresponds to ubiquitous airborne fungi. Furthermore, research into the function of these species may reveal whether they promote rust pathogenicity or enhance plant responses by activating resistance mechanisms.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Cruz, Darío ; MS2E Research Group, Departamento de Ciencias Biológicas y Agropecuarias, Universidad Técnica Particular de Loja, Loja, Ecuador ; Instituto Nacional de Biodiversidad INABIO, Quito, Ecuador
Jaramillo Riofrio, Andrea Carolina ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS) ; Instituto Nacional de Biodiversidad INABIO, Quito, Ecuador ; MS2E Research Group, Departamento de Ciencias de la Salud, Universidad Técnica Particular de Loja, Loja, Ecuador
Herrera, Paulo ; MS2E Research Group, Departamento de Ciencias Biológicas y Agropecuarias, Universidad Técnica Particular de Loja, Loja, Ecuador
Aguinsaca, Ruth; Facultad Agropecuaria y de Recursos Naturales Renovables, Universidad Nacional de Loja, Loja, Ecuador
Chamba, Marianela; Programa de Posgrado Biotecnología Agropecuaria, Universidad Técnica Particular de Loja, Loja, Ecuador
Language :
English
Title :
Fungal Diversity Detected by ITS-5.8S from Coffea arabica Leaves Infected by Rust (Hemileia vastatrix) in Southern Ecuador
Publication date :
October 2024
Journal title :
Diversity
eISSN :
1424-2818
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI)
This research was funded by the Vicerrectorado de Investigación of the Universidad Técnica Particular de Loja with a grant of two thousand US dollars ($2000).
Venegas Sánchez S. Orellana Bueno D. Pérez Jara P. La realidad Ecuatoriana en la producción de café RECIMUNDO Rev. Cient. Investig. Conoc. 2018 2 72 91 10.26820/recimundo/2.(2).2018.72-91
Arreaga-Ronquillo E. Quezada-Campoverde J. Barrezueta-Unda S. Cervantes-Alava A. Prado-Carpio E. Impacto económico generado por la producción cafetalera en Ecuador en el periodo 2016–2019 593 Digit. Publ. CEIT 2021 6 83 91 10.33386/593dp.2021.6.732
Ríos-Orjuela J.C. Falcón-Espitia N. Arias-Escobar A. Plazas-Cardona D. Conserving Biodiversity in Coffee Agroecosystems: Insights from a Herpetofauna Study in the Colombian Andes with Sustainable Management Proposal Perspect. Ecol. Conserv. 2024 22 196 204 10.1016/j.pecon.2024.04.001
Wasim S. Kukkar V. Awad V.M. Sakhamuru S. Malik B.H. Neuroprotective and Neurodegenerative Aspects of Coffee and Its Active Ingredients in View of Scientific Literature Cureus 2020 12 e9578 10.7759/cureus.9578
Ungvari Z. Kunutsor S.K. Coffee Consumption and Cardiometabolic Health: A Comprehensive Review of the Evidence GeroScience 2024 10.1007/s11357-024-01262-5
Avelino J. Cristancho M. Georgiou S. Imbach P. Aguilar L. Bornemann G. Läderach P. Anzueto F. Hruska A. Morales C. The coffee rust crises in Colombia and Central America (2008–2013): Impacts, plausible causes and proposed solutions Food Secur. 2015 7 303 321 10.1007/s12571-015-0446-9
Fernández F. Gúia para Facilitar el Aprendizaje en el Manejo del Cultivo de Café Robusta (Coffe canephora p.) Guía de Aprendizaje Instituto Nacional de Investigaciones Agropecuarias (INIAP) Quito, Ecuador 2017 008 134 Available online: https://www.bivica.org/file/view/id/6061 (accessed on 5 October 2024)
Ponce L. Orellana K. Acuña I. Alfonso J. Fuentes T. Situation of the Ecuadorian Coffee Industry: Perspectives Estud. Desarro. Soc. 2018 6 307 325
Talhinhas P. Batista D. Diniz I. Vieira A. Silva D. Loureiro A. Tavares S. Pereira A. Azinheira H. Guerra-Guimarães L. et al. The coffee leaf rust pathogen Hemileia vastatrix: One and a half centuries around the tropics Mol. Plant Pathol. 2017 18 1039 1051 10.1111/mpp.12512
Castillo N.E.T. Acosta Y.A. Parra-Arroyo L. Martínez-Prado M.A. Rivas-Galindo V.M. Iqbal H.M.N. Bonaccorso A.D. Melchor-Martínez E.M. Parra-Saldívar R. Towards an Eco-Friendly Coffee Rust Control: Compilation of Natural Alternatives from a Nutritional and Antifungal Perspective Plants 2022 11 2745 10.3390/plants11202745
Silva M. Guerra-Guimarães L. Diniz I. Loureiro A. Azinheira H. Pereira A. Tavares S. Batista D. Várzea V. An Overview of the Mechanisms Involved in Coffee-Hemileia vastatrix Interactions: Plant and Pathogen Perspectives Agronomy 2022 12 326 10.3390/agronomy12020326
De Resende M. Pozza E. Reichel T. Botelho D. Strategies for Coffee Leaf Rust Management in Organic Crop Systems Agronomy 2021 11 1865 10.3390/agronomy11091865
Kapeua-Ndacnou M. de Abreu L.M. de Macedo D.M. da Nóbrega T.F. Pereira C.M. Evans H.C. Barreto R.W. Assessing the biocontrol potential of Clonostachys species isolated as endophytes from Coffea species and as mycoparasites of Hemileia rusts of coffee in Africa J. Fungi 2023 9 248 10.3390/jof9020248 36836362
Peng Y. Li S. Yan J. Tang Y. Cheng J. Gao A. Yao X. Ruan J. Xu B. Research Progress on Phytopathogenic Fungi and Their Role as Biocontrol Agents Front. Microbiol. 2021 12 670135 10.3389/fmicb.2021.670135
De Oliveira Junqueira A. De Melo Pereira G. Coral Medina J. Alvear M. Rosero R. de Carvalho Neto D. Enríquez H. Soccol C. First description of bacterial and fungal communities in Colombian coffee beans fermentation analysed using Illumina-based amplicon sequencing Sci. Rep. 2019 9 8794 10.1038/s41598-019-45002-8
Fulthorpe R. Martin A. Isaac M. Root Endophytes of Coffee (Coffea arabica): Variation across Climatic Gradients and Relationships with Functional Traits Phytobiomes J. 2020 4 27 39 10.1094/PBIOMES-04-19-0021-R
Duong B. Marraccini P. Maeght J. Vaast P. Lebrun M. Duponnois R. Coffee Microbiota and Its Potential Use in Sustainable Crop Management. A Review Front. Sustain. Food Syst. 2020 4 607935 10.3389/fsufs.2020.607935
Lu L. Tibpromma S. Karunarathna S. Jayawardena R. Lumyong S. Xu J. Hyde K. Comprehensive Review of Fungi on Coffee Pathogens 2022 11 411 10.3390/pathogens11040411
Bosso L. Cristinzio G. Migliozzi A. Valentino D. Russo D. Plant pathogens but not antagonists change in soil fungal communities across a land abandonment gradient in a Mediterranean landscape Acta Oecol. 2017 78 1 6 10.1016/j.actao.2016.11.002
James T. Marino J. Perfecto I. Vandermeer J. Identification of Putative Coffee Rust Mycoparasites via Single–Molecule DNA Sequencing of Infected Pustules Appl. Environ. Microbiol. 2016 82 631 639 10.1128/AEM.02639-15
Irannia Z. Chen T. TACO: Taxonomic prediction of unknown OTUs through OTU co-abundance networks Quant. Biol. 2016 4 149 158 10.1007/s40484-016-0073-2
Tedersoo L. Drenkhan R. Anslan S. Morales-Rodriguez C. Cleary M. High-throughput identification and diagnostics of pathogens and pests: Overview and practical recommendations Mol. Ecol. Resour. 2018 19 47 76 10.1111/1755-0998.12959 30358140
Gómez-De La Cruz I. Pérez-Portilla E. Escamilla-Prado E. Martínez-Bolaños M. Carrión-Villarnovo G. Hernández-Leal T. Selección in vitro de micoparásitos con potencial de control biológico sobre Roya del café (Hemileia vastatrix) Rev. Mex. Fitopatol. Mex. J. Phytopathol. 2018 36 172 183 10.18781/R.MEX.FIT.1708-1
Guatimosim E. Schwartsburd P. Barreto R. Crous P. Novel fungi from an ancient niche: Cercosporoid and related sexual morphs on ferns Persoonia—Mol. Phylogeny Evol. Fungi 2016 37 106 141 10.3767/003158516X690934 28232762
Quispe-Apaza C. Mansilla-Samaniego R. López-Bonilla C. Espejo-Joya R. Villanueva-Caceda J. Monzón C. Diversidad genética de Hemileia vastatrix de dos Zonas productoras de café en el Perú Rev. Mex. Fitopatol. Mex. J. Phytopathol. 2017 35 418 436 10.18781/R.MEX.FIT.1612-7
Santana M. Zambolim E. Caixeta E. Zambolim L. Population genetic structure of the coffee pathogen Hemileia vastatrix in Minas Gerais, Brazil Trop. Plant Pathol. 2018 43 473 476 10.1007/s40858-018-0246-9
Pereira C.M. Sarmiento S.S. Colmán A.A. Belachew-Bekele K. Evans H.C. Barreto R.W. Mycodiversity in a micro-habitat: Twelve Cladosporium species, including four new taxa, isolated from uredinia of coffee leaf rust, Hemileia vastatrix Fungal Syst. Evol. 2024 14 9 33 10.3114/fuse.2024.14.02
Jackson D. Skillman J. Vandermeer J. Indirect biological control of the coffee leaf rust, Hemileia vastatrix, by the entomogenous fungus Lecanicillium lecanii in a complex coffee agroecosystem Biol. Control 2012 61 89 97 10.1016/j.biocontrol.2012.01.004
Velásquez O.R. Guía de Variedades de Café y Selección de Semilla Asociación Nacional del Café Anacafé, Guatemala 2019 Available online: https://www.anacafe.org/uploads/file/bb091944490b490482f329b0ea0ec6bd/Guia-variedades-y-seleccion-semilla.pdf (accessed on 27 September 2024)
Mihai R.A. Ortiz-Pillajo D.C. Iturralde-Proaño K.M. Vinueza-Pullotasig M.Y. Sisa-Tolagasí L.A. Villares-Ledesma M.L. Melo-Heras E.J. Cubi-Insuaste N.S. Catana R.D. Comprehensive Assessment of Coffee Varieties (Coffea arabica L.; Coffea canephora L.) from Coastal, Andean, and Amazonian Regions of Ecuador; A Holistic Evaluation of Metabolism, Antioxidant Capacity and Sensory Attributes Horticulturae 2024 10 200 10.3390/horticulturae10030200
Ochoa P.A. Fries A. Mejía D. Burneo J.I. Ruíz-Sinoga J.D. Cerdà A. Effects of Climate, Land Cover and Topography on Soil Erosion Risk in a Semiarid Basin of the Andes Catena 2016 140 31 42 10.1016/j.catena.2016.01.011
Apolo D. Fernández J.M. Benítez Á. Figueroa J.G. Estrada K. Cruz D. Phenotypic and Molecular Characterization of Yeast Diversity Associated to Postharvest Fermentation Process of Coffee Fruits in Southern Ecuador Diversity 2023 15 984 10.3390/d15090984
White T. Bruns T. Lee S. Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics PCR Protocols: A Guide to Methods and Applications Innis M. Gelfand D. Sninsky J. White T. Academic Press, Inc. New York, NY, USA 1990 315 322
Altschul S.F. Gish W. Miller W. Myers E.W. Lipman D.J. Basic local alignment search tool J. Mol. Biol. 1990 215 403 410 10.1016/S0022-2836(05)80360-2 2231712
Katoh K. Standley D. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Mol. Biol. Evol. 2013 30 772 780 10.1093/molbev/mst010 23329690
Göker M. Grimm G. Auch A. Aurahs R. Kučera M. A Clustering Optimization Strategy for Molecular Taxonomy Applied to Planktonic Foraminifera SSU rDNA Evol. Bioinform. 2010 6 EBO.S5504 10.4137/EBO.S5504 21037964
Cruz D. Suárez J. Kottke I. Piepenbring M. Cryptic species revealed by molecular phylogenetic analysis of sequences obtained from basidiomata of Tulasnella Mycologia 2014 106 708 722 10.3852/12-386
Herrera P. Kottke I. Molina M. Méndez M. Suárez J. Generalism in the interaction of Tulasnellaceae mycobionts with orchids characterizes a biodiversity hotspot in the tropical Andes of Southern Ecuador Mycoscience 2018 59 38 48 10.1016/j.myc.2017.08.003
Nei M. Kumar S. Molecular Evolution and Phylogenetics Oxford University Press Oxford, UK 2005
Kumar S. Stecher G. Li M. Knyaz C. Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms Mol. Biol. Evol. 2018 35 1547 1549 10.1093/molbev/msy096
Vrålstad T. ITS, OTUs and beyond-fungal hyperdiversity calls for supplementary solutions Mol. Ecol. 2011 20 2873 2875 10.1111/j.1365-294X.2011.05149.x
Schoch C. Seifert K. Huhndorf S. Robert V. Spouge J. Levesque C. Chen W. Bolchacova E. Voigt K. Crous P. et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi Proc. Natl. Acad. Sci. USA 2012 109 6241 6246 10.1073/pnas.1117018109 22454494
Nageen Y. Asemoloye M.D. Põlme S. Wang X. Xu S. Ramteke P.W. Pecoraro L. Analysis of culturable airborne fungi in outdoor environments in Tianjin, China BMC Microbiol. 2021 21 134 10.1186/s12866-021-02205-2
Frohlich-Nowoisky J. Pickersgill D.A. Despres V.R. Poschl U. High diversity of fungi in air particulate matter Proc. Natl. Acad. Sci. USA 2009 106 12814 12819 10.1073/pnas.0811003106
Barrowclough M. Stehouwer R. Alwang J. Gallagher R. Mosquera V. Dominguez J. Conservation agriculture on steep slopes in the Andes: Promise and obstacles J. Soil Water Conserv. 2016 71 91 102 10.2489/jswc.71.2.91
Tomao A. Antonio Bonet J. Castaño C. de-Miguel S. How does forest management affect fungal diversity and community composition? Current knowledge and future perspectives for the conservation of forest fungi For. Ecol. Manag. 2020 457 117678 10.1016/j.foreco.2019.117678
Kurtzman C. Mateo R. Kolecka A. Theelen B. Robert V. Boekhout T. Advances in yeast systematics and phylogeny and their use as predictors of biotechnologically important metabolic pathways FEMS Yeast Res. 2015 15 fov050 10.1093/femsyr/fov050
Monteiro M. Alves N. Queiroz M. Pinho D. Pereira O. Souza S. Cardoso P. Antimicrobial activity of endophytic fungi from coffee plants Biosci. J. 2017 33 381 389 10.14393/BJ-v33n2-34494
Silva H. Tozzi J. Terrasan C. Bettiol W. Endophytic microorganisms from coffee tissues as plant growth promoters and biocontrol agents of coffee leaf rust Biol. Control 2012 63 62 67 10.1016/j.biocontrol.2012.06.005
Salgado M. Lima C. Almeida A. Santos L. Pfenning L. First report of the occurence of Didymella sp., teleomorph of Phoma tarda, on Coffea arabica in Brazil Anais Simpósio de Pesquisa dos Cafés do Brasil, 5 Embrapa-Café Águas de Lindóia, Brasil Brasília, Brasil 2007 1 3
Vega F. Simpkins A. Aime M. Posada F. Peterson S. Rehner S. Infante F. Castillo A. Arnold A. Fungal endophyte diversity in coffee plants from Colombia, Hawai’i, Mexico and Puerto Rico Fungal Ecol. 2010 3 122 138 10.1016/j.funeco.2009.07.002
Cañarte C. Fuentes T. Manobanda M. Ayón N. Vera B. Prevalencia y diseminación de Verticillium sp. para el control biologico de la roya del café Rev. Cient. Investig. Actual. Mundo Cienc. 2018 2 92 119
Mosca S. Li Destri Nicosia M. Cacciola S. Schena L. Molecular Analysis of Colletotrichum Species in the Carposphere and Phyllosphere of Olive PLoS ONE 2014 9 e114031 10.1371/journal.pone.0114031 25501572
Silva M. Várzea V. Guerra-Guimarães L. Azinheira H. Fernandez D. Petitot A. Bertrand B. Lashermes P. Nicole M. Coffee resistance to the main diseases: Leaf rust and coffee berry disease Braz. J. Plant Physiol. 2006 18 119 147 10.1590/S1677-04202006000100010
Yasuda F. Izawa H. Yamagishi D. Akamatsu H. Kodama M. Otani H. Meira nashicola sp. nov., a novel basidiomycetous, anamorphic yeastlike fungus isolated from Japanese pear fruit with reddish stain Mycoscience 2006 47 36 40 10.1007/S10267-005-0266-4
Landell M. Brandão L. Barbosa A. Ramos J. Safar S. Gomes F. Sousa F. Morais P. Broetto L. Leoncini O. et al. Hannaella pagnoccae sp. nov., a tremellaceous yeast species isolated from plants and soil Int. J. Syst. Evol. Microbiol. 2014 64 1970 1977 10.1099/ijs.0.059345-0 24614844
Surussawadee J. Khunnamwong P. Srisuk N. Limtong S. Papiliotrema siamense f.a., sp. nov., a yeast species isolated from plant leaves Int. J. Syst. Evol. Microbiol. 2014 64 3058 3062 10.1099/ijs.0.065607-0 24925598
Choudhary P. Singh B. Chakdar H. Saxena A. DNA barcoding of phytopathogens for disease diagnostics and bio-surveillance World J. Microbiol. Biotechnol. 2021 37 54 10.1007/s11274-021-03019-0 33604719
Nishad R. Ahmed T. Rahman V. Kareem A. Modulation of Plant Defense System in Response to Microbial Interactions Front. Microbiol. 2020 11 1298 10.3389/fmicb.2020.01298
Poma-Angamarca R.A. Rojas J.R. Sánchez-Rodríguez A. Ruiz-González M.X. Diversity of Leaf Fungal Endophytes from Two Coffea arabica Varieties and Antagonism towards Coffee Leaf Rust Plants 2024 13 814 10.3390/plants13060814