{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,8]],"date-time":"2026-01-08T07:18:45Z","timestamp":1767856725103,"version":"3.49.0"},"reference-count":52,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2022,2,5]],"date-time":"2022-02-05T00:00:00Z","timestamp":1644019200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"FEDER funds through COMPETE (Programa Operacional Factores de Competitividade) and by national funds by FCT (Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia)","award":["PTDC\/ASP-PLA\/31133\/2017"],"award-info":[{"award-number":["PTDC\/ASP-PLA\/31133\/2017"]}]},{"name":"FEDER funds through COMPETE (Programa Operacional Factores de Competitividade) and by national funds by FCT (Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","award":["BioISI (UIDB\/04046\/2020)"],"award-info":[{"award-number":["BioISI (UIDB\/04046\/2020)"]}]},{"name":"FEDER funds through COMPETE (Programa Operacional Factores de Competitividade) and by national funds by FCT (Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","award":["Mountain Research Center - CIMO (UIDB\/00690\/2020)"],"award-info":[{"award-number":["Mountain Research Center - CIMO (UIDB\/00690\/2020)"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>The phyllosphere comprises the aerial parts of plants and is colonized by a great diversity of microorganisms, either growing inside (as endophytes) or on the surface (as epiphytes) of plant tissues. The factors that structure the diversity of epiphytes and the importance of these microorganisms for host plant protection have been less studied when compared to the case of endophytes. In this work, the epiphytic fungal communities from fruits of the olive tree (olives) in different maturation stages (green and semi-ripened), obtained from different olive orchard managements (integrated and organic production) and from distinct cultivars displaying different susceptibilities to olive anthracnose (Cobran\u00e7osa and Madural), are compared by using a metabarcoding approach. We discuss whether such differences in host resistance against anthracnose depend on both the fungal taxa or fungal community composition. A total of 1565 amplicon sequence variants (ASVs) were obtained, mainly belonging to the Ascomycota phylum and Saccharomycetes class. Although significant differences on epiphytic fungal richness were observed among olives obtained in different production systems and maturation stages, these factors in addition to host cultivar did not influence the composition of the epiphytes. Despite these results, a co-inertia analysis showed that Aureobasidium spp. and Sporocadaceae spp. were positively associated with the green olives of the cv. Madural produced under integrated production, while Saccharomycetales spp. (Kluyveromyces, Candida, Kazachstania and Saccharomyces) were positively associated with the semi-ripened olives of the cv. Cobran\u00e7osa obtained from organic production. The discriminant power of these fungi, some of them recognized as biocontrol agents, suggest that they might be important in conferring differences on host plant susceptibility to anthracnose.<\/jats:p>","DOI":"10.3390\/microorganisms10020376","type":"journal-article","created":{"date-parts":[[2022,2,6]],"date-time":"2022-02-06T20:38:40Z","timestamp":1644179920000},"page":"376","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Olive Fungal Epiphytic Communities Are Affected by Their Maturation Stage"],"prefix":"10.3390","volume":"10","author":[{"given":"Joana","family":"Castro","sequence":"first","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus of Gualtar, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8398-3580","authenticated-orcid":false,"given":"Daniela","family":"Costa","sequence":"additional","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus of Gualtar, 4710-057 Braga, Portugal"}]},{"given":"Rui M.","family":"Tavares","sequence":"additional","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus of Gualtar, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6331-3731","authenticated-orcid":false,"given":"Paula","family":"Baptista","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1385-4799","authenticated-orcid":false,"given":"Teresa","family":"Lino-Neto","sequence":"additional","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus of Gualtar, 4710-057 Braga, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2022,2,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1830","DOI":"10.3389\/fpls.2017.01830","article-title":"Olive cultivation in the southern hemisphere: Flowering, water requirements and oil quality responses to new crop environments","volume":"8","author":"Torres","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2514","DOI":"10.1016\/j.scitotenv.2018.10.175","article-title":"Energy and environmental performances of hybrid photovoltaic irrigation systems in Mediterranean intensive and super-intensive olive orchards","volume":"651","author":"Todde","year":"2019","journal-title":"Sci. Total Environ."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.scienta.2017.01.012","article-title":"Orchard management, soil organic carbon and ecosystem services in Mediterranean fruit tree crops","volume":"217","author":"Montanaro","year":"2017","journal-title":"Sci. Hortic."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Niu, J., Rang, Z., Zhang, C., Chen, W., Tian, F., Yin, H., and Dai, L. (2016). The succession pattern of soil microbial communities and its relationship with tobacco bacterial wilt. BMC Microbiol., 16.","DOI":"10.1186\/s12866-016-0845-x"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1093\/femsec\/fix050","article-title":"Plant microbial diversity is suggested as the key to future biocontrol and health trends","volume":"93","author":"Berg","year":"2017","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1094\/PBIOMES-01-19-0008-R","article-title":"Disease incidence in sugar beet fields is correlated with microbial diversity and distinct biological markers","volume":"3","author":"Kusstatscher","year":"2019","journal-title":"Phytobiomes J."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Gouvinhas, I., Martins-Lopes, P., Carvalho, T., Barros, A., and Gomes, S. (2019). Impact of Colletotrichum acutatum pathogen on olive phenylpropanoid metabolism. Agriculture, 9.","DOI":"10.3390\/agriculture9080173"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1038\/nrmicro2910","article-title":"Microbial life in the phyllosphere","volume":"10","author":"Vorholt","year":"2012","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"104168","DOI":"10.1016\/j.biocontrol.2019.104168","article-title":"The endophytic strain Bacillus velezensis OEE1: An efficient biocontrol agent against Verticillium wilt of olive and a potential plant growth promoting bacteria","volume":"142","author":"Azabou","year":"2020","journal-title":"Biol. Control"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Mannaa, M., and Seo, Y.S. (2021). Plants under the attack of allies: Moving towards the plant pathobiome paradigm. Plants, 10.","DOI":"10.3390\/plants10010125"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Lacava, P.T., and Azevedo, J.L. (2014). Biological Control of Insect-Pest and Diseases by Endophytes. Advances in Endophytic Research, Springer.","DOI":"10.1007\/978-81-322-1575-2_13"},{"key":"ref_12","first-page":"81","article-title":"Evidence of early flower infection in olives (Olea europaea) by Colletotrichum acutatum and C. gloeosporioides causing anthracnose disease","volume":"3","author":"Sergeeva","year":"2008","journal-title":"Australas. Plant Dis. Notes"},{"key":"ref_13","first-page":"531","article-title":"Caracterizaci\u00f3n morfol\u00f3gica y cultural de aislados de Colletotrichum spp. causantes de la Antracnosis del olivo","volume":"31","author":"Oliveira","year":"2005","journal-title":"Bolet\u00edn Sanid. Veg. Plagas"},{"key":"ref_14","first-page":"29","article-title":"Olive anthracnose","volume":"94","author":"Cacciola","year":"2012","journal-title":"J. Plant Pathol."},{"key":"ref_15","unstructured":"Malavolta, C., and Perdikis, D. (2021, October 11). Crop Specific Technical Guidelines for Integrated Production of Olives. IOBC-WPRS Commission IP Guidelines, Available online: https:\/\/www.iobc-wprs.org\/ip_practical_guidelines\/index.html."},{"key":"ref_16","unstructured":"Barranco, D., Fern\u00e1ndez-Escobar, R., and Rallo, L. (2008). Maduraci\u00f3n. El Cultivo del Olivo, Ediciones Mundi-Prensa y Junta de Andaluc\u00eda. [6th ed.]."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/s13595-018-0705-y","article-title":"Rapid and economical protocols for genomic and metagenomic DNA extraction from oak (Quercus brantii Lindl.)","volume":"75","author":"Ahmadi","year":"2018","journal-title":"Ann. For. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.mycol.2005.11.004","article-title":"Sequences, the environment and fungi","volume":"20","author":"Mitchell","year":"2006","journal-title":"Mycologist"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1256688","DOI":"10.1126\/science.1256688","article-title":"Global diversity and geography of soil fungi","volume":"346","author":"Tedersoo","year":"2014","journal-title":"Science"},{"key":"ref_20","unstructured":"Andrews, S. (2021, October 11). FastQC\u2014A Quality Control Tool for High Throughput Sequence Data [Internet]. Available online: https:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"ref_21","unstructured":"Joshi, N.A., and Fass, J.N. (2021, October 11). Sickle: A Sliding-Window, Adaptive, Quality-Based Trimming Tool for FastQ Files [Internet]. Available online: https:\/\/github.com\/najoshi\/sickle."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Nurk, S., Bankevich, A., Antipov, D., Gurevich, A., Korobeynikov, A., Lapidus, A., Prjibelsky, A., Pyshkin, A., Sirotkin, A., and Sirotkin, Y. (2013). Assembling genomes and mini-metagenomes from highly chimeric reads. Lecture Notes in Computer Science (including Subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics), Springer.","DOI":"10.1007\/978-3-642-37195-0_13"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2460","DOI":"10.1093\/bioinformatics\/btq461","article-title":"Search and clustering orders of magnitude faster than BLAST","volume":"26","author":"Edgar","year":"2010","journal-title":"Bioinformatics"},{"key":"ref_24","unstructured":"Aronesty, E. (2021, October 11). ea-utils: Command-Line Tools for Processing Biological Sequencing Data. Available online: https:\/\/expressionanalysis.github.io\/ea-utils\/."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"9743","DOI":"10.1038\/srep09743","article-title":"MICCA: A complete and accurate software for taxonomic profiling of metagenomic data","volume":"5","author":"Albanese","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"D259","DOI":"10.1093\/nar\/gky1022","article-title":"The UNITE database for molecular identification of fungi: Handling dark taxa and parallel taxonomic classifications","volume":"47","author":"Nilsson","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/nmeth.f.303","article-title":"QIIME allows analysis of high-throughput community sequencing data","volume":"7","author":"Caporaso","year":"2010","journal-title":"Nat. Methods"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Kowalchuk, G.A., de Bruijn, F.J., Head, I.M., Akkermans, A.D., and van Elsas, J.D. (2004). Application of ecological diversity statistics in microbial ecology. Molecular Microbial Ecology Manual, Kluwer Academic Publishers. [2nd ed.].","DOI":"10.1007\/978-1-4020-2177-0"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1574-6941.2003.tb01040.x","article-title":"Using ecological diversity measures with bacterial communities","volume":"43","author":"Hill","year":"2003","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_30","first-page":"178","article-title":"Past: Paleontological statistics software package for education and data analysis","volume":"4","author":"Hammer","year":"2001","journal-title":"Palaeontol. Electron."},{"key":"ref_31","unstructured":"Henderson, P.A., and Seaby, R.M.H. (2014). Community Analysis Package, Pisces Conservation Ltd."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2783","DOI":"10.1890\/07-0539.1","article-title":"Random forests for classification in ecology","volume":"88","author":"Cutler","year":"2007","journal-title":"Ecology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1023\/A:1010933404324","article-title":"Random forests","volume":"45","author":"Breiman","year":"2001","journal-title":"Mach. Learn."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1111\/j.1365-2427.1994.tb01741.x","article-title":"Co-inertia analysis: An alternative method for studying species\u2013environment relationships","volume":"31","author":"Chessel","year":"1994","journal-title":"Freshw. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v022.i04","article-title":"The ade4 package: Implementing the duality diagram for ecologists","volume":"22","author":"Dray","year":"2007","journal-title":"J. Stat. Softw."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Abdelfattah, A., Li Destri Nicosia, M.G., Cacciola, S.O., Droby, S., and Schena, L. (2015). Metabarcoding analysis of fungal diversity in the phyllosphere and carposphere of olive (Olea europaea). PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0131069"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"20423","DOI":"10.1038\/s41598-019-56977-9","article-title":"Defining the root endosphere and rhizosphere microbiomes from the World Olive Germplasm Collection","volume":"9","author":"Villadas","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"126693","DOI":"10.1016\/j.micres.2020.126693","article-title":"Illuminating Olea europaea L. endophyte fungal community","volume":"245","author":"Costa","year":"2021","journal-title":"Microbiol. Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1007\/s00248-008-9391-x","article-title":"Culturable fungi of stored \u201cgolden delicious\u201d apple fruits: A one-season comparison study of organic and integrated production systems in Switzerland","volume":"56","author":"Granado","year":"2008","journal-title":"Microb. Ecol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.ijfoodmicro.2014.02.002","article-title":"Influence of the farming system on the epiphytic yeasts and yeast-like fungi colonizing grape berries during the ripening process","volume":"177","author":"Martins","year":"2014","journal-title":"Int. J. Food Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1007\/s00248-018-1161-9","article-title":"Endophytic and epiphytic phyllosphere fungal communities are shaped by different environmental factors in a mediterranean ecosystem","volume":"76","author":"Gomes","year":"2018","journal-title":"Microb. Ecol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.biocontrol.2017.03.011","article-title":"Fungal community in olive fruits of cultivars with different susceptibilities to anthracnose and selection of isolates to be used as biocontrol agents","volume":"110","author":"Preto","year":"2017","journal-title":"Biol. Control"},{"key":"ref_43","first-page":"3531","article-title":"Terroir is the main driver of the epiphytic bacterial and fungal communities of mango carposphere in Reunion Island","volume":"11","author":"Rivallan","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1094\/MPMI-10-14-0331-FI","article-title":"Seasonal community succession of the phyllosphere microbiome","volume":"28","author":"Copeland","year":"2015","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"101003","DOI":"10.1016\/j.funeco.2020.101003","article-title":"Endophytic fungal community succession in reproductive organs of two olive tree cultivars with contrasting anthracnose susceptibilities","volume":"49","author":"Martins","year":"2021","journal-title":"Fungal Ecol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/j.funbio.2018.11.014","article-title":"Diversity of epiphytic fungi on the surface of Kyoho grape berries during ripening process in summer and winter at Nanning region, Guangxi, China","volume":"123","author":"Ding","year":"2019","journal-title":"Fungal Biol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Bill, M., Chidamba, L., Gokul, J.K., and Korsten, L. (2021). Mango endophyte and epiphyte microbiome composition during fruit development and post-harvest stages. Horticulturae, 7.","DOI":"10.3390\/horticulturae7110495"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1007\/s11274-019-2728-4","article-title":"Biocontrol yeasts: Mechanisms and applications","volume":"35","author":"Freimoser","year":"2019","journal-title":"World J. Microbiol. Biotechnol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1016\/j.simyco.2018.11.001","article-title":"Sporocadaceae, a family of coelomycetous fungi with appendage-bearing conidia","volume":"92","author":"Liu","year":"2019","journal-title":"Stud. Mycol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Galli, V., Romboli, Y., Barbato, D., Mari, E., Venturi, M., Guerrini, S., and Granchi, L. (2021). Indigenous Aureobasidium pullulans strains as biocontrol agents of Botrytis cinerea on grape berries. Sustainability, 13.","DOI":"10.3390\/su13169389"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Nigro, F., Antelmi, I., Labarile, R., Sion, V., and Pentimone, I. (2018). Biological control of olive anthracnose. Acta Horticulturae, International Society for Horticultural Science.","DOI":"10.17660\/ActaHortic.2018.1199.70"},{"key":"ref_52","first-page":"782","article-title":"Plant biostimulants: New insights into the biological control of Verticillium wilt of olive","volume":"12","author":"Trapero","year":"2021","journal-title":"Front. Plant Sci."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/2\/376\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:14:48Z","timestamp":1760134488000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/2\/376"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,5]]},"references-count":52,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2022,2]]}},"alternative-id":["microorganisms10020376"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms10020376","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,5]]}}}