{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,17]],"date-time":"2025-11-17T17:19:35Z","timestamp":1763399975261,"version":"build-2065373602"},"reference-count":52,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2021,1,25]],"date-time":"2021-01-25T00:00:00Z","timestamp":1611532800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["DL57\/2016\/CP[12345\/2018]\/CT[2475]","IF\/00819\/2015","PTDC\/BIA-BQM\/28539\/2017","UIDB\/04046\/2020 and UIDP\/04046\/2020"],"award-info":[{"award-number":["DL57\/2016\/CP[12345\/2018]\/CT[2475]","IF\/00819\/2015","PTDC\/BIA-BQM\/28539\/2017","UIDB\/04046\/2020 and UIDP\/04046\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Sustainability"],"abstract":"<jats:p>Grapevine (Vitis vinifera L.), widely used for berry and wine production, is highly susceptible to the pathogenic oomycete Plasmopara viticola, the etiological agent of grapevine downy mildew disease. The method commonly used to prevent and control P. viticola infection relies on multiple applications of chemical fungicides. However, with European Union goals to lower the usage of such chemicals in viticulture there is a need to develop new and more sustainable strategies. The use of beneficial microorganisms with biocontrol capabilities, such as the arbuscular mycorrhizal fungi (AMF), has been pointed out as a viable alternative. With this study, we intended to investigate the effect of AMF colonization on the expression of P. viticola effectors during infection of grapevine. Grapevine plants were inoculated with the AMF Rhizophagus irregularis and, after mycorrhizae development, plants were infected with P. viticola. The expression of P. viticola RxLR effectors was analyzed by real-time PCR (qPCR) during the first hours of interaction. Results show that pre-mycorrhizal inoculation of grapevine alters the expression of several P. viticola effectors; namely, PvRxLR28, which presented decreased expression in mycorrhizal plants at the two time points post-infection tested. These results suggest that the pre-inoculation of grapevine with AMF could interfere with the pathogen\u2019s ability to infect grapevine by modulation of pathogenicity effectors expression, supporting the hypothesis that AMF can be used to increase plant resistance to pathogens and promote more sustainable agriculture practices, particularly in viticulture.<\/jats:p>","DOI":"10.3390\/su13031226","type":"journal-article","created":{"date-parts":[[2021,1,25]],"date-time":"2021-01-25T12:28:31Z","timestamp":1611577711000},"page":"1226","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":29,"title":["First Insights into the Effect of Mycorrhizae on the Expression of Pathogen Effectors during the Infection of Grapevine with Plasmopara viticola"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0749-0877","authenticated-orcid":false,"given":"Ana","family":"Cruz-Silva","sequence":"first","affiliation":[{"name":"BioISI\u2014Instituto de Biossistemas e Ci\u00eancias Integrativas, Faculdade de Ci\u00eancias, Universidade de Lisboa, 1749-016 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8156-7700","authenticated-orcid":false,"given":"Andreia","family":"Figueiredo","sequence":"additional","affiliation":[{"name":"BioISI\u2014Instituto de Biossistemas e Ci\u00eancias Integrativas, Faculdade de Ci\u00eancias, Universidade de Lisboa, 1749-016 Lisboa, Portugal"}]},{"given":"M\u00f3nica","family":"Sebastiana","sequence":"additional","affiliation":[{"name":"BioISI\u2014Instituto de Biossistemas e Ci\u00eancias Integrativas, Faculdade de Ci\u00eancias, Universidade de Lisboa, 1749-016 Lisboa, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"880","DOI":"10.1002\/bies.20457","article-title":"PAMP recognition and the plant\u2013pathogen arms race","volume":"28","author":"Ingle","year":"2006","journal-title":"Bioessays"},{"key":"ref_2","first-page":"323","article-title":"The plant immune system","volume":"444","author":"Jones","year":"2006","journal-title":"Nat. Cell Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1111\/j.1364-3703.2009.00547.x","article-title":"The zig-zag-zig in oomycete-plant interactions","volume":"10","author":"Hein","year":"2009","journal-title":"Mol. Plant Pathol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1016\/j.pbi.2011.03.005","article-title":"How filamentous pathogens co-opt plants: The ins and outs of fungal effectors","volume":"14","author":"Bolton","year":"2011","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1111\/j.1364-3703.2009.00593.x","article-title":"Ten things to know about oomycete effectors","volume":"10","author":"Schornack","year":"2009","journal-title":"Mol. Plant Pathol."},{"key":"ref_6","first-page":"3","article-title":"Plasmopara viticola: A review of knowledge on downy mildew of grapevine and effective disease management","volume":"50","author":"Gessler","year":"2011","journal-title":"Phytopathol. Mediterr."},{"key":"ref_7","first-page":"382","article-title":"Grapevine pathogenic microorganisms: Understanding infection strategies and host response scenarios","volume":"7","author":"Earmijo","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.plaphy.2019.01.026","article-title":"Early stage metabolic events associated with the establishment of Vitis vinifera\u2013Plasmopara viticola compatible interaction","volume":"137","author":"Nascimento","year":"2019","journal-title":"Plant Physiol. Biochem."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1016\/j.funbio.2012.04.016","article-title":"Identification of effector genes from the phytopathogenic Oomycete Plasmopara viticola through the analysis of gene expression in germinated zoospores","volume":"116","author":"Mestre","year":"2012","journal-title":"Fungal Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pmpp.2015.05.002","article-title":"Characterization of the secretome of Plasmopara viticola by de novo transcriptome analysis","volume":"91","author":"Yin","year":"2015","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1111\/ppa.12469","article-title":"Comparative analysis of expressed CRN and RXLR effectors from two Plasmopara species causing grapevine and sunflower downy mildew","volume":"65","author":"Mestre","year":"2016","journal-title":"Plant Pathol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"46553","DOI":"10.1038\/srep46553","article-title":"Genome sequence of Plasmopara viticola and insight into the pathogenic mechanism","volume":"7","author":"Yin","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1038\/s41598-018-19158-8","article-title":"A multi-omics study of the grapevine-downy mildew (Plasmopara viticola) pathosystem unveils a complex protein coding- and noncoding-based arms race during infection","volume":"8","author":"Brilli","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"954","DOI":"10.1093\/gbe\/evz048","article-title":"A high-quality grapevine downy mildew genome assembly reveals rapidly evolving and lineage-specific putative host adaptation genes","volume":"11","author":"Dussert","year":"2019","journal-title":"Genome Biol. Evol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"692","DOI":"10.3389\/fmicb.2020.00692","article-title":"Insight into function and subcellular localization of Plasmopara viticola putative RXLR effectors","volume":"11","author":"Chen","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_16","first-page":"115","article-title":"A translocation signal for delivery of oomycete effector proteins into host plant cells","volume":"450","author":"Whisson","year":"2007","journal-title":"Nat. Cell Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1111\/j.1365-313X.2012.05079.x","article-title":"Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojaesuppress immunity in distantly related plants","volume":"72","author":"Anderson","year":"2012","journal-title":"Plant J."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"709","DOI":"10.3389\/fmicb.2016.00709","article-title":"Studying the mechanism of Plasmopara viticola RXLR effectors on suppressing plant immunity","volume":"7","author":"Xiang","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"286","DOI":"10.3389\/fpls.2018.00286","article-title":"In planta functional analysis and subcellular localization of the oomycete pathogen Plasmopara viticola candidate RXLR effector repertoire","volume":"9","author":"Liu","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1111\/mpp.12790","article-title":"Plasmopara viticola effector PvRXLR131 suppresses plant immunity by targeting plant receptor-like kinase inhibitor BKI1","volume":"20","author":"Lan","year":"2019","journal-title":"Mol. Plant Pathol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1682220","DOI":"10.1080\/15592324.2019.1682220","article-title":"Plasmopara viticola effector PvRXLR159 suppresses immune responses in Nicotiana benthamiana","volume":"14","author":"Lei","year":"2019","journal-title":"Plant Signal. Behav."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Azc\u00f3n-Aguilar, C., Barea, J.M., Gianinazzi, S., and Gianinazzi-Pearson, V. (2009). Priming plant defence against pathogens by arbuscular mycorrhizal fungi. Mycorrhizas-Functional Processes and Ecological Impact, Springer.","DOI":"10.1007\/978-3-540-87978-7"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Varma, A., Prasad, R., and Tuteja, N. (2017). Arbuscular mycorrhiza mediated control of plant pathogens. Mycorrhiza-Nutrient Uptake, Biocontrol, Ecorestoration, Springer International Publishing.","DOI":"10.1007\/978-3-319-68867-1"},{"key":"ref_24","first-page":"579","article-title":"The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection","volume":"13","author":"Segundo","year":"2011","journal-title":"Mol. Plant Pathol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"786","DOI":"10.3389\/fpls.2015.00786","article-title":"Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus","volume":"6","author":"Song","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.phytochem.2016.09.002","article-title":"Arbuscular mycorrhizal symbiosis stimulates key genes of the phenylpropanoid biosynthesis and stilbenoid production in grapevine leaves in response to downy mildew and grey mould infection","volume":"131","author":"Bruisson","year":"2016","journal-title":"Phytochemistry"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1111\/jph.12662","article-title":"Arbuscular mycorrhiza-mediated resistance in tomato against Cladosporium fulvum-induced mould disease","volume":"166","author":"Wang","year":"2018","journal-title":"J. Phytopathol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-018-27622-8","article-title":"Omics approaches revealed how arbuscular mycorrhizal symbiosis enhances yield and resistance to leaf pathogen in wheat","volume":"8","author":"Fiorilli","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.pmpp.2011.06.005","article-title":"Mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans","volume":"76","author":"Gallou","year":"2011","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2769","DOI":"10.1093\/jxb\/eraa030","article-title":"Role and mechanisms of callose priming in mycorrhiza-induced resistance","volume":"71","author":"Pastor","year":"2020","journal-title":"J. Exp. Bot."},{"key":"ref_31","unstructured":"Reynier, A. (2002). Manual de Viticultura, Mundi Prensa. [6th ed.]."},{"key":"ref_32","first-page":"312","article-title":"Nematode and grape rootstock interactions including an improved understanding of tolerance","volume":"38","author":"McKenry","year":"2006","journal-title":"J. Nematol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1007\/s10142-012-0261-8","article-title":"Cultivar-specific kinetics of gene induction during downy mildew early infection in grapevine","volume":"12","author":"Figueiredo","year":"2012","journal-title":"Funct. Integr. Genom."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1007\/s11032-008-9186-2","article-title":"Identification, isolation and characterization of a CC-NBS-LRR candidate disease resistance gene family in grapevine","volume":"22","author":"Kortekamp","year":"2008","journal-title":"Mol. Breed."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"R19","DOI":"10.1186\/gb-2007-8-2-r19","article-title":"qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data","volume":"8","author":"Hellemans","year":"2007","journal-title":"Genome Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3657","DOI":"10.1093\/jxb\/ers046","article-title":"Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine","volume":"63","author":"Hao","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1007\/s00572-010-0352-0","article-title":"Arbuscular mycorrhizal symbiosis elicits proteome responses opposite of P-starvation in SO4 grapevine rootstock upon root colonisation with two Glomus species","volume":"21","author":"Johnson","year":"2011","journal-title":"Mycorrhiza"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-020-66067-w","article-title":"AMF communities associated to Vitis vinifera in an Italian vineyard subjected to integrated pest management at two different phenological stages","volume":"10","author":"Massa","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Nogales, A., Santos, E.S., Abreu, M.M., Ar\u00e1n, D., Victorino, G., Pereira, H.S., Lopes, C.M., and Viegas, W. (2019). Mycorrhizal inoculation differentially affects grapevine\u2019s performance in copper contaminated and non-contaminated soils. Front. Plant Sci., 9.","DOI":"10.3389\/fpls.2018.01906"},{"key":"ref_40","unstructured":"Smith, S.E., and Read, D. (2008). Preface. Mycorrhizal Symbiosis, Academic Press."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1007\/s00572-020-00933-3","article-title":"Responses of Vitis vinifera cv. Cabernet Sauvignon roots to the arbuscular mycorrhizal fungus Funneliformis mosseae and the plant growth-promoting rhizobacterium Ensifer meliloti include changes in volatile organic compounds","volume":"30","author":"Fiaschi","year":"2020","journal-title":"Mycorrhiza"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"8","DOI":"10.5344\/ajev.2001.52.1.8","article-title":"Comparative response of selected grapevine rootstocks and cultivars to inoculation with different mycorrhizal fungi","volume":"52","author":"Linderman","year":"2001","journal-title":"Am. J. Enol. Vitic."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1017\/S001447970300125X","article-title":"Effects of drought stress on mycorrhizal and non-mycorrhizal cabernet sauvignon grapevine, grafted onto various rootstocks","volume":"39","author":"Nikolaou","year":"2003","journal-title":"Exp. Agric."},{"key":"ref_44","first-page":"8","article-title":"Effect of inoculation with mycorrhizal fungi on growth and nutrient uptake of grapevine genotypes (Vitis Spp.)","volume":"75","author":"Ozdemir","year":"2010","journal-title":"Europ. J. Hort. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1125","DOI":"10.1016\/j.funbio.2018.07.006","article-title":"Up-regulated RxLR effector genes of Plasmopara viticola in synchronized host-free stages and infected leaves of hosts with different susceptibility","volume":"122","author":"Spring","year":"2018","journal-title":"Fungal Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12864-016-3192-2","article-title":"Transcriptome analysis of the fungal pathogen Fusarium oxysporum f. sp. medicaginis during colonisation of resistant and susceptible Medicago truncatula hosts identifies differential pathogenicity profiles and novel candidate effectors","volume":"17","author":"Thatcher","year":"2016","journal-title":"BMC Genom."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1094\/PHYTO-06-18-0204-R","article-title":"Simultaneous transcriptome analysis of host and pathogen highlights the interaction between Brassica oleracea and Sclerotinia sclerotiorum","volume":"109","author":"Ding","year":"2019","journal-title":"Phytopathology"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-020-63668-3","article-title":"Transcriptional analyses of differential cultivars during resistant and susceptible interactions with Peronospora effusa, the causal agent of spinach downy mildew","volume":"10","author":"Kandel","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"16153","DOI":"10.1038\/nplants.2016.153","article-title":"Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen","volume":"2","author":"Zhang","year":"2016","journal-title":"Nat. Plants"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Zhang, Q., Gao, X., Ren, Y., Ding, X., Qiu, J., Li, N., Zeng, F., and Chu, Z. (2018). Improvement of verticillium wilt resistance by applying arbuscular mycorrhizal fungi to a cotton variety with high symbiotic efficiency under field conditions. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19010241"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"110595","DOI":"10.1016\/j.plantsci.2020.110595","article-title":"Root-to-shoot signalling in mycorrhizal tomato plants upon Botrytis cinerea infection","volume":"298","author":"Pastor","year":"2020","journal-title":"Plant Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1094\/MPMI.1998.11.10.1017","article-title":"Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus","volume":"11","author":"Cordier","year":"1998","journal-title":"Mol. Plant-Microbe Interact."}],"container-title":["Sustainability"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2071-1050\/13\/3\/1226\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:14:58Z","timestamp":1760159698000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2071-1050\/13\/3\/1226"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,25]]},"references-count":52,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["su13031226"],"URL":"https:\/\/doi.org\/10.3390\/su13031226","relation":{},"ISSN":["2071-1050"],"issn-type":[{"type":"electronic","value":"2071-1050"}],"subject":[],"published":{"date-parts":[[2021,1,25]]}}}