title: Human Management of a Wild Plant Modulates the Evolutionary Dynamics of a Gene Determining Recessive Resistance to Virus Infection.
abstract: This work analyses the genetic variation and evolutionary patterns of recessive resistance loci involved in matching-allele (MA) host-pathogen interactions, focusing on the pvr2 resistance gene to potyviruses of the wild pepper Capsicum annuum glabriusculum (chiltepin). Chiltepin grows in a variety of wild habitats in Mexico, and its cultivation in home gardens started about 25 years ago. Potyvirus infection of Capsicum plants requires the physical interaction of the viral VPg with the pvr2 product, the translation initiation factor eIF4E1. Mutations impairing this interaction result in resistance, according to the MA model. The diversity of pvr2/eIF4E1 in wild and cultivated chiltepin populations from six biogeographical provinces in Mexico was analysed in 109 full-length coding sequences from 97 plants. Eleven alleles were found, and their interaction with potyvirus VPg in yeast-two-hybrid assays, plus infection assays of plants, identified six resistance alleles. Mapping resistance mutations on a pvr2/eIF4E1 model structure showed that most were around the cap-binding pocket and strongly altered its surface electrostatic potential, suggesting resistance-associated costs due to functional constraints. The pvr2/eIF4E1 phylogeny established that susceptibility was ancestral and resistance was derived. The spatial structure of pvr2/eIF4E1 diversity differed from that of neutral markers, but no evidence of selection for resistance was found in wild populations. In contrast, the resistance alleles were much more frequent, and positive selection stronger, in cultivated chiltepin populations, where diversification of pvr2/eIF4E1 was higher. This analysis of the genetic variation of a recessive resistance gene involved in MA host-pathogen interactions in populations of a wild plant show that evolutionary patterns differ according to the plant habitat, wild or cultivated. It also demonstrates that human management of the plant population has profound effects on the diversity and the evolution of the resistance gene, resulting in the selection of resistance alleles.
authors.affiliation: Centro de Biotecnología y Genómica de Plantas (UPM-INIA), and E.T.S.I. Agrónomos, Campus de Montegancedo, Universidad Politécnica de Madrid, Pozuelo de Alarcón, Madrid, Spain.
authors.forename: Nils
authors.initials: N
authors.lastname: Poulicard
authors.affiliation: Centro de Biotecnología y Genómica de Plantas (UPM-INIA), Campus de Montegancedo, Pozuelo de Alarcón (Madrid) and Departamento de Sistemas y Recursos Naturales, E.T.S.I. Montes, Universidad Politécnica de Madrid (UPM), Madrid, Spain.
authors.forename: Luis Fernández
authors.initials: LF
authors.lastname: Pacios
authors.affiliation: Institut National de Recherche Agronomique (INRA), UR1052, Génétique et Amélioration des Fruits et Légumes, Centre de Recherche PACA, Domaine Saint Maurice, CS60094, 84143, Montfavet, France.
authors.forename: Jean-Luc
authors.initials: JL
authors.lastname: Gallois
authors.affiliation: Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, México, D.F., México.
authors.forename: Daniel
authors.initials: D
authors.lastname: Piñero
authors.affiliation: Centro de Biotecnología y Genómica de Plantas (UPM-INIA), and E.T.S.I. Agrónomos, Campus de Montegancedo, Universidad Politécnica de Madrid, Pozuelo de Alarcón, Madrid, Spain.
authors.forename: Fernando
authors.initials: F
authors.lastname: García-Arenal
mesh_terms: D000483:Alleles; D002212:Capsicum / Q000235:genetics* / Q000821:virology; D060467:Disease Resistance / Q000235:genetics*; D039561:Eukaryotic Initiation Factor-4E / Q000235:genetics*; D054884:Host-Pathogen Interactions / Q000235:genetics*; D006801:Humans; D009154:Mutation; D010935:Plant Diseases / Q000235:genetics / Q000821:virology; D010940:Plant Proteins / Q000235:genetics*; D017800:Potyvirus / Q000235:genetics / Q000472:pathogenicity
chemical_list: D039561:Eukaryotic Initiation Factor-4E; D010940:Plant Proteins