title: Cytonuclear interactions affect adaptive traits of the annual plant Arabidopsis thaliana in the field.
abstract: Although the contribution of cytonuclear interactions to plant fitness variation is relatively well documented at the interspecific level, the prevalence of cytonuclear interactions at the intraspecific level remains poorly investigated. In this study, we set up a field experiment to explore the range of effects that cytonuclear interactions have on fitness-related traits in Arabidopsis thaliana To do so, we created a unique series of 56 cytolines resulting from cytoplasmic substitutions among eight natural accessions reflecting within-species genetic diversity. An assessment of these cytolines and their parental lines scored for 28 adaptive whole-organism phenotypes showed that a large proportion of phenotypic traits (23 of 28) were affected by cytonuclear interactions. The effects of these interactions varied from slight but frequent across cytolines to strong in some specific parental pairs. Two parental pairs accounted for half of the significant pairwise interactions. In one parental pair, Ct-1/Sha, we observed symmetrical phenotypic responses between the two nuclear backgrounds when combined with specific cytoplasms, suggesting nuclear differentiation at loci involved in cytonuclear epistasis. In contrast, asymmetrical phenotypic responses were observed in another parental pair, Cvi-0/Sha. In the Cvi-0 nuclear background, fecundity and phenology-related traits were strongly affected by the Sha cytoplasm, leading to a modified reproductive strategy without penalizing total seed production. These results indicate that natural variation in cytoplasmic and nuclear genomes interact to shape integrative traits that contribute to adaptation, thereby suggesting that cytonuclear interactions can play a major role in the evolutionary dynamics ofA. thaliana.
authors.affiliation: Laboratoire Evolution, Ecologie et Paléontologie, UMR CNRS 8198, Université de Lille, F-59655 Villeneuve d'Ascq Cedex, France; Institut National de la Recherche Agronomique (INRA), Laboratoire des Interactions Plantes-Microorganismes, UMR441, F-31326 Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, F-31326 Castanet-Tolosan, France;
authors.forename: Fabrice
authors.initials: F
authors.lastname: Roux
authors.affiliation: Génétique Quantitative et Evolution-Le Moulon, INRA, Université Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91190 Gif-sur-Yvette, France; Mathematiques et Informatique Appliquées, AgroParisTech, INRA, Université Paris-Saclay, 75005 Paris, France;
authors.forename: Tristan
authors.initials: T
authors.lastname: Mary-Huard
authors.affiliation: Laboratoire Evolution, Ecologie et Paléontologie, UMR CNRS 8198, Université de Lille, F-59655 Villeneuve d'Ascq Cedex, France;
authors.forename: Elise
authors.initials: E
authors.lastname: Barillot
authors.affiliation: Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, F-78026 Versailles, France;
authors.forename: Estelle
authors.initials: E
authors.lastname: Wenes
authors.affiliation: Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, F-78026 Versailles, France;
authors.forename: Lucy
authors.initials: L
authors.lastname: Botran
authors.affiliation: Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, F-78026 Versailles, France;
authors.forename: Stéphanie
authors.initials: S
authors.lastname: Durand
authors.affiliation: Laboratoire Evolution, Ecologie et Paléontologie, UMR CNRS 8198, Université de Lille, F-59655 Villeneuve d'Ascq Cedex, France;
authors.forename: Romain
authors.initials: R
authors.lastname: Villoutreix
authors.affiliation: Mathematiques et Informatique Appliquées, AgroParisTech, INRA, Université Paris-Saclay, 75005 Paris, France; Institute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRA, Université Paris-Sud, Université Evry, Université Paris-Saclay, Batiment 630, F-91405 Orsay, France; Institute of Plant Sciences Paris-Saclay IPS2, Paris Diderot, Sorbonne Paris-Cité, Bâtiment 630, F-91405 Orsay, France.
authors.forename: Marie-Laure
authors.initials: ML
authors.lastname: Martin-Magniette
authors.affiliation: Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, F-78026 Versailles, France;
authors.forename: Christine
authors.initials: C
authors.lastname: Camilleri
authors.affiliation: Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, F-78026 Versailles, France; Francoise.Budar@versailles.inra.fr.
authors.forename: Françoise
authors.initials: F
authors.lastname: Budar
mesh_terms: D000222:Adaptation, Physiological; D017360:Arabidopsis / Q000235:genetics* / Q000502:physiology*; D005075:Biological Evolution; D002467:Cell Nucleus / Q000235:genetics / Q000502:physiology; D003593:Cytoplasm / Q000235:genetics / Q000502:physiology; D004843:Epistasis, Genetic; D056084:Genetic Fitness; D014644:Genetic Variation; D018745:Genome, Plant; D010641:Phenotype
keywords: cytolines; cytoplasm × nucleus interactions; fitness-related traits; organelles; plant adaptation