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Front. Plant Sci. | doi: 10.3389/fpls.2019.00032

NOVEL CYTONUCLEAR COMBINATIONS MODIFY ARABIDOPSIS THALIANA SEED PHYSIOLOGY AND VIGOR

 Clément Boussardon1, Marie-Laure Martin-Magniette2, 3, 4, Béatrice Godin1, Abdelilah Benamar5,  Benjamin Vittrant2,  Sylvie Citerne1, Tristan Mary-Huard6, 7,  David Macherel5, Loïc Rajjou1 and  Françoise BUDAR8*
  • 1Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, France
  • 2UMR MIA-Paris, AgroParisTech, INRA, Université Paris-Saclay, ,, France
  • 3Institute of Plant Sciences Paris Saclay IPS2, CNRS, INRA, Université Paris-Sud, Université Evry, Université Paris-Saclay, France
  • 4Institute of Plant Sciences Paris-Saclay IPS2, Paris Diderot, Sorbonne Paris-Cité, France
  • 5IRHS, Université d’Angers, INRA, Agrocampus Ouest, UMR 1345, SFR 4207 QUASAV, France
  • 6UMR MIA-Paris, AgroParisTech, INRA, Université Paris-Saclay, France
  • 7Génétique Quantitative et Evolution–Le Moulon, INRA, Université Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, France
  • 8INRA UMR1318 Institut Jean Pierre Bourgin, France

Dormancy and germination vigor are complex traits of primary importance for adaptation and agriculture. Intraspecific variation in cytoplasmic genomes and cytonuclear interactions were previously reported to affect germination in Arabidopsis using novel cytonuclear combinations that disrupt coadaptation between natural variants of nuclear and cytoplasmic genomes. However, specific aspects of dormancy and germination vigor were not thoroughly explored, nor the parental contributions to the genetic effects.
Here, we specifically assessed dormancy, germination performance and longevity of seeds from Arabidopsis plants with natural and new genomic compositions. All three traits were modified by cytonuclear reshuffling. Both depth and release rate of dormancy could be modified by a changing of cytoplasm. Significant changes on dormancy and germination performance due to specific cytonuclear interacting combinations mainly occurred in opposite directions, consistent with the idea that a single physiological consequence of the new genetic combination affected both traits oppositely. However, this was not always the case.
Interestingly, the ability of parental accessions to contribute to significant cytonuclear interactions modifying the germination phenotype was different depending on whether they provided the nuclear or cytoplasmic genetic compartment. The observed deleterious effects of novel cytonuclear combinations (in comparison with the nuclear parent) were consistent with a contribution of cytonuclear interactions to germination adaptive phenotypes. More surprisingly, we also observed favorable effects of novel cytonuclear combinations, suggesting suboptimal genetic combinations exist in natural populations for these traits. Reduced sensitivity to exogenous ABA and faster endogenous ABA decay during germination were observed in a novel cytonuclear combination that also exhibited enhanced longevity and better germination performance, compared to its natural nuclear parent. Taken together, our results strongly support that cytoplasmic genomes represent an additional resource of natural variation for breeding seed vigor traits.

Keywords: cytolines, cytonuclear co-adaptation, Cytonuclear interaction, dormancy, Seed longevity, Germination, Seed vigor

Received: 05 Oct 2018; Accepted: 10 Jan 2019.

Edited by:

Philippe Giegé, Center for the National Scientific Research (CNRS), France

Reviewed by:

Elina Welchen, National University of the Littoral, Argentina
Véronique Larosa, University of Liège, Belgium  

Copyright: © 2019 Boussardon, Martin-Magniette, Godin, Benamar, Vittrant, Citerne, Mary-Huard, Macherel, Rajjou and BUDAR. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Françoise BUDAR, INRA UMR1318 Institut Jean Pierre Bourgin, Versailles, France, francoise.budar@inra.fr