Cytonuclear interactions remain stable during allopolyploid evolution despite repeated whole-genome duplications in Brassica.

Brassica napus Brassica oleracea Brassica rapa allopolyploidy chloroplast duplicated genes genome inheritance intergenomic conflicts interspecific hybridization

Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
05 2019
Historique:
received: 31 05 2018
revised: 14 12 2018
accepted: 02 01 2019
pubmed: 4 1 2019
medline: 28 4 2020
entrez: 4 1 2019
Statut: ppublish

Résumé

Several plastid macromolecular protein complexes are encoded by both nuclear and plastid genes. Therefore, cytonuclear interactions are held in place to prevent genomic conflicts that may lead to incompatibilities. Allopolyploidy resulting from hybridization and genome doubling of two divergent species can disrupt these fine-tuned interactions, as newly formed allopolyploid species confront biparental nuclear chromosomes with a uniparentally inherited plastid genome. To avoid any deleterious effects of unequal genome inheritance, preferential transcription of the plastid donor over the other donor has been hypothesized to occur in allopolyploids. We used Brassica as a model to study the effects of paleopolyploidy in diploid parental species, as well as the effects of recent and ancient allopolyploidy in Brassica napus, on genes implicated in plastid protein complexes. We first identified redundant nuclear copies involved in those complexes. Compared with cytosolic protein complexes and with genome-wide retention rates, genes involved in plastid protein complexes show a higher retention of genes in duplicated and triplicated copies. Those redundant copies are functional and are undergoing strong purifying selection. We then compared transcription patterns and sequences of those redundant gene copies between resynthesized allopolyploids and their diploid parents. The neopolyploids showed no biased subgenome expression or maternal homogenization via gene conversion, despite the presence of some non-synonymous substitutions between plastid genomes of parental progenitors. Instead, subgenome dominance was observed regardless of the maternal progenitor. Our results provide new insights on the evolution of plastid protein complexes that could be tested and generalized in other allopolyploid species.

Identifiants

pubmed: 30604905
doi: 10.1111/tpj.14228
doi:

Banques de données

GENBANK
['MG717286', 'MG717287', 'MG717288', 'MG717289', 'NC_029334', 'NC_000932', 'JF317353', 'NC_016668', 'NC_007500', 'NC_007602']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

434-447

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L027844/1
Pays : United Kingdom

Informations de copyright

© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.

Auteurs

Julie Ferreira de Carvalho (J)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Jérémy Lucas (J)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Gwenaëlle Deniot (G)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Cyril Falentin (C)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Olivier Filangi (O)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Marie Gilet (M)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Fabrice Legeai (F)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Maryse Lode (M)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Jérôme Morice (J)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Gwenn Trotoux (G)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Jean-Marc Aury (JM)

Commissariat à l'Energie Atomique, Genoscope, Institut de biologie François-Jacob, Evry, 91057, France.

Valérie Barbe (V)

Commissariat à l'Energie Atomique, Genoscope, Institut de biologie François-Jacob, Evry, 91057, France.

Jean Keller (J)

UMR CNRS 6553 ECOBIO, OSUR, Université de Rennes 1, Rennes, 35042, France.

Rod Snowdon (R)

Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Heinrich-Buff-Ring 26-32, Giessen, 35392, Germany.

Zhesi He (Z)

Department of Biology, University of York, Heslington, York, YO10 5DD, UK.

France Denoeud (F)

Commissariat à l'Energie Atomique, Genoscope, Institut de biologie François-Jacob, Evry, 91057, France.
UMR CNRS 8030, Evry, CP5706, France.
Université d'Evry-Val-d'Essonne, Université Paris-Saclay, Evry, 91000, France.

Patrick Wincker (P)

Commissariat à l'Energie Atomique, Genoscope, Institut de biologie François-Jacob, Evry, 91057, France.
UMR CNRS 8030, Evry, CP5706, France.
Université d'Evry-Val-d'Essonne, Université Paris-Saclay, Evry, 91000, France.

Ian Bancroft (I)

Department of Biology, University of York, Heslington, York, YO10 5DD, UK.

Anne-Marie Chèvre (AM)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Mathieu Rousseau-Gueutin (M)

IGEPP, INRA, Agrocampus Ouest, Université de Rennes 1, Le Rheu, 35653, France.

Articles similaires

Genome Size Genome, Plant Magnoliopsida Evolution, Molecular Arabidopsis
Genome, Chloroplast Phylogeny Evolution, Molecular Ilex Microsatellite Repeats
Citrus Phenylalanine Ammonia-Lyase Stress, Physiological Multigene Family Phylogeny
Genome, Plant Medicago sativa Crops, Agricultural Genomics Polyploidy

Classifications MeSH