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

Julie Ferreira de Carvalho (1) , Jérémy Lucas (1) , Gwenaëlle Deniot (1) , Cyril Falentin (1) , Olivier Filangi (1) , Marie Gilet (1) , Fabrice Legeai (1) , Maryse Lodé-Taburel (1) , Jérôme Morice (1) , Gwenn Trotoux (1) , Valérie Barbe (2) , Jean Keller (3) , Rod Snowdon (4) , Zhesi He (5) , France Denoeud (6, 7, 2) , Patrick Wincker (6, 7, 2) , Ian Bancroft (5) , Anne-Marie Chèvre (1) , Mathieu Rousseau-Gueutin (1)

1 IGEPP - Institut de Génétique, Environnement et Protection des Plantes
2 GENOSCOPE - Genoscope - Centre national de séquençage [Evry]
3 ECOBIO - Ecosystèmes, biodiversité, évolution [Rennes]
4 JLU - Justus-Liebig-Universität Gießen = Justus Liebig University
5 University of York [York, UK]
6 JACOB - Institut de Biologie François JACOB
7 UEVE - Université d'Évry-Val-d'Essonne

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 uniparentally inherited plastid genome. To avoid any deleterious effects of unequal genome inheritance, preferential transcription of the plastid donor over the other one 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 to cytosolic protein complexes and to 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 undergoing strong purifying selection. We then compared transcription patterns and sequences of those redundant gene copies between resynthesized allopolyploids and their diploid parents. The neo-polyploids showed no biased subgenome expression or maternal homogenization via gene conversion despite 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 which could be tested and generalized in other allopolyploid species. This article is protected by copyright. All rights reserved.

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

Domains: Life Sciences [q-bio]; Vegetal Biology; Botanics; Life Sciences [q-bio]; Biochemistry, Molecular Biology; Genomics [q-bio.GN]; Computer Science [cs]; Bioinformatics [q-bio.QM]

Julie Ferreira de Carvalho, Jérémy Lucas, Gwenaëlle Deniot, Cyril Falentin, Olivier Filangi, et al.. Cytonuclear interactions remain stable during allopolyploid evolution despite repeated whole-genome duplications in Brassica. Plant Journal, 2019, 98 (3), pp.434-447. ⟨10.1111/tpj.14228⟩. ⟨hal-02019346⟩