Literature DB >> 30604905

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

Julie Ferreira de Carvalho1, Jérémy Lucas1, Gwenaëlle Deniot1, Cyril Falentin1, Olivier Filangi1, Marie Gilet1, Fabrice Legeai1, Maryse Lode1, Jérôme Morice1, Gwenn Trotoux1, Jean-Marc Aury2, Valérie Barbe2, Jean Keller3, Rod Snowdon4, Zhesi He5, France Denoeud2,6,7, Patrick Wincker2,6,7, Ian Bancroft5, Anne-Marie Chèvre1, Mathieu Rousseau-Gueutin1.   

Abstract

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

Entities:  

Keywords:  zzm321990Brassica napuszzm321990; zzm321990Brassica oleraceazzm321990; zzm321990Brassica rapazzm321990; allopolyploidy; chloroplast; duplicated genes; genome inheritance; intergenomic conflicts; interspecific hybridization

Mesh:

Year:  2019        PMID: 30604905     DOI: 10.1111/tpj.14228

Source DB:  PubMed          Journal:  Plant J        ISSN: 0960-7412            Impact factor:   6.417


  10 in total

1.  Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels.

Authors:  Evan S Forsythe; Corrinne E Grover; Emma R Miller; Justin L Conover; Mark A Arick; M Carolina F Chavarro; Soraya C M Leal-Bertioli; Daniel G Peterson; Joel Sharbrough; Jonathan F Wendel; Daniel B Sloan
Journal:  Proc Natl Acad Sci U S A       Date:  2022-07-19       Impact factor: 12.779

2.  Genome diploidization associates with cladogenesis, trait disparity, and plastid gene evolution.

Authors:  Sheng Zuo 左胜; Xinyi Guo 郭新异; Terezie Mandáková; Mark Edginton; Ihsan A Al-Shehbaz; Martin A Lysak
Journal:  Plant Physiol       Date:  2022-08-29       Impact factor: 8.005

3.  Replaying the evolutionary tape to investigate subgenome dominance in allopolyploid Brassica napus.

Authors:  Kevin A Bird; Chad E Niederhuth; Shujun Ou; Malia Gehan; J Chris Pires; Zhiyong Xiong; Robert VanBuren; Patrick P Edger
Journal:  New Phytol       Date:  2021-01-09       Impact factor: 10.151

4.  Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum.

Authors:  Changping Li; Xiaofei Wang; Yaxian Xiao; Xuhan Sun; Jinbin Wang; Xuan Yang; Yuchen Sun; Yan Sha; Ruili Lv; Yanan Yu; Baoxu Ding; Zhibin Zhang; Ning Li; Tianya Wang; Jonathan F Wendel; Bao Liu; Lei Gong
Journal:  Mol Biol Evol       Date:  2020-12-16       Impact factor: 16.240

5.  Global Patterns of Subgenome Evolution in Organelle-Targeted Genes of Six Allotetraploid Angiosperms.

Authors:  Joel Sharbrough; Justin L Conover; Matheus Fernandes Gyorfy; Corrinne E Grover; Emma R Miller; Jonathan F Wendel; Daniel B Sloan
Journal:  Mol Biol Evol       Date:  2022-04-10       Impact factor: 8.800

6.  A temporal gradient of cytonuclear coordination of chaperonins and chaperones during RuBisCo biogenesis in allopolyploid plants.

Authors:  Changping Li; Baoxu Ding; Xintong Ma; Xuan Yang; Hongyan Wang; Yuefan Dong; Zhibin Zhang; Jinbin Wang; Xiaochong Li; Yanan Yu; Yiyang Yu; Bao Liu; Jonathan F Wendel; Yidan Li; Tianya Wang; Lei Gong
Journal:  Proc Natl Acad Sci U S A       Date:  2022-08-15       Impact factor: 12.779

7.  Variation in cytonuclear expression accommodation among allopolyploid plants.

Authors:  Corrinne E Grover; Evan S Forsythe; Joel Sharbrough; Emma R Miller; Justin L Conover; Rachael A DeTar; Carolina Chavarro; Mark A Arick; Daniel G Peterson; Soraya C M Leal-Bertioli; Daniel B Sloan; Jonathan F Wendel
Journal:  Genetics       Date:  2022-09-30       Impact factor: 4.402

Review 8.  Cytonuclear Genetic Incompatibilities in Plant Speciation.

Authors:  Zoé Postel; Pascal Touzet
Journal:  Plants (Basel)       Date:  2020-04-10

9.  Nuclear-Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid.

Authors:  Yufei Zhai; Xiaqing Yu; Zaobing Zhu; Panqiao Wang; Ya Meng; Qinzheng Zhao; Ji Li; Jinfeng Chen
Journal:  Genes (Basel)       Date:  2019-10-30       Impact factor: 4.096

10.  Genome-Wide Duplication of Allotetraploid Brassica napus Produces Novel Characteristics and Extensive Ploidy Variation in Self-Pollinated Progeny.

Authors:  Liqin Yin; Zhendong Zhu; Xuan Luo; Liangjun Huang; Yu Li; Annaliese S Mason; Jin Yang; Xianhong Ge; Yan Long; Jisheng Wang; Qiong Zou; Lanrong Tao; Zeming Kang; Rong Tang; Maolin Wang; Shaohong Fu
Journal:  G3 (Bethesda)       Date:  2020-10-05       Impact factor: 3.154

  10 in total

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