The evolution of extremely diverged plastomes in Selaginellaceae (lycophyte) is driven by repeat patterns and the underlying DNA maintenance machinery.

Selaginella sinensis GC content RNA editing dynamic mitogenome network plastome perfect repeats

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:
08 2022
Historique:
revised: 25 05 2022
received: 06 04 2022
accepted: 31 05 2022
pubmed: 2 6 2022
medline: 30 7 2022
entrez: 1 6 2022
Statut: ppublish

Résumé

Two factors are proposed to account for the unusual features of organellar genomes: the disruptions of organelle-targeted DNA replication, repair, and recombination (DNA-RRR) systems in the nuclear genome and repetitive elements in organellar genomes. Little is known about how these factors affect organellar genome evolution. The deep-branching vascular plant family Selaginellaceae is known to have a deficient DNA-RRR system and convergently evolved organellar genomes. However, we found that the plastid genome (plastome) of Selaginella sinensis has extremely accelerated substitution rates, a low GC content, pervasive repeat elements, a dynamic network structure, and it lacks direct or inverted repeats. Unexpectedly, its organelle DNA-RRR system is short of a plastid-targeted Recombinase A1 (RecA1) and a mitochondrion-targeted RecA3, in line with other explored Selaginella species. The plastome contains a large collection of short- and medium-sized repeats. Given the absence of RecA1 surveillance, we propose that these repeats trigger illegitimate recombination, accelerated mutation rates, and structural instability. The correlations between repeat quantity and architectural complexity in the Selaginella plastomes support these conclusions. We, therefore, hypothesize that the interplay of the deficient DNA-RRR system and the high repeat content has led to the extraordinary divergence of the S. sinensis plastome. Our study not only sheds new light on the mechanism of plastome divergence by emphasizing the power of cytonuclear integration, but it also reconciles the longstanding contradiction on the effects of DNA-RRR system disruption on genome structure evolution.

Identifiants

pubmed: 35648423
doi: 10.1111/tpj.15851
doi:

Substances chimiques

DNA 9007-49-2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

768-784

Informations de copyright

© 2022 Society for Experimental Biology and John Wiley & Sons Ltd.

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Auteurs

Qiao-Ping Xiang (QP)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China.

Jun-Yong Tang (JY)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.

Ji-Gao Yu (JG)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.

David Roy Smith (DR)

Department of Biology, University of Western Ontario, London, N6A 5B7, Ontario, Canada.

Yan-Mei Zhu (YM)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China.

Ya-Rong Wang (YR)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China.

Jong-Soo Kang (JS)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China.

Jie Yang (J)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.

Xian-Chun Zhang (XC)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China.

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