The evolutionarily diverged single-stranded DNA-binding proteins SSB1/SSB2 differentially affect the replication, recombination and mutation of organellar genomes in Arabidopsis thaliana

doi:10.1016/j.pld.2024.11.001

Plant Diversity ›› 2025, Vol. 47 ›› Issue (01): 127-135.DOI: 10.1016/j.pld.2024.11.001

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The evolutionarily diverged single-stranded DNA-binding proteins SSB1/SSB2 differentially affect the replication, recombination and mutation of organellar genomes in Arabidopsis thaliana

Weidong Zhu^a,b, Jie Qian^c, Yingke Hou^a,f,g, Luke R. Tembrock^d, Liyun Nie^a,e, Yi-Feng Hsu^c, Yong Xiang^a, Yi Zou^a, Zhiqiang Wu^a

a. Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China;
b. Guangdong Laboratory for Lingnan Modern Agriculture, College of Life Sciences, South China Agricultural University, Guangzhou 510642, China;
c. School of Life Sciences, Southwest University, Chongqing 400715, China;
d. Department of Biology, Colorado State University, Fort Collins, CO 80523, USA;
e. School of Medical, Molecular and Forensic Sciences, Murdoch University, Murdoch, WA 6149, Australia;
f. State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, China;
g. Shenzhen Research Institute of Henan University, Shenzhen 518000, China

Received:2024-08-06 Revised:2024-11-03 Online:2025-02-15 Published:2025-01-25
Contact: Yi Zou,E-mail:zouyi@caas.cn;Zhiqiang Wu,E-mail:wuzhiqiang@caas.cn
Supported by:
This work was supported by grants from the National Natural Science Foundation of China (32170238, 32400191), Guangdong Basic and Applied Basic Research Foundation (2023A1515111029), the Science, Technology and Innovation Commission of Shenzhen Municipality (RCYX20200714114538196), the Chinese Academy of Agricultural Sciences Elite Youth Program (grant 110243160001007) and the Guangdong Pearl River Talent Program (2021QN02N792).

The evolutionarily diverged single-stranded DNA-binding proteins SSB1/SSB2 differentially affect the replication, recombination and mutation of organellar genomes in Arabidopsis thaliana

Weidong Zhu^a,b, Jie Qian^c, Yingke Hou^a,f,g, Luke R. Tembrock^d, Liyun Nie^a,e, Yi-Feng Hsu^c, Yong Xiang^a, Yi Zou^a, Zhiqiang Wu^a

a. Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China;
b. Guangdong Laboratory for Lingnan Modern Agriculture, College of Life Sciences, South China Agricultural University, Guangzhou 510642, China;
c. School of Life Sciences, Southwest University, Chongqing 400715, China;
d. Department of Biology, Colorado State University, Fort Collins, CO 80523, USA;
e. School of Medical, Molecular and Forensic Sciences, Murdoch University, Murdoch, WA 6149, Australia;
f. State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, China;
g. Shenzhen Research Institute of Henan University, Shenzhen 518000, China

通讯作者: Yi Zou,E-mail:zouyi@caas.cn;Zhiqiang Wu,E-mail:wuzhiqiang@caas.cn
基金资助:
This work was supported by grants from the National Natural Science Foundation of China (32170238, 32400191), Guangdong Basic and Applied Basic Research Foundation (2023A1515111029), the Science, Technology and Innovation Commission of Shenzhen Municipality (RCYX20200714114538196), the Chinese Academy of Agricultural Sciences Elite Youth Program (grant 110243160001007) and the Guangdong Pearl River Talent Program (2021QN02N792).

Abstract

Abstract: Single-stranded DNA-binding proteins (SSBs) play essential roles in the replication, recombination and repair processes of organellar DNA molecules. In Arabidopsis thaliana, SSBs are encoded by a small family of two genes (SSB1 and SSB2). However, the functional divergence of these two SSB copies in plants remains largely unknown, and detailed studies regarding their roles in the replication and recombination of organellar genomes are still incomplete. In this study, phylogenetic, gene structure and protein motif analyses all suggested that SSB1 and SSB2 probably diverged during the early evolution of seed plants. Based on accurate long-read sequencing results, ssb1 and ssb2 mutants had decreased copy numbers for both mitochondrial DNA (mtDNA) and plastid DNA (ptDNA), accompanied by a slight increase in structural rearrangements mediated by intermediate-sized repeats in mt genome and small-scale variants in both genomes. Our findings provide an important foundation for further investigating the effects of DNA dosage in the regulation of mutation frequencies in plant organellar genomes.

Key words: SSB, Organellar genomes, Replication, Recombination, Mutation

摘要： Single-stranded DNA-binding proteins (SSBs) play essential roles in the replication, recombination and repair processes of organellar DNA molecules. In Arabidopsis thaliana, SSBs are encoded by a small family of two genes (SSB1 and SSB2). However, the functional divergence of these two SSB copies in plants remains largely unknown, and detailed studies regarding their roles in the replication and recombination of organellar genomes are still incomplete. In this study, phylogenetic, gene structure and protein motif analyses all suggested that SSB1 and SSB2 probably diverged during the early evolution of seed plants. Based on accurate long-read sequencing results, ssb1 and ssb2 mutants had decreased copy numbers for both mitochondrial DNA (mtDNA) and plastid DNA (ptDNA), accompanied by a slight increase in structural rearrangements mediated by intermediate-sized repeats in mt genome and small-scale variants in both genomes. Our findings provide an important foundation for further investigating the effects of DNA dosage in the regulation of mutation frequencies in plant organellar genomes.

关键词: SSB, Organellar genomes, Replication, Recombination, Mutation

Weidong Zhu, Jie Qian, Yingke Hou, Luke R. Tembrock, Liyun Nie, Yi-Feng Hsu, Yong Xiang, Yi Zou, Zhiqiang Wu. The evolutionarily diverged single-stranded DNA-binding proteins SSB1/SSB2 differentially affect the replication, recombination and mutation of organellar genomes in Arabidopsis thaliana[J]. Plant Diversity, 2025, 47(01): 127-135.

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The evolutionarily diverged single-stranded DNA-binding proteins SSB1/SSB2 differentially affect the replication, recombination and mutation of organellar genomes in Arabidopsis thaliana

The evolutionarily diverged single-stranded DNA-binding proteins SSB1/SSB2 differentially affect the replication, recombination and mutation of organellar genomes in Arabidopsis thaliana

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