Evolutionary dynamics of mitochondrial genomes and intracellular transfers among diploid and allopolyploid cotton species

Jiali Kong; Jie Wang; Liyun Nie; Luke R Tembrock; Changsong Zou; Shenglong Kan; Xiongfeng Ma; Jonathan F Wendel; Zhiqiang Wu

doi:10.1186/s12915-025-02115-z

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Evolutionary dynamics of mitochondrial genomes and intracellular transfers among diploid and allopolyploid cotton species

Journal article

Open access

Peer reviewed

Evolutionary dynamics of mitochondrial genomes and intracellular transfers among diploid and allopolyploid cotton species

Jiali Kong, Jie Wang, Liyun Nie, Luke R Tembrock, Changsong Zou, Shenglong Kan, Xiongfeng Ma, Jonathan F Wendel and Zhiqiang Wu

BMC biology, Vol.23(1), pp.9-20

2025

DOI: https://doi.org/10.1186/s12915-025-02115-z

PMID: 39794789

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Abstract

Diploidy

Evolution, Molecular

Genome, Mitochondrial

Genome, Plant

Gossypium - genetics

Phylogeny

Polyploidy

Plant mitochondrial genomes (mitogenomes) exhibit extensive structural variation yet extremely low nucleotide mutation rates, phenomena that remain only partially understood. The genus Gossypium, a globally important source of cotton, offers a wealth of long-read sequencing resources to explore mitogenome and plastome variation and dynamics accompanying the evolutionary divergence of its approximately 50 diploid and allopolyploid species. Here, we assembled 19 mitogenomes from Gossypium species, representing all genome groups (diploids A through G, K, and the allopolyploids AD) based on a uniformly applied strategy. A graph-based mitogenome assembly method revealed more alternative structural conformations than previously recognized, some of which confirmed the mitogenome structure reported in earlier studies on cotton. Using long-read data, we quantified alternative conformations mediated by recombination events between repeats, and phylogenetically informative structural variants were noted. Nucleotide substitution rate comparisons between coding and non-coding regions revealed low mutation rates across the entire mitogenome. Genome-wide mapping of nuclear organellar DNA transfers (NUOTs) in Gossypium revealed a nonrandom distribution of transfers in the nuclear genome. In cotton, the fate of NUOT events varied, with mitochondrion-to-nucleus transfer (NUMT) predominantly retained as short fragments in the nuclear genome, with more plastid sequences integrated into the nucleus. Phylogenetic relationships inferred using different data sets highlighted distinct evolutionary histories among these cellular compartments, providing ancillary evidence relevant to the evolutionary history of Gossypium. A comprehensive analysis of organellar genome variation demonstrates complex structural variation and low mutation rates across the entire mitogenome and reveals the history of organellar genome transfer among the three genomes throughout the cotton genus. The findings enhance our general understanding of mitogenome evolution, comparative organellar and nuclear evolutionary rates, and the history of inter-compartment genomic integration.

Details

Title: Evolutionary dynamics of mitochondrial genomes and intracellular transfers among diploid and allopolyploid cotton species
Authors/Creators: Jiali Kong - Henan University
Jie Wang - Agricultural Genomics Institute at Shenzhen
Liyun Nie - Agricultural Genomics Institute at Shenzhen
Luke R Tembrock - Colorado State University
Changsong Zou - Henan University
Shenglong Kan - Agricultural Genomics Institute at Shenzhen
Xiongfeng Ma - Chinese Academy of Agricultural Sciences
Jonathan F Wendel - Iowa State University
Zhiqiang Wu - Huazhong Agricultural University
Publication Details: BMC biology, Vol.23(1), pp.9-20
Grant note: 2021QN02N792 / the Guangdong Pearl River Talent Program No. JCYJ20220818103212025 / the Shenzhen Fundamental Research Program 110243160001007 / the Chinese Academy of Agricultural Sciences Elite Youth Program 32170238 / National Natural Science Foundation of China
Identifiers: 991005732478707891
Copyright: © The Author(s) 2025.
Murdoch Affiliation: School of Medical, Molecular and Forensic Sciences
Language: English
Resource Type: Journal article

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Collaboration types: Domestic collaboration; International collaboration
Citation topics: 3 Agriculture, Environment & Ecology; 3.4 Crop Science; 3.4.1922 Alternative Oxidase
Web Of Science research areas: Biology
ESI research areas: Biology & Biochemistry