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Remarkable mitochondrial genome heterogeneity in Meniocus linifolius (Brassicaceae)

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Abstract

Key message

Detailed analyses of 16 genomes identified a remarkable acceleration of mutation rate, hence mitochondrial sequence and structural heterogeneity, in Meniocus linifolius (Brassicaceae).

Abstract

The powerhouse, mitochondria, in plants feature high levels of structural variation, while the encoded genes are normally conserved. However, the substitution rates and spectra of mitochondria DNA within the Brassicaceae, a family with substantial scientific and economic importance, have not been adequately deciphered. Here, by analyzing three newly assembled and 13 known mitochondrial genomes (mitogenomes), we report the highly variable genome structure and mutation rates in Brassicaceae. The genome sizes and GC contents are 196,604 bp and 46.83%, 288,122 bp and 44.79%, and 287,054 bp and 44.93%, for Meniocus linifolius (Mli), Crucihimalaya lasiocarpa (Cla), and Lepidium sativum (Lsa), respectively. In total, 29, 33, and 34 protein-coding genes (PCGs) and 14, 18, and 18 tRNAs are annotated for Mli, Cla, and Lsa, respectively, while all mitogenomes contain one complete circular molecule with three rRNAs and abundant RNA editing sites. The Mli mitogenome features four conformations likely mediated by the two pairs of long repeats, while at the same time seems to have an unusual evolutionary history due to higher GC content, loss of more genes and sequences, but having more repeats and plastid DNA insertions. Corroborating with these, an ambiguous phylogenetic position with long branch length and elevated synonymous substitution rate in nearly all PCGs are observed for Mli. Taken together, our results reveal a high level of mitogenome heterogeneity at the family level and provide valuable resources for further understanding the evolutionary pattern of organelle genomes in Brassicaceae.

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Availability of supporting data

The data presented in the study are deposited in the GenBank repository, with accession numbers: OQ701529, BK063239, BK063798 and OR666673 (plastome).

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Acknowledgements

This work was partially facilitated by the Germplasm Bank of Wild Species and the iFlora HPC Center of GBOWS, KIB, CAS. We appreciate Jing-ling Li, Wei Dai, Fang Liu and Landi Feng for useful discussions and kind help.

Funding

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences to D-Z.L. and J-Y.H. (XDB31000000).

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J-YH and D-ZL conceptualized and coordinated the project; JL collected the samples, analyzed, and visualized the data, and wrote the manuscript with the help from J-YH and D-ZL. All authors read and approved the final manuscript.

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Correspondence to Jin-Yong Hu or De-Zhu Li.

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Liu, J., Hu, JY. & Li, DZ. Remarkable mitochondrial genome heterogeneity in Meniocus linifolius (Brassicaceae). Plant Cell Rep 43, 36 (2024). https://doi.org/10.1007/s00299-023-03102-w

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