Unequally Abundant Chromosomes and Unusual Collections of Transferred Sequences Characterize Mitochondrial Genomes of Gastrodia (Orchidaceae), One of the Largest Mycoheterotrophic Plant Genera

文献类型： 外文期刊

第一作者： Wang, Hanchen

作者： Wang, Hanchen;Shao, Bingyi;Li, Jingrui;Wen, Yingying;Qin, Shiyu;Jin, Xiaohua;Wang, Hanchen;Shao, Bingyi;Wang, Deyi;Wang, Deyi;Li, Zhanghai;Chase, Mark W.;Chase, Mark W.;Li, Jianwu;Feng, Yanlei;Qin, Shiyu;Chen, Binghua;Wu, Zhiqiang

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关键词： organelle genome; convergent evolution; plant-microbe interaction; horizontal gene transfer; mutation rate

期刊名称：MOLECULAR BIOLOGY AND EVOLUTION （ 影响因子：5.3； 五年影响因子：11.9 ）

ISSN： 0737-4038

年卷期： 2025 年 42 卷 4 期

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收录情况： SCI

摘要： The mystery of genomic alternations in heterotrophic plants is among the most intriguing in evolutionary biology. Compared to plastid genomes (plastomes) with parallel size reduction and gene loss, mitochondrial genome (mitogenome) variation in heterotrophic plants remains underexplored in many aspects. To further unravel the evolutionary outcomes of heterotrophy, we present a comparative mitogenomic study with 13 de novo assemblies of Gastrodia (Orchidaceae), one of the largest fully mycoheterotrophic plant genera, and its relatives. Analyzed Gastrodia mitogenomes range from 0.56 to 2.1 Mb, each consisting of numerous, unequally abundant chromosomes or contigs. Size variation might have evolved through chromosome rearrangements followed by stochastic loss of "dispensable" chromosomes, with deletion-biased mutations. The discovery of a hyper-abundant (similar to 15 times intragenomic average) chromosome in two assemblies represents the hitherto most extreme copy number variation in any mitogenomes, with similar architectures discovered in two metazoan lineages. Transferred sequence contents highlight asymmetric evolutionary consequences of heterotrophy: despite drastically reduced intracellular plastome transfers convergent across heterotrophic plants, their rarity of horizontally acquired sequences sharply contrasts parasitic plants, where massive transfers from their hosts prevail. Rates of sequence evolution are markedly elevated but not explained by copy number variation, extending prior findings of accelerated molecular evolution from parasitic to heterotrophic plants. Putative evolutionary scenarios for these mitogenomic convergence and divergence fit well with the common (e.g. plastome contraction) and specific (e.g. host identity) aspects of the two heterotrophic types. These idiosyncratic mycoheterotrophs expand known architectural variability of plant mitogenomes and provide mechanistic insights into their content and size variation.

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