Shahbazi Mehrdad, Kneřová Jana, Kubíková Denisa, Doležalová Alžběta, Szecówka Marek, Santos Yasmim Dutra, Wendel Jonathan F, Sharbrough Joel, Kopecký David
Centre of Plant Structural and Functional Genomics, Institute of Experimental Botany of the Czech Academy of Sciences, Olomouc, Czech Republic.
National Centre for Biomolecular Research, Faculty of Science, Masaryk University, Brno, Czech Republic.
Plant J. 2025 Aug;123(4):e70451. doi: 10.1111/tpj.70451.
Plants rely on tight coordination between nuclear, mitochondrial, and chloroplast genomes to form essential multi-enzyme cytonuclear complexes. Whole-genome duplication (WGD) doubles the nuclear genome, potentially disrupting cytonuclear stoichiometry unless organellar genomes respond accordingly. Targeted analyses of chloroplasts and mitochondria enabled us to dissect the extent and mechanisms of adjustments in both organelles immediately after WGD and across generations in Arabidopsis auto- and allopolyploids. We observed a substantial overcompensation of organellar genome copies in both organelles in early-generation autotetraploids primarily through multiplication of DNA copies within organelles rather than increasing the number of organelles. Despite higher DNA content, mitochondria maintained their volume, and chloroplasts were even smaller. In successive generations, chloroplast DNA copy numbers continued to rise, whereas mitochondrial DNA copies declined. Gene expression patterns also differed between chloroplasts and mitochondria and between auto- and allopolyploids. In autopolyploids, immediate transcriptional changes were minimal, but by the fourth generation after WGD, nuclear genes involved in mitochondria-nuclear complexes were downregulated. In allopolyploids, transcriptional changes appeared immediately in the first generation (chloroplast genes were upregulated and mitochondrial genes were downregulated). Our findings demonstrate that cytonuclear balance is restored through dynamic, organelle-specific, and polyploid-type-specific mechanisms. These insights advance our understanding of the evolution of polyploid genomes.
植物依赖于核基因组、线粒体基因组和叶绿体基因组之间的紧密协调，以形成必需的多酶细胞-核复合物。全基因组复制（WGD）使核基因组加倍，可能会破坏细胞-核化学计量，除非细胞器基因组做出相应反应。对叶绿体和线粒体的靶向分析使我们能够剖析拟南芥同源多倍体和异源多倍体在WGD后立即以及跨代过程中两个细胞器的调整程度和机制。我们观察到，在早期世代的同源四倍体中，两个细胞器的细胞器基因组拷贝数都有显著的过度补偿，主要是通过细胞器内DNA拷贝的增殖，而不是增加细胞器的数量。尽管DNA含量较高，但线粒体维持了其体积，而叶绿体甚至更小。在连续世代中，叶绿体DNA拷贝数持续上升，而线粒体DNA拷贝数下降。叶绿体和线粒体之间以及同源多倍体和异源多倍体之间的基因表达模式也有所不同。在同源多倍体中，立即发生的转录变化很小，但在WGD后的第四代，参与线粒体-核复合物的核基因被下调。在异源多倍体中，转录变化在第一代就立即出现（叶绿体基因上调，线粒体基因下调）。我们的研究结果表明，细胞-核平衡是通过动态的、细胞器特异性的和多倍体类型特异性的机制恢复的。这些见解推进了我们对多倍体基因组进化的理解。
