Zedek František, Šmerda Jakub, Halasová Aneta, Adamec Lubomír, Veleba Adam, Plačková Klára, Bureš Petr
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic.
Department of Experimental and Functional Morphology, Institute of Botany of the Czech Academy of Sciences, Dukelská 135, 37901, Třeboň, Czech Republic.
Ann Bot. 2024 Dec 31;134(7):1131-1138. doi: 10.1093/aob/mcae107.
Species of the carnivorous family Lentibulariaceae exhibit the smallest genomes in flowering plants. We explored the hypothesis that their minute genomes result from the unique mitochondrial cytochrome c oxidase (COX) mutation. The mutation may boost mitochondrial efficiency, which is especially useful for suction-bladder traps of Utricularia, but also increase DNA-damaging reactive oxygen species, leading to genome shrinkage through deletion-biased DNA repair. We aimed to explore the impact of this mutation on genome size, providing insights into genetic mutation roles in plant genome evolution under environmental pressures.
We compiled and measured genome and mean chromosome sizes for 127 and 67 species, respectively, representing all three genera (Genlisea, Pinguicula and Utricularia) of Lentibulariaceae. We also isolated and analysed COX sequences to detect the mutation. Through phylogenetic regressions and Ornstein-Uhlenbeck models of trait evolution, we assessed the impact of the COX mutation on the genome and chromosome sizes across the family.
Our findings reveal significant correlations between the COX mutation and smaller genome and chromosome sizes. Specifically, species carrying the ancestral COX sequence exhibited larger genomes and chromosomes than those with the novel mutation. This evidence supports the notion that the COX mutation contributes to genome downsizing, with statistical analyses confirming a directional evolution towards smaller genomes in species harbouring these mutations.
Our study confirms that the COX mutation in Lentibulariaceae is associated with genome downsizing, probably driven by increased reactive oxygen species production and subsequent DNA damage requiring deletion-biased repair mechanisms. While boosting mitochondrial energy output, this genetic mutation compromises genome integrity and may potentially affect recombination rates, illustrating a complex trade-off between evolutionary advantages and disadvantages. Our results highlight the intricate processes by which genetic mutations and environmental pressures shape genome size evolution in carnivorous plants.
狸藻科食肉植物的物种在开花植物中拥有最小的基因组。我们探讨了这样一种假说，即它们微小的基因组源于独特的线粒体细胞色素c氧化酶（COX）突变。这种突变可能会提高线粒体效率，这对狸藻的捕虫囊陷阱特别有用，但也会增加破坏DNA的活性氧，通过偏向缺失的DNA修复导致基因组收缩。我们旨在探究这种突变对基因组大小的影响，从而深入了解在环境压力下基因突变在植物基因组进化中的作用。
我们分别汇编并测量了狸藻科三个属（螺旋狸藻属、捕虫堇属和狸藻属）的127个和67个物种的基因组大小和平均染色体大小。我们还分离并分析了COX序列以检测该突变。通过系统发育回归和性状进化的奥恩斯坦 - 乌伦贝克模型，我们评估了COX突变对整个科的基因组和染色体大小的影响。
我们的研究结果揭示了COX突变与较小的基因组和染色体大小之间存在显著相关性。具体而言，携带祖先COX序列的物种比具有新突变的物种表现出更大的基因组和染色体。这一证据支持了COX突变导致基因组缩小的观点，统计分析证实了在携带这些突变的物种中朝着更小基因组的定向进化。
我们的研究证实，狸藻科中的COX突变与基因组缩小有关，可能是由活性氧产生增加以及随后需要偏向缺失修复机制的DNA损伤所驱动。虽然这种基因突变提高了线粒体能量输出，但它损害了基因组完整性，并可能潜在地影响重组率，说明了进化利弊之间的复杂权衡。我们的结果突出了基因突变和环境压力塑造食肉植物基因组大小进化的复杂过程。
