Ricou Anthony, Simon Matthieu, Duflos Rémi, Azzopardi Marianne, Roux Fabrice, Budar Françoise, Camilleri Christine
Université Paris-Saclay, INRAE, AgroParisTech, Institute Jean-Pierre Bourgin for Plant Sciences (IJPB), Versailles, France.
LIPME, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France.
PLoS Genet. 2025 Jan 13;21(1):e1011451. doi: 10.1371/journal.pgen.1011451. eCollection 2025 Jan.
Gamete killers are genetic loci that distort segregation in the progeny of hybrids because the killer allele promotes the elimination of the gametes that carry the sensitive allele. They are widely distributed in eukaryotes and are important for understanding genome evolution and speciation. We had previously identified a pollen killer in hybrids between two distant natural accessions of Arabidopsis thaliana. This pollen killer involves three genetically linked genes, and we previously reported the identification of the gene encoding the antidote that protects pollen grains from the killer activity. In this study, we identified the two other genes of the pollen killer by using CRISPR-Cas9 induced mutants. These two genes are necessary for the killer activity that we demonstrated to be specific to pollen. The cellular localization of the pollen killer encoded proteins suggests that the pollen killer activity involves the mitochondria. Sequence analyses reveal predicted domains from the same families in the killer proteins. In addition, the C-terminal half of one of the killer proteins is identical to the antidote, and one amino acid, crucial for the antidote activity, is also essential for the killer function. Investigating more than 700 worldwide accessions of A. thaliana, we confirmed that the locus is subject to important structural rearrangements and copy number variation. By exploiting available de novo genomic sequences, we propose a scenario for the emergence of this pollen killer in A. thaliana. Furthermore, we report the co-occurrence and behavior of killer and sensitive genotypes in several local populations, a prerequisite for studying gamete killer evolution in the wild. This highlights the potential of the Arabidopsis model not only for functional studies of gamete killers but also for investigating their evolutionary trajectories at complementary geographical scales.
配子杀手是一些基因位点，它们会扭曲杂种后代的分离情况，因为杀手等位基因会促使携带敏感等位基因的配子被消除。它们广泛分布于真核生物中，对于理解基因组进化和物种形成很重要。我们之前在拟南芥的两个远缘自然变种的杂种中鉴定出了一种花粉杀手。这种花粉杀手涉及三个基因连锁的基因，我们之前报道了编码解毒剂的基因的鉴定，该解毒剂可保护花粉粒免受杀手活性的影响。在本研究中，我们利用CRISPR-Cas9诱导的突变体鉴定出了花粉杀手的另外两个基因。这两个基因对于我们证明为花粉特异性的杀手活性是必需的。花粉杀手编码蛋白的细胞定位表明花粉杀手活性涉及线粒体。序列分析揭示了杀手蛋白中来自相同家族的预测结构域。此外，其中一种杀手蛋白的C端一半与解毒剂相同，对于解毒剂活性至关重要的一个氨基酸对于杀手功能也必不可少。对全球700多个拟南芥变种进行研究后，我们证实该基因座经历了重要的结构重排和拷贝数变异。通过利用可用的从头基因组序列，我们提出了这种花粉杀手在拟南芥中出现的一种情况。此外，我们报告了杀手和敏感基因型在几个当地种群中的共存和行为，这是研究野生环境中配子杀手进化的一个前提条件。这突出了拟南芥模型不仅在配子杀手功能研究方面的潜力，而且在互补地理尺度上研究其进化轨迹方面的潜力。
