Structural evolution drives diversification of the large LRR-RLK gene family

Cells are continuously exposed to chemical signals that they must discriminate between and respond to appropriately. In embryophytes, the Leucine-Rich Repeat Receptor-Like Kinases (LRR-RLKs) are signal receptors critical in development and defense. LRR-RLKs have diversified to hundreds of genes in many plant genomes. Although intensively studied, a well-resolved LRR-RLK gene tree has remained elusive. 

To resolve the LRR-RLK gene tree, we developed an improved gene discovery method based on iterative Hidden Markov Model (HMM)-searching and phylogenetic inference. We used this method to infer complete gene trees for each of the LRR-RLK subclades, and reconstructed the deepest nodes of the full gene family.

We discovered that the LRR-RLK gene family is even larger than previously thought, and that protein domain gains and losses are prevalent. These structural modifications, some of which likely predate embryophyte diversification, led to misclassification of some LRR-RLK variants as members of other gene families. Our work corrects this misclassification.

Our results reveal ongoing structural evolution generating novel LRR-RLK genes. These new genes are raw material for the diversification of signaling in development and defense. Our methods also enable phylogenetic reconstruction in any large gene family.

细胞持续暴露于各类化学信号环境中，必须对其进行精准甄别并做出恰当响应。在有胚植物（embryophytes）中，富含亮氨酸重复序列类受体激酶（Leucine-Rich Repeat Receptor-Like Kinases，LRR-RLKs）是调控植物发育与免疫防御的关键信号受体。在诸多植物基因组中，LRR-RLKs已扩增至数百个基因拷贝。尽管该家族已被广泛研究，但目前仍缺乏分辨率较高的LRR-RLKs完整基因树。

为解析LRR-RLKs基因树，我们开发了一种基于迭代隐马尔可夫模型（Hidden Markov Model，HMM）搜索与系统发育推断的改进型基因挖掘方法。利用该方法，我们为每个LRR-RLKs亚分支构建了完整基因树，并重构了该基因家族全谱系的深层演化节点。

研究发现，LRR-RLKs基因家族的规模远超此前认知，且蛋白质结构域的获得与丢失事件极为普遍。这些结构变异部分甚至早于有胚植物的分化事件发生，其导致部分LRR-RLK变异体被错误归类为其他基因家族成员，而本研究纠正了这一分类误差。

研究结果揭示了持续进行的结构进化过程可产生全新的LRR-RLK基因，这些新基因为植物发育与防御信号通路的多样化提供了原始进化素材。此外，本研究开发的方法同样适用于任何大型基因家族的系统发育重建。