Yang Li, Liu Shengyi, Schranz M Eric, Bouwmeester Klaas
Biosystematics Group, Wageningen University and Research, Droevendaalsesteeg 1, Wageningen, 6708 PB, The Netherlands.
Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture, Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan, Hubei, 430062, China.
BMC Plant Biol. 2025 Jan 22;25(1):91. doi: 10.1186/s12870-025-06099-4.
HOPZ-ACTIVATED RESISTANCE 1 (ZAR1) is a nucleotide-binding leucine-rich repeat (NLR) protein functioning as a recognition hub to initiate effector-triggered immunity against bacterial pathogens. To initiate defense, ZAR1 associates with different HOPZ-ETI-DEFICIENT 1 (ZED1)-Related Kinases (ZRKs) to form resistosomes to indirectly perceive effector-induced perturbations. Few studies have focused on the phylogenomic characteristics of ZAR1 and ZRK immune gene families and their evolutionary relationships. To trace the origin and divergence of ZAR1 and ZRK immune gene families across the plant kingdom, we performed phylogenomic analyses using an extended set of plant genomes.
Genome-wide identification of ZAR1 and ZRK immune gene families by blast similarity searches combined with phylogenetic analysis showed that these two gene families have experienced frequent gene losses in massive lineages. Gene distribution patterns across the plant kingdom revealed that ZAR1 and ZRK emerged after the divergence of most angiosperms from Amborella and before the split of magnoliids, monocots, and eudicots. Co-occurrence of ZAR1-A and ZRKs was found in various plant species belonging to different angiosperm orders, but both genes were found to be absent in chlorophyta, bryophytes, lycophytes, ferns, and gymnosperms. We also detected a large number of concerted gene losses in angiosperms, especially within the orders Fabales, Cucurbitales, Asterales, and Apiales. All analysed monocot genomes thus far examined, except for the aroid Colocasia esculenta, were previously reported to lack both ZAR1-A and ZRKs. Here we now report other exceptions on the concerted ZAR1-A-ZRKs presence-absence pattern within several early diverging monocot lineages, including the genome of Acorus tatarinowii-a species representing the first branching monocot lineage. We also revealed strong variation in ZAR1-A-ZRKs co-occurrence within the asterid order Ericales, suggesting patterns of de-coevolution in angiosperms. Our research further shows that both gene families experienced significant diversification through various duplication events. Additionally, their evolutionary paths have been shaped by frequent gene losses and lineage-specific transposition.
This study provides novel findings on the evolution of ZAR1 and ZRK immune gene families across a wide range of plant species, suggesting that more potential exceptions can be expected when expanding the list of sequenced genomes from distinct orders. Our results provide new hypotheses about the origin and diversification of these critical immune genes for future functional studies.
HOPZ激活抗性1（ZAR1）是一种核苷酸结合富含亮氨酸重复序列（NLR）蛋白，作为识别枢纽启动针对细菌病原体的效应子触发免疫。为启动防御，ZAR1与不同的HOPZ-ETI缺陷1（ZED1）相关激酶（ZRK）结合形成抗病小体，以间接感知效应子诱导的扰动。很少有研究关注ZAR1和ZRK免疫基因家族的系统基因组特征及其进化关系。为追溯ZAR1和ZRK免疫基因家族在整个植物界的起源和分化，我们使用一组扩展的植物基因组进行了系统基因组分析。
通过Blast相似性搜索结合系统发育分析对ZAR1和ZRK免疫基因家族进行全基因组鉴定，结果表明这两个基因家族在大量谱系中经历了频繁的基因丢失。植物界的基因分布模式表明，ZAR1和ZRK在大多数被子植物与无油樟分化之后、木兰类植物、单子叶植物和真双子叶植物分化之前出现。在属于不同被子植物目 的各种植物物种中发现了ZAR1-A和ZRK的共现，但在绿藻、苔藓植物、石松植物、蕨类植物和裸子植物中均未发现这两个基因。我们还在被子植物中检测到大量协同基因丢失，特别是在豆目、葫芦目、菊目和伞形目 中。到目前为止，除了天南星科的芋之外，所有分析的单子叶植物基因组都被报道缺乏ZAR1-A和ZRK。在这里，我们现在报告了几个早期分化的单子叶植物谱系中ZAR1-A-ZRK共现模式的其他例外情况，包括代表第一个分支单子叶植物谱系的石菖蒲基因组。我们还揭示了杜鹃花目 中ZAR1-A-ZRK共现的强烈变异，表明被子植物中存在反协同进化模式。我们的研究进一步表明，这两个基因家族都通过各种复制事件经历了显著的多样化。此外，它们的进化路径受到频繁的基因丢失和谱系特异性转座的影响。
本研究提供了关于ZAR1和ZRK免疫基因家族在广泛植物物种中进化的新发现，表明在扩大来自不同目 的测序基因组列表时可能会有更多潜在的例外情况。我们的结果为这些关键免疫基因的起源和多样化提供了新的假设，以供未来进行功能研究。
