Conserved role of the SERK‒BIR module in development and immunity across land plants

In the model angiosperm Arabidopsis thaliana, SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES (SERKs), which are subfamily II of leucine-rich repeat receptor-like kinases (LRR-RLKs), play diverse roles in development and immunity as co-receptors for a multitude of LRR-RLKs including BRASSINOSTEROID INSENSITIVE 1 (BRI1) and FLAGELLIN SENSITIVE 2 (FLS2) . The conserved tyrosine (Y) residue in AtSERK3 plays a crucial role in signaling specificity for differentiating AtBRI1- and AtFLS2-mediated pathways. BRI ASSOCIATED RECEPTOR KINASE 1 (BAK1)-INTERACTING RECEPTOR-LIKE KINASES (BIRs) interact with SERKs under resting conditions, negatively regulating SERK-mediated pathways. SERK and BIR are highly conserved in land plants, whereas BRI1 and FLS2 homologs are absent or poorly conserved in bryophyte lineages. Very little is known about biological functions of SERK homologs in non-flowering plants. The genome of the model liverwort Marchantia polymorpha encodes the single SERK and BIR homolog, namely MpSERK and MpBIR. We here show that Mpserk disruptants display growth and developmental defects with no observable sexual and vegetative reproduction. Complementation analysis revealed a contribution of the conserved Y residue of MpSERK in growth. Proximity labelling-based interactomics of MpSERK identified MpBIR as an interactor. Mpbir disruptants displayed defects in reproductive organ development. Transcriptomes of Mpserk and Mpbir showed antagonistic patterns, suggesting MpBIR functions as a MpSERK repressor. We revealed that the pathogenic bacterium Pseudomonas syringae pv. tomato DC3000 could hardly grow on Mpbir, indicating a significant role of the MpSERK‒MpBIR module in immunity. Taken together, we propose that the SERK-BIR functional module was already established in the last common ancestor of land plants for regulating both development and immunity.

在模式被子植物拟南芥（Arabidopsis thaliana）中，体细胞胚胎发生受体样激酶（somatic embryogenesis receptor-like kinases, SERKs）作为富含亮氨酸重复序列受体样激酶（leucine-rich repeat receptor-like kinases, LRR-RLKs）的II亚家族，是包括油菜素甾醇不敏感1（BRASSINOSTEROID INSENSITIVE 1, BRI1）和鞭毛蛋白敏感2（FLAGELLIN SENSITIVE 2, FLS2）在内的多种LRR-RLK的共受体，在植物发育与免疫过程中发挥多样功能。拟南芥SERK3（AtSERK3）中保守的酪氨酸（Y）残基，在区分AtBRI1和AtFLS2介导的信号通路特异性方面发挥关键作用。BRI1关联受体激酶1（BRI ASSOCIATED RECEPTOR KINASE 1, BAK1）互作受体样激酶（BAK1-INTERACTING RECEPTOR-LIKE KINASES, BIRs）在静息状态下与SERKs发生互作，负调控SERK介导的信号通路。SERK与BIR在陆生植物中高度保守，而苔藓类支系中BRI1与FLS2同源物要么缺失，要么保守性极差。目前学界对非开花植物中SERK同源物的生物学功能所知甚少。模式植物地钱（Marchantia polymorpha）的基因组仅编码1个SERK与1个BIR同源物，分别为MpSERK与MpBIR。本研究证实，Mpserk敲除突变体表现出生长与发育缺陷，且无法观察到有性及无性繁殖现象。互补实验分析表明，MpSERK中保守的Y残基对植物生长具有重要贡献。基于邻近标记的MpSERK互作组学研究鉴定出MpBIR为其互作蛋白。Mpbir敲除突变体存在生殖器官发育缺陷。Mpserk与Mpbir的转录组呈现拮抗表达模式，提示MpBIR作为MpSERK的负调控因子发挥功能。研究发现，病原菌丁香假单胞菌番茄致病变种DC3000（Pseudomonas syringae pv. tomato DC3000）几乎无法在Mpbir突变体上增殖，表明MpSERK-MpBIR模块在植物免疫中发挥重要作用。综上，本研究提出SERK-BIR功能模块早在陆生植物的最后共同祖先中就已确立，用于协同调控植物发育与免疫。