Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Curr Biol. 2019 Sep 23;29(18):3006-3017.e3. doi: 10.1016/j.cub.2019.07.060. Epub 2019 Aug 29.
Somatic cell fusion and conspecific cooperation are crucial social traits for microbial unicellular-to-multicellular transitions, colony expansion, and substrate foraging but are also associated with risks of parasitism. We identified a cell wall remodeling (cwr) checkpoint that acts upon cell contact to assess genetic compatibility and regulate cell wall dissolution during somatic cell fusion in a wild population of the filamentous fungus Neurospora crassa. Non-allelic interactions between two linked loci, cwr-1 and cwr-2, were necessary and sufficient to block cell fusion: cwr-1 encodes a polysaccharide monooxygenase (PMO), a class of enzymes associated with extracellular degradative capacities, and cwr-2 encodes a predicted transmembrane protein. Mutations of sites in CWR-1 essential for PMO catalytic activity abolished the block in cell fusion between formerly incompatible strains. In Neurospora, alleles cwr-1 and cwr-2 were highly polymorphic, fell into distinct haplogroups, and showed trans-species polymorphisms. Distinct haplogroups and trans-species polymorphisms at cwr-1 and cwr-2 were also identified in the distantly related genus Fusarium, suggesting convergent evolution. Proteins involved in chemotropic processes showed extended localization at contact sites, suggesting that cwr regulates the transition between chemotropic growth and cell wall dissolution. Our work revealed an allorecognition surveillance system based on kind discrimination that inhibits cooperative behavior in fungi by blocking cell fusion upon contact, contributing to fungal immunity by preventing formation of chimeras between genetically non-identical colonies.
体细胞融合和同物种合作是微生物从单细胞到多细胞转变、菌落扩张和基质觅食的关键社会特征，但也与寄生风险有关。我们鉴定了一个细胞壁重塑 (cwr) 检查点，它在细胞接触时起作用，以评估遗传相容性并调节体细胞融合过程中的细胞壁溶解，这是在丝状真菌粗糙脉孢菌的野生种群中发现的。两个连锁基因座 cwr-1 和 cwr-2 之间的非等位基因相互作用是阻止细胞融合所必需且充分的：cwr-1 编码多糖单加氧酶 (PMO)，这是一类与细胞外降解能力相关的酶，而 cwr-2 编码一个预测的跨膜蛋白。CWR-1 中对 PMO 催化活性至关重要的位点突变消除了以前不兼容菌株之间细胞融合的阻断。在粗糙脉孢菌中，cwr-1 和 cwr-2 等位基因高度多态性，分为不同的单倍型群，表现出跨物种多态性。在亲缘关系较远的镰刀菌属中，也鉴定到了 cwr-1 和 cwr-2 的不同单倍型群和跨物种多态性，表明存在趋同进化。参与趋化过程的蛋白质在接触部位表现出扩展的定位，表明 cwr 通过在接触时阻止细胞融合来调节从趋化生长到细胞壁溶解的转变。我们的工作揭示了一种基于种类识别的异体识别监测系统，该系统通过在接触时阻止细胞融合来抑制真菌的合作行为，通过防止遗传上不同的菌落之间形成嵌合体，为真菌免疫做出贡献。
