Allorecognition upon Fungal Cell-Cell Contact Determines Social Cooperation and Impacts the Acquisition of Multicellularity
Allorecognition upon Fungal Cell-Cell Contact Determines Social Cooperation and Impacts the Acquisition of Multicellularity
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DOI：
10.1016/j.cub.2019.07.060
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发表时间：
2019-09-23
期刊：
影响因子：
9.2
通讯作者：
Glass, N. Louise
中科院分区：
文献类型：
--
作者：
Goncalves, A. Pedro;Heller, Jens;Glass, N. Louise
体细胞融合和同种协作是微生物从单细胞到多细胞转变、菌落扩张和底物觅食的关键社会特征，但也与寄生风险有关。我们确定了一个细胞壁重塑(CWR)检查点，该检查点作用于细胞接触，以评估遗传亲和性，并在丝状真菌粗面脉孢子菌野生种群的体细胞融合过程中调节细胞壁溶解。Cwr-1和cwr-2这两个连锁基因座之间的非等位基因相互作用是阻止细胞融合的必要条件和充分条件：cwr-1编码一种与细胞外降解能力相关的多糖单加氧酶(PMO)，而cwr-2编码一种预测的跨膜蛋白。CWR-1中对PMO催化活性至关重要的位点的突变消除了以前不相容的菌株之间细胞融合的障碍。在脉孢菌中，等位基因cwr-1和cwr-2具有较高的多态性，可分为不同的单倍群，并表现出跨种间的多态。在远缘镰刀菌属中也发现了cwr-1和cwr-2的不同单倍群和跨物种多态，这表明进化趋同。参与趋化过程的蛋白质在接触部位显示了广泛的定位，这表明cwr调节着趋化生长和细胞壁溶解之间的转换。我们的工作揭示了一种基于种类歧视的同种异体识别监测系统，该系统通过阻止细胞接触时的融合来抑制真菌中的合作行为，通过防止基因上不同的菌落之间形成嵌合体来促进真菌免疫。
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. Nonallelic 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 transspecies 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.