NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi

NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi
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DOI:
10.1073/pnas.1719705115
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发表时间:
2018-03-06
影响因子:
11.1
通讯作者:
Glass, N. Louise
Glass, N. Louise
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Heller, Jens;Clave, Corinne;Glass, N. Louise

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在植物和后生动物中,属于NOD样受体(NLR)家族的细胞内受体是先天免疫的主要贡献者。丝状真菌基因组包含大量编码蛋白质的基因库,这些蛋白质具有与植物和动物NLR相似的结构,但功能大多未知。在这里,我们确定和分子特征patatin样磷脂酶-1(PLP-1),NLR样蛋白含有一个N-末端patatin样磷脂酶结构域,核苷酸结合结构域(NBD),和C末端tetratricopeptide repeat(TPR)结构域。PLP-1保护着必需的SNARE蛋白SEC-9; plp-1和sec-9的遗传差异在两种远亲真菌物种粗糙脉孢菌和鹅柄孢菌中起触发同种异体识别和细胞死亡的作用。脉孢菌种群样本的分析表明,plp-1和sec-9等位基因是高度多态性的,分离成离散的单倍型,并显示跨种多态性。在携带不相容的sec-9和PLP-1等位基因的细胞之间融合时,诱导同种异体识别和细胞死亡,这取决于SEC-9和PLP-1之间的物理相互作用。PLP-1的中心NBD和马铃薯糖蛋白样磷脂酶活性对于同种异体识别和细胞死亡是必不可少的,而SEC-9的TPR结构域和多态性SNARE结构域在赋予等位基因特异性中起作用。我们的数据表明,真菌NLR样蛋白的功能类似于植物和动物中的NLR免疫受体,表明NLR是植物和动物中先天免疫和真菌中同种异体识别的主要贡献者。
In plants and metazoans, intracellular receptors that belong to the NOD-like receptor (NLR) family are major contributors to innate immunity. Filamentous fungal genomes contain large repertoires of genes encoding for proteins with similar architecture to plant and animal NLRs with mostly unknown function. Here, we identify and molecularly characterize patatin-like phospholipase-1 (PLP-1), an NLR-like protein containing an N-terminal patatin-like phospholipase domain, a nucleotide-binding domain (NBD), and a Cterminal tetratricopeptide repeat (TPR) domain. PLP-1 guards the essential SNARE protein SEC-9; genetic differences at plp-1 and sec-9 function to trigger allorecognition and cell death in two distantly related fungal species, Neurospora crassa and Podospora anserina. Analyses of Neurospora population samples revealed that plp-1 and sec-9 alleles are highly polymorphic, segregate into discrete haplotypes,and show transspecies polymorphism. Upon fusion between cells bearing incompatible sec-9 and plp-1 alleles, allorecognition and cell death are induced, which are dependent upon physical interaction between SEC-9 and PLP-1. The central NBD and patatin-like phospholipase activity of PLP-1 are essential for allorecognition and cell death, while the TPR domain and the polymorphic SNARE domain of SEC-9 function in conferring allelic specificity. Our data indicate that fungal NLR-like proteins function similar to NLR immune receptors in plants and animals, showing that NLRs are major contributors to innate immunity in plants and animals and for allorecognition in fungi.