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The N-terminal domains of NLR immune receptors exhibit structural and functional similarities across divergent plant lineages
The Plant Cell ( IF 11.6 ) Pub Date : 2024-04-10 , DOI: 10.1093/plcell/koae113
Khong-Sam Chia 1 , Jiorgos Kourelis 2 , Albin Teulet 3 , Martin Vickers 4 , Toshiyuki Sakai 2 , Joseph F Walker 5 , Sebastian Schornack 3 , Sophien Kamoun 2 , Philip Carella 1
Affiliation  

Nucleotide-binding domain and leucine-rich repeat (NLR) proteins are a prominent class of intracellular immune receptors in plants. However, our understanding of plant NLR structure and function is limited to the evolutionarily young flowering plant clade. Here, we describe an extended spectrum of NLR diversity across divergent plant lineages and demonstrate the structural and functional similarities of N-terminal domains that trigger immune responses. We show that the broadly distributed coiled-coil (CC) and toll/interleukin-1 receptor (TIR) domain families of non-flowering plants retain immune-related functions through trans-lineage activation of cell death in the angiosperm Nicotiana benthamiana. We further examined a CC subfamily specific to non-flowering lineages and uncovered an essential N-terminal MAEPL motif that is functionally comparable to motifs in resistosome-forming CC-NLRs. Consistent with a conserved role in immunity, the ectopic activation of CCMAEPL in the non-flowering liverwort Marchantia polymorpha led to profound growth inhibition, defense gene activation, and signatures of cell death. Moreover, comparative transcriptomic analyses of CCMAEPL activity delineated a common CC-mediated immune program shared across evolutionarily divergent non-flowering and flowering plants. Collectively, our findings highlight the ancestral nature of NLR-mediated immunity during plant evolution that dates its origin to at least ∼500 million years ago.

中文翻译:

NLR 免疫受体的 N 端结构域在不同植物谱系中表现出结构和功能相似性

核苷酸结合域和富含亮氨酸重复序列 (NLR) 蛋白是植物中一类重要的细胞内免疫受体。然而,我们对植物 NLR 结构和功能的理解仅限于进化上年轻的开花植物进化枝。在这里,我们描述了不同植物谱系中 NLR 多样性的扩展谱,并证明了触发免疫反应的 N 端结构域的结构和功能相似性。我们发现,非开花植物中广泛分布的卷曲螺旋(CC)和Toll/白细胞介素-1受体(TIR)结构域家族通过被子植物本塞姆氏烟草中细胞死亡的跨谱系激活而保留了免疫相关功能。我们进一步检查了非开花谱系特有的 CC 亚家族,并发现了一个重要的 N 末端 MAEPL 基序,该基序在功能上与形成抗性体的 CC-NLR 中的基序相当。与免疫中的保守作用一致,不开花地钱地钱中 CCMAEPL 的异位激活导致了严重的生长抑制、防御基因激活和细胞死亡特征。此外,CCMAEPL 活性的比较转录组分析描绘了进化上不同的非开花和开花植物所共有的共同 CC 介导的免疫程序。总的来说,我们的研究结果强调了植物进化过程中 NLR 介导的免疫的祖先性质,其起源至少可追溯到约 5 亿年前。
更新日期:2024-04-10
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