NRC3 的次功能化改变了烟草 NRC 网络的遗传结构

IF 4.5 2区 生物学 Q1 Agricultural and Biological Sciences PLoS Genetics Pub Date : 2024-09-12 DOI:10.1371/journal.pgen.1011402
Ching-Yi Huang, Yu-Seng Huang, Yu Sugihara, Hung-Yu Wang, Lo-Ting Huang, Juan Carlos Lopez-Agudelo, Yi-Feng Chen, Kuan-Yu Lin, Bing-Jen Chiang, AmirAli Toghani, Jiorgos Kourelis, Chun-Hsiung Wang, Lida Derevnina, Chih-Hang Wu
{"title":"NRC3 的次功能化改变了烟草 NRC 网络的遗传结构","authors":"Ching-Yi Huang, Yu-Seng Huang, Yu Sugihara, Hung-Yu Wang, Lo-Ting Huang, Juan Carlos Lopez-Agudelo, Yi-Feng Chen, Kuan-Yu Lin, Bing-Jen Chiang, AmirAli Toghani, Jiorgos Kourelis, Chun-Hsiung Wang, Lida Derevnina, Chih-Hang Wu","doi":"10.1371/journal.pgen.1011402","DOIUrl":null,"url":null,"abstract":"Nucleotide-binding domain and leucine-rich repeat (NLR) proteins play crucial roles in immunity against pathogens in both animals and plants. In solanaceous plants, activation of several sensor NLRs triggers their helper NLRs, known as NLR-required for cell death (NRC), to form resistosome complexes to initiate immune responses. While the sensor NLRs and downstream NRC helpers display diverse genetic compatibility, molecular evolutionary events leading to the complex network architecture remained elusive. Here, we showed that solanaceous NRC3 variants underwent subfunctionalization after the divergence of <jats:italic>Solanum</jats:italic> and <jats:italic>Nicotiana</jats:italic>, altering the genetic architecture of the NRC network in <jats:italic>Nicotiana</jats:italic>. Natural solanaceous NRC3 variants form three allelic groups displaying distinct compatibilities with the sensor NLR Rpi-blb2. Ancestral sequence reconstruction and analyses of natural and chimeric variants identified six key amino acids involved in sensor-helper compatibility. These residues are positioned on multiple surfaces of the resting NRC3 homodimer, collectively contributing to their compatibility with Rpi-blb2. Upon activation, Rpi-blb2-compatible NRC3 variants form membrane-associated punctate and high molecular weight complexes, and confer resistance to the late blight pathogen <jats:italic>Phytophthora infestans</jats:italic>. Our findings revealed how mutations in NRC alleles lead to subfunctionalization, altering sensor-helper compatibility and contributing to the increased complexity of the NRC network.","PeriodicalId":20266,"journal":{"name":"PLoS Genetics","volume":null,"pages":null},"PeriodicalIF":4.5000,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Subfunctionalization of NRC3 altered the genetic structure of the Nicotiana NRC network\",\"authors\":\"Ching-Yi Huang, Yu-Seng Huang, Yu Sugihara, Hung-Yu Wang, Lo-Ting Huang, Juan Carlos Lopez-Agudelo, Yi-Feng Chen, Kuan-Yu Lin, Bing-Jen Chiang, AmirAli Toghani, Jiorgos Kourelis, Chun-Hsiung Wang, Lida Derevnina, Chih-Hang Wu\",\"doi\":\"10.1371/journal.pgen.1011402\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"Nucleotide-binding domain and leucine-rich repeat (NLR) proteins play crucial roles in immunity against pathogens in both animals and plants. In solanaceous plants, activation of several sensor NLRs triggers their helper NLRs, known as NLR-required for cell death (NRC), to form resistosome complexes to initiate immune responses. While the sensor NLRs and downstream NRC helpers display diverse genetic compatibility, molecular evolutionary events leading to the complex network architecture remained elusive. Here, we showed that solanaceous NRC3 variants underwent subfunctionalization after the divergence of <jats:italic>Solanum</jats:italic> and <jats:italic>Nicotiana</jats:italic>, altering the genetic architecture of the NRC network in <jats:italic>Nicotiana</jats:italic>. Natural solanaceous NRC3 variants form three allelic groups displaying distinct compatibilities with the sensor NLR Rpi-blb2. Ancestral sequence reconstruction and analyses of natural and chimeric variants identified six key amino acids involved in sensor-helper compatibility. These residues are positioned on multiple surfaces of the resting NRC3 homodimer, collectively contributing to their compatibility with Rpi-blb2. Upon activation, Rpi-blb2-compatible NRC3 variants form membrane-associated punctate and high molecular weight complexes, and confer resistance to the late blight pathogen <jats:italic>Phytophthora infestans</jats:italic>. Our findings revealed how mutations in NRC alleles lead to subfunctionalization, altering sensor-helper compatibility and contributing to the increased complexity of the NRC network.\",\"PeriodicalId\":20266,\"journal\":{\"name\":\"PLoS Genetics\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":4.5000,\"publicationDate\":\"2024-09-12\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"PLoS Genetics\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1371/journal.pgen.1011402\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"Agricultural and Biological Sciences\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Genetics","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1371/journal.pgen.1011402","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Agricultural and Biological Sciences","Score":null,"Total":0}
引用次数: 0

摘要

核苷酸结合域和富亮氨酸重复(NLR)蛋白在动物和植物对抗病原体的免疫中发挥着至关重要的作用。在茄科植物中,几种传感器 NLR 的激活会触发它们的辅助 NLR(即细胞死亡所需的 NLR(NRC)),形成抗原体复合物,启动免疫反应。虽然传感器 NLRs 和下游 NRC 辅助器显示出不同的遗传兼容性,但导致复杂网络结构的分子进化事件仍然难以捉摸。在这里,我们发现茄科植物的 NRC3 变体在茄科植物和烟草植物分化后经历了亚功能化,改变了烟草植物 NRC 网络的遗传结构。天然茄科植物 NRC3 变体形成了三个等位基因群,与传感器 NLR Rpi-blb2 具有不同的兼容性。通过对天然变体和嵌合变体的祖先序列重建和分析,确定了涉及传感器-助手兼容性的六个关键氨基酸。这些残基位于静止的 NRC3 同源二聚体的多个表面,共同促成了它们与 Rpi-blb2 的兼容性。激活后,与 Rpi-blb2 兼容的 NRC3 变体会形成与膜相关的点状高分子量复合物,并对晚疫病病原体 Phytophthora infestans 产生抗性。我们的研究结果揭示了 NRC 等位基因的突变是如何导致亚功能化、改变传感器-助手的兼容性并增加 NRC 网络的复杂性的。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
Subfunctionalization of NRC3 altered the genetic structure of the Nicotiana NRC network
Nucleotide-binding domain and leucine-rich repeat (NLR) proteins play crucial roles in immunity against pathogens in both animals and plants. In solanaceous plants, activation of several sensor NLRs triggers their helper NLRs, known as NLR-required for cell death (NRC), to form resistosome complexes to initiate immune responses. While the sensor NLRs and downstream NRC helpers display diverse genetic compatibility, molecular evolutionary events leading to the complex network architecture remained elusive. Here, we showed that solanaceous NRC3 variants underwent subfunctionalization after the divergence of Solanum and Nicotiana, altering the genetic architecture of the NRC network in Nicotiana. Natural solanaceous NRC3 variants form three allelic groups displaying distinct compatibilities with the sensor NLR Rpi-blb2. Ancestral sequence reconstruction and analyses of natural and chimeric variants identified six key amino acids involved in sensor-helper compatibility. These residues are positioned on multiple surfaces of the resting NRC3 homodimer, collectively contributing to their compatibility with Rpi-blb2. Upon activation, Rpi-blb2-compatible NRC3 variants form membrane-associated punctate and high molecular weight complexes, and confer resistance to the late blight pathogen Phytophthora infestans. Our findings revealed how mutations in NRC alleles lead to subfunctionalization, altering sensor-helper compatibility and contributing to the increased complexity of the NRC network.
求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
PLoS Genetics
PLoS Genetics 生物-遗传学
CiteScore
8.10
自引率
2.20%
发文量
438
审稿时长
1 months
期刊介绍: PLOS Genetics is run by an international Editorial Board, headed by the Editors-in-Chief, Greg Barsh (HudsonAlpha Institute of Biotechnology, and Stanford University School of Medicine) and Greg Copenhaver (The University of North Carolina at Chapel Hill). Articles published in PLOS Genetics are archived in PubMed Central and cited in PubMed.
期刊最新文献
Subfunctionalization of NRC3 altered the genetic structure of the Nicotiana NRC network The transcription factor RUNT-like regulates pupal cuticle development via promoting a pupal cuticle protein transcription Direct targets of MEF2C are enriched for genes associated with schizophrenia and cognitive function and are involved in neuron development and mitochondrial function Evolutionary rate covariation is pervasive between glycosylation pathways and points to potential disease modifiers Histone variant H2A.Z is needed for efficient transcription-coupled NER and genome integrity in UV challenged yeast cells
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1