Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network.

Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network.
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DOI:
10.1371/journal.pbio.3001136
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发表时间:
2021-08
期刊:
影响因子:
9.8
通讯作者:
Kamoun S
Kamoun S
中科院分区:
生物学1区
文献类型:
--
作者:
Derevnina L;Contreras MP;Adachi H;Upson J;Vergara Cruces A;Xie R;Skłenar J;Menke FLH;Mugford ST;MacLean D;Ma W;Hogenhout SA;Goverse A;Maqbool A;Wu CH;Kamoun S

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在植物中,含有核苷酸结合域和富含亮氨酸重复序列(NLR)的蛋白质可以形成受体网络,赋予过敏性细胞死亡和先天免疫。一类NLR,称为细胞死亡所需的NLR(NRC),是一个复杂网络中的中心节点,可以抵御多种病原体,并包括茄科植物NLR的一半。鉴于这种NLR网络的普遍性,我们假设病原体收敛地进化为分泌靶向NRC活性的效应子。为了测试这一点,我们筛选了165个细菌、卵菌、线虫和蚜虫效应子的文库,以确定它们抑制由NRC依赖性抗病蛋白Prf和Rpi-blb 2引发的细胞死亡反应的能力。在5个已鉴定的抑制因子中,1个孢囊线虫蛋白和1个卵菌蛋白抑制NRC 2和NRC 3的自身免疫突变体的活性,但不抑制NRC 4,表明它们特异性地抵消NRC蛋白的一个子集,独立于它们的传感器NLR伙伴。尽管孢囊线虫效应子SPRYSEC 15结合NRC 2和NRC 3的核苷酸结合结构域,但卵菌效应子AVRcap 1b通过膜运输相关蛋白NbTOL 9a(Myb 1样蛋白9a的靶点)抑制这些NRC的反应。我们的结论是,植物病原体已经进化到通过不同的机制来抵消NRC免疫受体网络的中心节点。与病原体效应子的协同进化可能驱动了NRC多样化,使其在大规模扩展的NLR网络中成为功能冗余的节点。植物病原体已经进化到抵消其宿主的免疫系统。筛选抑制烟草中传感器NLR介导的细胞死亡的病原体效应物,鉴定来自孢囊线虫和卵菌的抑制免疫网络的NRC分支以抑制免疫相关的细胞死亡应答的效应物。
In plants, nucleotide-binding domain and leucine-rich repeat (NLR)-containing proteins can form receptor networks to confer hypersensitive cell death and innate immunity. One class of NLRs, known as NLR required for cell death (NRCs), are central nodes in a complex network that protects against multiple pathogens and comprises up to half of the NLRome of solanaceous plants. Given the prevalence of this NLR network, we hypothesised that pathogens convergently evolved to secrete effectors that target NRC activities. To test this, we screened a library of 165 bacterial, oomycete, nematode, and aphid effectors for their capacity to suppress the cell death response triggered by the NRC-dependent disease resistance proteins Prf and Rpi-blb2. Among 5 of the identified suppressors, 1 cyst nematode protein and 1 oomycete protein suppress the activity of autoimmune mutants of NRC2 and NRC3, but not NRC4, indicating that they specifically counteract a subset of NRC proteins independently of their sensor NLR partners. Whereas the cyst nematode effector SPRYSEC15 binds the nucleotide-binding domain of NRC2 and NRC3, the oomycete effector AVRcap1b suppresses the response of these NRCs via the membrane trafficking-associated protein NbTOL9a (Target of Myb 1-like protein 9a). We conclude that plant pathogens have evolved to counteract central nodes of the NRC immune receptor network through different mechanisms. Coevolution with pathogen effectors may have driven NRC diversification into functionally redundant nodes in a massively expanded NLR network. Plant pathogens have evolved to counteract their hosts’ immune systems. A screen for pathogen effectors that suppress sensor NLR-mediated cell death in tobacco identifies effectors from a cyst nematode and an oomycete that suppress the NRC branch of the immune network to inhibit the immune-related cell death response.
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