An atypical NLR protein modulates the NRC immune receptor network in Nicotiana benthamiana.
An atypical NLR protein modulates the NRC immune receptor network in Nicotiana benthamiana.
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DOI：
10.1371/journal.pgen.1010500
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发表时间：
2023-01
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影响因子：
4.5
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中科院分区：
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在asterid植物中，NRC免疫受体网络已经从一对连接的基因进化为一个由传感器和辅助NLR（核苷酸结合结构域和富含亮氨酸的重复序列）蛋白组成的遗传分散和系统发育结构网络。在一些物种中，如模式植物烟叶（Nicotiana benthamiana）和其他茄科植物，NRC （NLR-REQUIRED FOR CELL DEATH）网络形成了多达一半的NLRome， NRC以不同复杂性的基因簇分布在整个基因组中。在这里，我们描述了NRCX，一个NRC家族的非典型成员，缺乏这些NLR辅助蛋白的典型特征，如功能性n端MADA基序和触发自身免疫的能力。与其他NRCs相比，benthamiana NRCX的系统基因沉默显著损害植物生长，导致矮化表型。值得注意的是，NRCX沉默植物的侏儒症部分依赖于NRCX的类似物NRC2和NRC3，而不是NRC4。尽管系统沉默NRCX会对植物生长产生负面影响，但在benthamiana成熟叶片中，NRCX的位点基因沉默不会导致可见的细胞死亡表型。然而，NRCX表达的改变调节了NRC2和NRC3介导的超敏反应，其方式与NRCX在NRC网络中的负作用一致。我们得出结论，NRCX是NRC网络的一个非典型成员，它已经进化到有助于这个基因不相关的NLR网络的稳态。植物有一个有效的免疫系统来对抗各种病原体，如真菌、卵菌、细菌、病毒、线虫和昆虫。在免疫系统的第一层，受体蛋白检测病原体并激活防御反应。植物基因组编码非常庞大和多样化的免疫受体，其中一些是成对的或作为复杂的受体网络起作用。然而，免疫系统对植物来说是有代价的，不适当的受体激活会导致生长抑制和自身免疫。在这里，我们展示了一个非典型的免疫受体基因作为免疫受体网络的调节剂的功能。这种受体基因的进化是为了维持免疫系统的稳态，平衡生长和免疫之间的健康权衡。进一步了解植物如何调节其免疫受体系统，将有助于培育出适应性损失有限的抗病作物。
The NRC immune receptor network has evolved in asterid plants from a pair of linked genes into a genetically dispersed and phylogenetically structured network of sensor and helper NLR (nucleotide-binding domain and leucine-rich repeat-containing) proteins. In some species, such as the model plant Nicotiana benthamiana and other Solanaceae, the NRC (NLR-REQUIRED FOR CELL DEATH) network forms up to half of the NLRome, and NRCs are scattered throughout the genome in gene clusters of varying complexities. Here, we describe NRCX, an atypical member of the NRC family that lacks canonical features of these NLR helper proteins, such as a functional N-terminal MADA motif and the capacity to trigger autoimmunity. In contrast to other NRCs, systemic gene silencing of NRCX in N. benthamiana markedly impairs plant growth resulting in a dwarf phenotype. Remarkably, dwarfism of NRCX silenced plants is partially dependent on NRCX paralogs NRC2 and NRC3, but not NRC4. Despite its negative impact on plant growth when silenced systemically, spot gene silencing of NRCX in mature N. benthamiana leaves doesn’t result in visible cell death phenotypes. However, alteration of NRCX expression modulates the hypersensitive response mediated by NRC2 and NRC3 in a manner consistent with a negative role for NRCX in the NRC network. We conclude that NRCX is an atypical member of the NRC network that has evolved to contribute to the homeostasis of this genetically unlinked NLR network. Plants have an effective immune system to fight off diverse pathogens such as fungi, oomycetes, bacteria, viruses, nematodes and insects. In the first layer of their immune system, receptor proteins act to detect pathogens and activate the defense response. Plant genomes encode very large and diverse repertoires of immune receptors, some of which function in pairs or as complex receptor networks. However, the immune system can come at a cost for plants and inappropriate receptor activation results in growth suppression and autoimmunity. Here, we show that an atypical immune receptor gene functions as a modulator of the immune receptor network. This type of receptor gene evolved to maintain homeostasis of the immune system and balance fitness trade-offs between growth and immunity. Further understanding how plants regulate their immune receptor system should help guide breeding disease resistant crops with limited fitness penalties.
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