Pathogen-Associated Molecular Pattern-Triggered Immunity Involves Proteolytic Degradation of Core Nonsense-Mediated mRNA Decay Factors During the Early Defense Response

9.618Q1       

Plant Cell

2020 Apr;32(4):1081-1101.

doi: 10.1105/tpc.19.00631. Epub 2020 Feb 21.

Ho Won Jung 1, Gagan Kumar Panigrahi 2 3 4, Ga Young Jung 1, Yu Jeong Lee 1, Ki Hun Shin 2 3, Annapurna Sahoo 2 3, Eun Su Choi 1, Eunji Lee 1, Kyung Man Kim 2 3, Seung Hwan Yang 5, Jong-Seong Jeon 6, Sung Chul Lee 7, Sang Hyon Kim 8

一作单位： 东亚大学应用生物科学系，韩国釜山(Department of Applied Bioscience, Dong-A University, Busan 49315, Korea)

Abstract

        Nonsense-mediated mRNA decay (NMD), an mRNA quality control process, is thought to function in plant immunity. A subset of fully spliced (FS) transcripts of Arabidopsis (Arabidopsis thaliana) resistance (R) genes are upregulated during bacterial infection. Here, we report that 81.2% and 65.1% of FS natural TIR-NBS-LRR (TNL) and CC-NBS-LRR transcripts, respectively, retain characteristics of NMD regulation, as their transcript levels could be controlled posttranscriptionally. Both bacterial infection and the perception of bacteria by pattern recognition receptors initiated the destruction of core NMD factors UP-FRAMESHIFT1 (UPF1), UPF2, and UPF3 in Arabidopsis within 30 min of inoculation via the independent ubiquitination of UPF1 and UPF3 and their degradation via the 26S proteasome pathway. The induction of UPF1 and UPF3 ubiquitination was delayed in mitogen-activated protein kinase3 (mpk3) and mpk6, but not in salicylic acid-signaling mutants, during the early immune response. Finally, previously uncharacterized TNL-type R transcripts accumulated in upf mutants and conferred disease resistance to infection with a virulent Pseudomonas strain in plants. Our findings demonstrate that NMD is one of the main regulatory processes through which PRRs fine-tune R transcript levels to reduce fitness costs and achieve effective immunity.

摘要

        无意义介导的mRNA衰变（NMD），一种mRNA质量控制过程，被认为在植物免疫中起作用。拟南芥抗性的完整剪接（FS）转录物的抗性（R）基因在细菌感染过程中被上调。在这里，我们报告说，FS天然TIR-NBS-LRR（TNL）和CC-NBS-LRR转录本的81.2％和65.1％保留了NMD调节的特征，因为它们的转录本水平可以在转录后进行控制。细菌感染和模式识别受体对细菌的感知都会在接种后30分钟内通过UPF1和UPF3的独立泛素化并通过降解来降解拟南芥中核心NMD因子UP-FRAMESHIFT1（UPF1），UPF2和UPF3。 26S蛋白酶体途径。UPF1和UPF3泛素化的诱导在被延迟有丝分裂原-活化蛋白激酶3（MPK3）和MPK6，但不是在早期免疫反应中出现在水杨酸信号突变体中。最后，先前未表征的TNL型R转录物积累在upf突变体中，并赋予了植物抵抗强毒假单胞菌菌株感染的抗病能力。我们的发现表明，NMD是PRR通过微调R转录水平以降低适应性成本并获得有效免疫力的主要调控过程之一。

** Sang Hyon Kim **

韩国明知大学教授Myongji University