A Brassica miRNA Regulates Plant Growth and Immunity through Distinct Modes of Action

First author: Chen Cui; Affiliations: CAS Institute of Microbiology (中科院微生物研究所): Beijing, China

Corresponding author: Cheng-Guo Duan

In plants, high disease resistance often results in a fitness penalty to plant growth. Therefore, breeding crops with a balanced yield and disease resistance has become a major challenge. Recently, microRNA (miRNA)-mediated R gene turnover has been shown to be a protective mechanism for plants to prevent autoimmunity in the absence of pathogens. However, whether these miRNAs play a role in plant growth and how miRNA-mediated R gene turnover responds to pathogen infection have been rarely explored. Here, we identified the Brassica miRNA, miR1885, targets both immune receptor gene and development-related gene for negative regulation through distinct modes of action. MiR1885 directly silences a TIR-NBS-LRR class of R gene BraTNL1 but represses the expression of photosynthesis-related gene BraCP24 through Trans-Acting Silencing (TAS) gene BraTIR1-mediated silencing. We found that, under natural conditions, miR1885 was kept in low levels to maintain normal development and basal immunity but peaked during the floral transition to promote flowering. Interestingly, upon Turnip mosaic virus (TuMV) infection, miR1885-dependent trans-acting silencing of BraCP24 was enhanced to speed up floral transition, whereas miR1885-mediated R gene turnover was overwhelmed by TuMV-induced BraTNL1 expression, reflecting an integrative regulation of the arms race between plants and pathogens. Collectively, our results demonstrate that a single Brassica miRNA dynamically regulates both innate immunity and plant growth and responds to viral infection, therefore demonstrating an integrative strategy for Brassica in modulating the interplay between growth, immunity and pathogen infection.

在植物中，疾病抗性强通常会牺牲植物生长的适应性。因此，目前农作物育种的一个主要挑战就是保证产量和疾病抗性的平衡。最近，miRNA介导的R基因表达转换是植物在没有病原菌的情况下预防自身免疫的保护机制。然而，这些miRNA在植物生长过程中是否发挥重要作用，以及miRNA介导的R基因转换如何响应于病原菌侵染等都不清楚。本文中，作者在芸苔属中鉴定到了一个miRNA，即miR1885，同时可以靶向免疫受体基因和发育相关基因，并且通过不同的作用模式负调控这些基因的表达。MiR1885能够直接沉默一个TIR-NBS-LRR类R基因BraTNL1，但需要通过反式作用沉默TAS基因BraTIR1介导的沉默来抑制光合作用相关基因BraCP24的表达。作者发现在自然条件下，miR1885的表达水平保持在较低的水平，以维持植株的正常发育和基础免疫；但在成花转变过程中达到峰值以促进植株开花。有趣的是，植株一旦遭受芜菁花叶病毒TuMV的侵染，依赖于miR1885的BraCP24基因的反式作用沉默被增强，从而加速成花转变，而TuMV诱导的BraTNL1基因表达会压制miR1885介导的R基因转换，反应了植物和病原菌之间相互竞争的综合调控。综上，本文的研究揭示了一个芸苔属miRNA能够动态调控天然免疫和植物生长，并且响应于病毒的侵染，因此，揭示了一个芸苔属植株中调控生长、免疫和病原菌侵染之间互作的综合策略。

通讯：段成国 (https://www.psc.ac.cn/research_vpersonal.asp?id=44)

个人简介：1997-2001年，山东农业大学，学士；2001-2004年，山东农业大学，硕士；2004-2008年，中科院微生物研究所，博士；2011-2016年，美国普渡大学，博士后。

研究方向：1. 表观遗传途径介导的基因表达与RNA加工机制及其对植物生长发育与抗逆的调控；2. 植物非生物逆境胁迫响应过程中表观遗传途径（包括DNA甲基化、非编码RNA与组蛋白修饰等内容）的调控机制及其应用；3. 植物-病原（生物逆境胁迫）互作的表观遗传调控机制及抗性育种；

doi: https://doi.org/10.1016/j.molp.2019.11.010

Journal: Molecular Plant

Published date: November 29, 2019