National Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research (Wuhan), Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China.
Plant Physiol. 2023 Jul 3;192(3):2537-2553. doi: 10.1093/plphys/kiad201.
Rice (Oryza sativa L.) microRNA156/529-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE7/14/17 (miR156/529-SPL7/14/17) modules have pleiotropic effects on many biological pathways. OsSPL7/14 can interact with DELLA protein SLENDER RICE1 (SLR1) to modulate gibberellin acid (GA) signal transduction against the bacterial pathogen Xanthomonas oryzae pv. oryzae. However, whether the miR156/529-OsSPL7/14/17 modules also regulate resistance against other pathogens is unclear. Notably, OsSPL7/14/17 functioning as transcriptional activators, their target genes, and the corresponding downstream signaling pathways remain largely unexplored. Here, we demonstrate that miR156/529 play negative roles in plant immunity and that miR156/529-regulated OsSPL7/14/17 confer broad-spectrum resistance against 2 devastating bacterial pathogens. Three OsSPL7/14/17 proteins directly bind to the promoters of rice Allene Oxide Synthase 2 (OsAOS2) and NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (OsNPR1) and activate their transcription, regulating jasmonic acid (JA) accumulation and the salicylic acid (SA) signaling pathway, respectively. Overexpression of OsAOS2 or OsNPR1 impairs the susceptibility of the osspl7/14/17 triple mutant. Exogenous application of JA enhances resistance of the osspl7/14/17 triple mutant and the miR156 overexpressing plants. In addition, genetic evidence confirms that bacterial pathogen-activated miR156/529 negatively regulate pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) responses, such as pattern recognition receptor Xa3/Xa26-initiated PTI. Our findings demonstrate that bacterial pathogens modulate miR156/529-OsSPL7/14/17 modules to suppress OsAOS2-catalyzed JA accumulation and the OsNPR1-promoted SA signaling pathway, facilitating pathogen infection. The uncovered miR156/529-OsSPL7/14/17-OsAOS2/OsNPR1 regulatory network provides a potential strategy to genetically improve rice disease resistance.
水稻(Oryza sativa L.)microRNA156/529-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE7/14/17(miR156/529-SPL7/14/17)模块对许多生物途径具有多效性。OsSPL7/14 可以与赤霉素酸(GA)信号转导的 DELLA 蛋白 SLENDER RICE1(SLR1)相互作用,以调节对细菌病原体稻黄单胞菌 pv.oryzae 的抗性。然而,miR156/529-OsSPL7/14/17 模块是否也调节对其他病原体的抗性尚不清楚。值得注意的是,OsSPL7/14/17 作为转录激活因子,其靶基因和相应的下游信号通路仍在很大程度上未被探索。在这里,我们证明 miR156/529 在植物免疫中起负作用,并且 miR156/529 调节的 OsSPL7/14/17 赋予对 2 种破坏性细菌病原体的广谱抗性。三种 OsSPL7/14/17 蛋白直接与水稻丙二烯氧化物合酶 2(OsAOS2)和非致病相关基因 1(OsNPR1)的启动子结合,并激活它们的转录,分别调节茉莉酸(JA)的积累和水杨酸(SA)信号通路。OsAOS2 或 OsNPR1 的过表达会损害 osspl7/14/17 三重突变体的易感性。JA 的外源应用增强了 osspl7/14/17 三重突变体和 miR156 过表达植物的抗性。此外,遗传证据证实,细菌病原体可调节 miR156/529 来负调控病原体相关分子模式(PAMP)触发的免疫(PTI)反应,例如模式识别受体 Xa3/Xa26 引发的 PTI。我们的研究结果表明,细菌病原体可调节 miR156/529-OsSPL7/14/17 模块来抑制 OsAOS2 催化的 JA 积累和 OsNPR1 促进的 SA 信号通路,从而促进病原体感染。所揭示的 miR156/529-OsSPL7/14/17-OsAOS2/OsNPR1 调控网络为通过遗传改良水稻抗病性提供了一种潜在策略。