State Key Laboratory of Cotton Biology, Henan Key Laboratory of Plant Stress Biology, School of Life Sciences, School of Computer and Information Engineering, Henan University, Kaifeng 475001, China.
College of life science and agricultural engineering, Nanyang Normal University, Nanyang 473000, China.
Plant Physiol. 2022 May 3;189(1):264-284. doi: 10.1093/plphys/kiac041.
In plants, long noncoding RNAs (lncRNAs) regulate disease resistance against fungi and other pathogens. However, the specific mechanism behind this regulation remains unclear. In this study, we identified disease resistance-related lncRNAs as well as their regulating genes and assessed their functions by infection of cotton (Gossypium) chromosome segment substitution lines with Verticillium dahliae. Our results demonstrated that lncRNA7 and its regulating gene Pectin methylesterase inhibitor 13 (GbPMEI13) positively regulated disease resistance via the silencing approach, while ectopic overexpression of GbPMEI13 in Arabidopsis (Arabidopsis thaliana) promoted growth and enhanced resistance to V. dahliae. In contrast, lncRNA2 and its regulating gene Polygalacturonase 12 (GbPG12) negatively regulated resistance to V. dahliae. We further found that fungal disease-related agents, including the pectin-derived oligogalacturonide (OG), could downregulate the expression of lncRNA2 and GbPG12, leading to pectin accumulation. Conversely, OG upregulated the expression of lncRNA7, which encodes a plant peptide phytosulfokine (PSK-α), which was confirmed by lncRNA7 overexpression and Ultra Performance Liquid Chromatography Tandem Mass Spectrometry (UPLC-MS) experiments. We showed that PSK-α promoted 3-Indoleacetic acid (IAA) accumulation and activated GbPMEI13 expression through Auxin Response Factor 5. Since it is an inhibitor of pectin methylesterase (PME), GbPMEI13 promotes pectin methylation and therefore increases the resistance to V. dahliae. Consistently, we also demonstrated that GbPMEI13 inhibits the mycelial growth and spore germination of V. dahliae in vitro. In this study, we demonstrated that lncRNA7, lncRNA2, and their regulating genes modulate cell wall defense against V. dahliae via auxin-mediated signaling, providing a strategy for cotton breeding.
在植物中，长链非编码 RNA（lncRNA）调节对真菌和其他病原体的抗病性。然而，这种调节的具体机制尚不清楚。在这项研究中，我们鉴定了与疾病抗性相关的 lncRNA 及其调节基因，并通过感染棉花（Gossypium）染色体片段替代系Verticillium dahliae 来评估它们的功能。我们的结果表明，lncRNA7 及其调节基因果胶甲酯酶抑制剂 13（GbPMEI13）通过沉默途径正向调节抗病性，而在拟南芥（Arabidopsis thaliana）中异位过表达 GbPMEI13 促进了生长并增强了对 V. dahliae 的抗性。相比之下，lncRNA2 及其调节基因多聚半乳糖醛酸酶 12（GbPG12）负向调节对 V. dahliae 的抗性。我们还发现，真菌疾病相关物质，包括果胶衍生的寡聚半乳糖醛酸（OG），可以下调 lncRNA2 和 GbPG12 的表达，导致果胶积累。相反，OG 上调了 lncRNA7 的表达，该基因编码植物肽植物磺化肽（PSK-α），这通过 lncRNA7 过表达和超高效液相色谱串联质谱（UPLC-MS）实验得到证实。我们表明 PSK-α 通过生长素响应因子 5 促进 3-吲哚乙酸（IAA）积累并激活 GbPMEI13 表达。由于它是果胶甲酯酶（PME）的抑制剂，GbPMEI13 促进果胶甲基化，从而提高对 V. dahliae 的抗性。一致地，我们还证明 GbPMEI13 抑制 V. dahliae 在体外的菌丝生长和孢子萌发。在这项研究中，我们证明 lncRNA7、lncRNA2 及其调节基因通过生长素介导的信号转导调节细胞壁对 V. dahliae 的防御，为棉花育种提供了一种策略。
