Cao Liwen, Chen Yao, Xiao Kai, Chen Liang
State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, China.
University of Chinese Academy of Science, Beijing, 100049, China.
J Integr Plant Biol. 2025 Apr;67(4):1009-1027. doi: 10.1111/jipb.13897. Epub 2025 Mar 28.
Leaf senescence can be triggered by various abiotic stresses. Among these, heat stress emerges as a pivotal environmental factor, particularly in light of the predicted rise in global temperatures. However, the molecular mechanism underlying heat-induced leaf senescence remains largely unexplored. As a cool-season grass species, tall fescue (Festuca arundinacea) is an ideal and imperative material for investigating heat-induced leaf senescence because heat stress easily triggers leaf senescence to influence its forage yield and turf quality. Here, we investigated the role of FaNAC047 in heat-induced leaf senescence. Overexpression of FaNAC047 promoted heat-induced leaf senescence in transgenic tall fescue that was evidenced by a more seriously destructive photosystem and higher accumulation of reactive oxygen species (ROS), whereas knockdown of FaNAC047 delayed leaf senescence. Further protein-DNA interaction assays indicated that FaNAC047 directly activated the transcriptions of NON-YELLOW COLORING 1 (FaNYC1), NYC1-like (FaNOL), and STAY-GREEN (FaSGR) but directly inhibited Catalases 2 (FaCAT2) expression, thereby promoting chlorophyll degradation and ROS accumulation. Subsequently, protein-protein interaction assays revealed that FaNAC047 physically interacted with FaNAC058 to enhance its regulatory effect on FaNYC1, FaNOL, FaSGR, and FaCAT2. Additionally, FaNAC047 could transcriptionally activate FaNAC058 expression to form a regulatory cascade, driving senescence progression. Consistently, the knockdown of FaNAC058 significantly delayed heat-induced leaf senescence. Collectively, our results reveal that FaNAC047-FaNAC058 module coordinately mediates chlorophyll degradation and ROS production to positively regulate heat-induced leaf senescence. The findings illustrate the molecular network of heat-induced leaf senescence for breeding heat-resistant plants.
叶片衰老可由多种非生物胁迫触发。其中，热胁迫成为一个关键的环境因素，尤其是考虑到全球气温预计会上升。然而，热诱导叶片衰老的分子机制在很大程度上仍未被探索。作为一种冷季型禾本科植物，高羊茅（Festuca arundinacea）是研究热诱导叶片衰老的理想且必要的材料，因为热胁迫容易触发叶片衰老，从而影响其牧草产量和草坪质量。在此，我们研究了FaNAC047在热诱导叶片衰老中的作用。FaNAC047的过表达促进了转基因高羊茅中热诱导的叶片衰老，这通过更严重受损的光合系统和更高的活性氧（ROS）积累得以证明，而FaNAC047的敲低则延迟了叶片衰老。进一步的蛋白质 - DNA相互作用分析表明，FaNAC047直接激活了非黄化1（FaNYC1）、NYC1样（FaNOL）和保持绿色（FaSGR）的转录，但直接抑制过氧化氢酶2（FaCAT2）的表达，从而促进叶绿素降解和ROS积累。随后，蛋白质 - 蛋白质相互作用分析揭示FaNAC047与FaNAC058发生物理相互作用，以增强其对FaNYC1、FaNOL、FaSGR和FaCAT2的调控作用。此外，FaNAC047可以转录激活FaNAC058的表达，形成一个调控级联，推动衰老进程。一致地，FaNAC058的敲低显著延迟了热诱导的叶片衰老。总体而言，我们的结果表明FaNAC047 - FaNAC058模块协同介导叶绿素降解和ROS产生，以正向调节热诱导的叶片衰老。这些发现阐明了热诱导叶片衰老的分子网络，为培育耐热植物提供了依据。
