Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, S-90187 Umeå, Sweden.
National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China.
Plant Physiol. 2022 Aug 1;189(4):1943-1960. doi: 10.1093/plphys/kiac244.
Leaf senescence can be induced by stress or aging, sometimes in a synergistic manner. It is generally acknowledged that the ability to withstand senescence-inducing conditions can provide plants with stress resilience. Although the signaling and transcriptional networks responsible for a delayed senescence phenotype, often referred to as a functional stay-green trait, have been actively investigated, very little is known about the subsequent metabolic adjustments conferring this aptitude to survival. First, using the individually darkened leaf (IDL) experimental setup, we compared IDLs of wild-type (WT) Arabidopsis (Arabidopsis thaliana) to several stay-green contexts, that is IDLs of two functional stay-green mutant lines, oresara1-2 (ore1-2) and an allele of phytochrome-interacting factor 5 (pif5), as well as to leaves from a WT plant entirely darkened (DP). We provide compelling evidence that arginine and ornithine, which accumulate in all stay-green contexts-likely due to the lack of induction of amino acids (AAs) transport-can delay the progression of senescence by fueling the Krebs cycle or the production of polyamines (PAs). Secondly, we show that the conversion of putrescine to spermidine (SPD) is controlled in an age-dependent manner. Thirdly, we demonstrate that SPD represses senescence via interference with ethylene signaling by stabilizing the ETHYLENE BINDING FACTOR1 and 2 (EBF1/2) complex. Taken together, our results identify arginine and ornithine as central metabolites influencing the stress- and age-dependent progression of leaf senescence. We propose that the regulatory loop between the pace of the AA export and the progression of leaf senescence provides the plant with a mechanism to fine-tune the induction of cell death in leaves, which, if triggered unnecessarily, can impede nutrient remobilization and thus plant growth and survival.
叶片衰老可以由胁迫或衰老引起，有时以协同方式发生。人们普遍认为，能够承受诱导衰老的条件可以为植物提供抗胁迫能力。尽管负责延迟衰老表型的信号和转录网络，通常称为功能性保持绿色性状，已经被积极研究，但对于赋予这种生存能力的后续代谢调整知之甚少。首先，我们使用单独黑暗化叶片（IDL）实验设置，将野生型（WT）拟南芥（Arabidopsis thaliana）的 IDL 与几种保持绿色的情况进行了比较，即两种功能性保持绿色突变体线 ore1-2 和 phy-tochrome-interacting factor 5（pif5）的一个等位基因的 IDL，以及完全黑暗化的 WT 植物叶片（DP）。我们提供了令人信服的证据，表明精氨酸和鸟氨酸在所有保持绿色的情况下积累，这可能是由于缺乏诱导氨基酸（AAs）转运所致，通过为三羧酸循环或多胺（PA）的产生提供燃料，可以延缓衰老的进展。其次，我们表明腐胺向亚精胺（SPD）的转化受年龄依赖性控制。第三，我们证明 SPD 通过稳定 ETHYLENE BINDING FACTOR1 和 2（EBF1/2）复合物来干扰乙烯信号，从而抑制衰老。总之，我们的结果确定精氨酸和鸟氨酸作为影响叶片衰老应激和年龄依赖性进展的核心代谢物。我们提出，AA 输出的速度与叶片衰老的进展之间的调节环为植物提供了一种机制，可以精细调节叶片中细胞死亡的诱导，如果不必要地触发，这可能会阻碍养分再利用，从而影响植物的生长和生存。
