Metabolic control of arginine and ornithine levels paces the progression of leaf senescence

Abstract

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, i.e., 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 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 is controlled in an age-dependent manner. Thirdly, we demonstrate that spermidine 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 amino acid 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.

Selenium Nanoparticles Mitigate Cadmium Stress in Tomato through Enhanced Accumulation and Transport of Sulfate/Selenite and Polyamines

“…As polyamines are crucial repressors of ethylene production in plants, higher polyamine levels resulted in lower ethylene concentrations . Notably, SeNPs play a vital role in many other abiotic and biochemical reactions in plants.…”

“…40 SAM was reported to be capable of forming polyamines and ethylene through the action of S-adenosylmethionine decarboxylase (SAMDC) and acetyl-CoA synthetase (ACS) enzymes, respectively. 41 We found that SeNPs treatment upregulated the activities of SAM and SAMDC in the shoots and roots and downregulated the activities of ACS and 1aminocyclopropane-1-carboxylic acid oxidase (ACO) (Figure 5A−D). Furthermore, under Cd stress conditions, SeNPstreated plants had higher concentrations of putrescine, spermidine, and spermine than those of the control, and the SeNPs-treated seedlings exhibited reduced ethylene production (Figure 5E−H).…”

Pyrroline‐5‐carboxylate dehydrogenase is an essential enzyme for proline dehydrogenase function during dark‐induced senescence in Arabidopsis thaliana

“…As OAT uses ornithine, which comes from arginine degradation by arginase, we could hypothesize that OAT affects nitrogen remobilization during DIS by this pathway. Recently, Liebsch et al (2022) found that metabolism of basic amino acids such as arginine and ornithine is paramount in adjusting senescence progression in Arabidopsis . These two amino acids were proposed to act as respiratory substrates via P5C and glutamate but not proline, or as precursors for polyamines biosynthesis.…”

Shade-Induced Leaf Senescence in Plants

“…The metabolic shift in the amino acid pool prolongs the lifespan of leaves by facilitating respiratory substrates and enhancing polyamines biosynthesis. This, in turn, retards leaf senescence by interfering with the ethylene signaling pathway [ 36 ].…”