Developmentally controlled changes during Arabidopsis leaf development indicate causes for loss of stress tolerance with age

Abstract

Leaf senescence is the final stage of leaf development and is induced by the gradual occurrence of Age-Related Changes (ARCs). The process of leaf senescence has been well described but the cellular events leading to this process are still poorly understood. By analysis of progressively ageing, but not yet senescing Arabidopsis thaliana rosette leaves, we aimed to better understand processes occurring prior to the onset of senescence. Using gene expression analysis, we found that as leaves mature, genes responding to oxidative stress and genes involved in stress-hormone biosynthesis and signalling were upregulated. A decrease in primary metabolites that provide protection against oxidative stress provided a possible explanation for the increased stress signature. The gene expression and metabolomics changes occurred concomitantly to a decrease in drought, salinity and dark stress tolerance of individual leaves. Importantly, stress-related genes showed elevated expression in the early ageing mutant old5 and decreased expression in the delayed-ageing mutant ore9. We propose that the decreased stress tolerance with age results from the occurrence of senescence-inducing ARCs that is integrated into the leaf developmental program, and that this ensures a timely and certain death.

Quantitative Analysis of UV-B Radiation Interception and Bioactive Compound Contents in Kale by Leaf Position According to Growth Progress

“…As growth progressed, the TFC increase rate in the upper leaves increased noticeably ( Figure 7B ). In other words, young leaves had the highest UV-B susceptibility for TFC, which was consistent with the previous findings of general stress susceptibility with leaf age ( Sperdouli and Moustakas, 2014 ; Moustaka et al, 2015 ; Kanojia et al, 2020 ). As growth progressed, the TFC and TPC increase rates increased or decreased for all leaf positions, but the actual concentrations were similar between 14 and 28 DAT ( Figures 5 , 7 ).…”

“…As growth progressed, the TFC increase rate in the upper leaves increased noticeably (Figure 7B). In other words, young leaves had the highest UV-B susceptibility for TFC, which was consistent with the previous findings of general stress susceptibility with leaf age (Sperdouli and Moustakas, 2014;Moustaka et al, 2015;Kanojia et al, 2020).…”

Age-Dependent Abiotic Stress Resilience in Plants

“…Under optimal growth conditions, the onset of leaf senescence occurs in an age-dependent manner and involves a complex interplay between internal and external factors, which determine its timing, progression, and completion [35]. Mature leaves can become competent for internal and external factors that activate senescence due to the accumulation of age-related changes [36]. During early leaf development, leaves are not responsive toward senescence-inducing factors, probably to protect younger leaves [37].…”

Primary metabolic processes as drivers of leaf ageing

“…For instance, leaves of 3000-year-old Platycladus orientalis had higher ROS levels together with the upregulation of genes involved in ROS production and stress responses than the leaves of a 20-year-old plant of the same species [ 34 ]. Likewise, age-dependent transcriptomes of Arabidopsis leaves showed that the expression of genes associated with oxidative stress were elevated in leaves before the completion of leaf growth and senescence initiation [ 6 , 35 ]. An analysis of the Arabidopsis leaf transcriptome during ageing also showed enrichment of abiotic stress-responsive genes in matured leaves before the onset of senescence [ 19 ].…”

“…In light, sugars are converted to starch, which is remobilised at night to support metabolism and growth of plants [ 43 ]. In a recent study, analysis of primary metabolites in progressively ageing Arabidopsis leaves showed that 14 sugar metabolites, including fructose, glucose, maltose, mannitol, galactose, trehalose, and other unidentified sugars that were high in young expanding leaves, decreased gradually during leaf expansion, and well before the onset of leaf senescence [ 35 ]. A similar pattern of reduction in sugar metabolites before the initiation of senescence was observed in comprehensive metabolomics studies performed on Nicotiana tabacum (tobacco) leaves during five developmental stages [ 44 ].…”