Programming of Plant Leaf Senescence with Temporal and Inter-Organellar Coordination of Transcriptome in Arabidopsis1  

Abstract

Plant leaves, harvesting light energy and fixing CO 2 , are a major source of foods on the earth. Leaves undergo developmental and physiological shifts during their lifespan, ending with senescence and death. We characterized the key regulatory features of the leaf transcriptome during aging by analyzing total-and small-RNA transcriptomes throughout the lifespan of Arabidopsis (Arabidopsis thaliana) leaves at multidimensions, including age, RNA-type, and organelle. Intriguingly, senescing leaves showed more coordinated temporal changes in transcriptomes than growing leaves, with sophisticated regulatory networks comprising transcription factors and diverse small regulatory RNAs. The chloroplast transcriptome, but not the mitochondrial transcriptome, showed major changes during leaf aging, with a strongly shared expression pattern of nuclear transcripts encoding chloroplast-targeted proteins. Thus, unlike animal aging, leaf senescence proceeds with tight temporal and distinct interorganellar coordination of various transcriptomes that would be critical for the highly regulated degeneration and nutrient recycling contributing to plant fitness and productivity.Most organisms undergo age-dependent developmental changes during their lifespans. The timely decision of developmental changes during the lifespan is a critical evolutionary characteristic that maximizes fitness in a given ecological setting (Leopold, 1961;Fenner, 1998;Samach and Coupland, 2000). Plants use unique developmental strategies throughout their lifespans as opposed to animals. In plants, most organs are formed postnatally from sets of stem cells in the seed. In addition, plants are sessile and cope with encountering environments physiologically, rather than behaviorally. Thus, they have developed highly plastic and interactive developmental programs to incorporate environmental changes into their developmental decisions (Pigliucci, 1998;Sultan, 2000).The leaf is an organ that characterizes the fundamental aspects of plants. Leaves harvest light energy, fix CO 2 to produce carbohydrates, and, as primary producers in our ecosystem, serve as a major food source on the earth. Leaves undergo a series of developmental and physiological shifts during their lifespans. A leaf is initially formed as a leaf primordium derived from the stem cells at the shoot apical meristem and develops into a photosynthetic organ through biogenesis processes involving cell division, differentiation, and expansion (Tsukaya, 2013). In the later stages of their lifespans, leaves undergo organ-level senescence and eventually death. Organlevel senescence in plants involves postmitotic senescence and is a term used similarly as "aging" in animals. During the senescence stage, leaf cells undergo dramatic shifts in physiology from biogenesis to the sequential 1 This research was supported by the Institute for Basic Science (IBS-R013-D1 and IBS-R013-G1), the DGIST R&D Program (2014010043, 2015010004, 2015010011, 20150100012, and 15-01-HRLA-01), Basic Science Research Program (2010-0...

Major Cys protease activities are not essential for senescence in individually darkened Arabidopsis leaves

“…To select proteases implicated in leaf senescence, we compared the transcript levels for Arabidopsis protease-encoding genes in green and senescent leaves from a recently published leaf development time course [54]. We binned these proteases into 41 protease families according to the MEROPS peptidase database [7].…”

Natural allelic variation of GVS1 confers diversity in the regulation of leaf senescence in Arabidopsis

“…f–j). Furthermore, similar to other senescence regulators like RELATED TO ABI3/VP1 or AUXIN RESPONSIVE FACTOR2 (Lim et al ., ; Woo et al ., , ), GVS1 transcript levels gradually increase with leaf age, reaching a maximum at the early senescence stage but decreasing as senescence proceeds (Fig. S8), indicating that GVS1 might be important in regulating the initiation of leaf senescence.…”

“…A total of 1197 (90.1%) of 1318 genes belonged to SAGs, further supporting the dedicated functions of GVS1 in the regulation of SAGs. Next we identified the biological processes enriched within 1318 genes compared to the 5836 SAG s. This analysis showed that GVS1 predominantly modulates a variety of essential biological processes previously identified to occur during leaf senescence (Breeze et al ., ; Woo et al ., ), such as organ senescence, defense responses, photosynthetic processes, metabolic processes and transport, and protein regulation (Fig. e).…”

“…Diverse stress responses, such as the response to pathogens and anthocyanin accumulation, also correlated with leaf senescence in accessions, which is consistent with previous work indicating an overlap between leaf senescence and defense response programs (Haffner et al ., ). For example, many defense response genes are induced through leaf aging, and many senescence mutants exhibit altered defense responses (Buchanan‐Wollaston et al ., ; Breeze et al ., ; Lee et al ., ; Woo et al ., ). Our analysis also revealed significant variation in leaf senescence correlated with relative humidity or aridity during the growing season, although there is no apparent pattern of geographical distribution.…”

Synthetic biogenesis of chromoplasts from leaf chloroplasts

“…For the comparison of different biological systems, we selected the significantly enriched gene ontologies from our N. benthamiana RNAseq experiment (p and q values <0.05) and compared their Z-score values with those obtained from the analysis of published RNAseq data of tomato fruit ripening and Arabidopsis leaf senescence. In particular, we used the RPM values of the total pericarp at mature green (MG), light ripe (LR) and red ripe (RR) stages (Shinozaki et al, 2018) and the FPKM values of the 16D and 30D senescence stages (Woo et al, 2016). DEGs resulting from LR/MG, RR/MG and 30D/16D comparisons were filtered as described above for N. benthamiana crtB/GFP.Student's t-tests were used for the rest of statistical analyses using GraphPad Prism 5.0a (GraphPad Software).…”