Multidimensional Transcriptome Analysis of Arabidopsis Leaf Senescence Program

Abstract

Most organisms undergo age-dependent developmental shifts during their life spans, ending with senescence and death. Plant leaves, as a major food source on the earth harvesting the light energy and fixing CO2, also undergo physiological shifts during their life span controlled by highly plastic developmental programs. To investigate how the transcriptional programs are operated to maximize plant fitness during the life span, high-resolution transcriptome datasets were generated. Strand-specific total RNA-seq and small RNA-seq datasets covering the entire Arabidopsis (Arabidopsis thaliana) leaf life span enabled multidimensional analysis of leaf transcriptomes, including age, RNAtype, and organelle. Global changes of coding and long noncoding RNAs, small regulatory RNAs, and various noncoding RNA-derived small RNAs were explored. Whole leaf life span was divided into two developmental stages, growth-to-maturation and maturation-to-senescence, to illuminate the differences between the early and late developmental stages. Unexpectedly, senescing leaves showed higher degree of temporal coordination in transcriptomes than growing leaves, with complex multi-level regulations comprising transcription factors and diverse small regulatory RNAs. Another novel finding is that the chloroplast transcriptome, but not the mitochondrial transcriptome, is utilized as a key constituent in leaf life span programs showing a strong temporal and organellar coordination with nuclear transcripts encoding chloroplast-targeted proteins. Thus, contrary to animal aging, leaf senescence proceeds with tight coordination between nuclear and chloroplast transcriptomes which would be critical for balanced metabolic processes and nutrient relocalization contributing to plant fitness and productivity. This Arabidopsis leaf transcriptome provides a comprehensive resource for multidimensional understanding of functional and regulatory programs during life span.