Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice

Abstract

Coleoptile is the small conical, short-lived, sheath-like organ that safeguards the first leaf and shoot apex in cereals. It is also the first leaf-like organ to senesce that provides nutrition to the developing shoot and is, therefore, believed to play a crucial role in seedling establishment in rice and other grasses. Though histochemical studies have helped in understanding the pattern of cell death in senescing rice coleoptiles, genome-wide expression changes during coleoptile senescence have not yet been explored. With an aim to investigate the gene regulation underlying the coleoptile senescence (CS), we performed a combinatorial whole genome expression analysis by sequencing transcriptome and miRNAome of senescing coleoptiles. Transcriptome analysis revealed extensive reprogramming of 3439 genes belonging to several categories, the most prominent of which encoded for transporters, transcription factors (TFs), signaling components, cell wall organization enzymes, redox homeostasis, stress response and hormone metabolism. Small RNA sequencing identified 41 known and 21 novel miRNAs that were differentially expressed during CS. Comparison of gene expression and miRNA profiles generated for CS with publicly available leaf senescence (LS) datasets revealed that the two aging programs are remarkably distinct at molecular level in rice. Integration of expression data of transcriptome and miRNAome identified high confidence 140 miRNA-mRNA pairs forming 42 modules, thereby demonstrating multi-tiered regulation of CS. The present study has generated a comprehensive resource of the molecular networks that enrich our understanding of the fundamental pathways regulating coleoptile senescence in rice.