Unraveling multifaceted contributions of small regulatory RNAs to photomorphogenic development in Arabidopsis

Meng-Chun Lin, Huang-Lung Tsai, Sim-Lin Lim, Shih-Tong Jeng, Shu-Hsing Wu

Post-transcriptional control of gene expression mediated by small regulatory RNAs (sRNAs) is vital for growth and development of diverse organisms. The biogenesis of sRNAs is regulated by both positive and negative regulators known to regulate photomorphogenic development. Two microRNAs (miRNAs), miR157 and miR319, also regulate photomorphogenesis. However, genome-wide profiling of sRNAs and their regulation of target genes during photomorphogenesis has been missing. We provide a comprehensive view of sRNA-controlled gene expression in this developmental process. By profiling sRNAs and the 5' ends of degraded mRNAs during the first 24 h of photomorphogenic development in Arabidopsis, we identified 335 sRNA-mediated mRNA cleavage events in de-etiolating seedlings. These cleavage events are primarily resulted from actions of highly expressed miRNAs and irrelevant to the abundance of target mRNAs. In the light, the expression of the slicer protein gene ARGONAUTE1 in the miRNA functioning pathway could be fine-tuned by miRNA168a/b. We also found that miR396a/b positively regulates de-etiolation by suppressing GROWTH REGULATING FACTORs. Our results suggest that the miRNAs are required to tune down the target mRNAs and regulate photomorphogenesis. sRNAs may have a broad impact on gene expression regulation for optimized photomorphogenic development. With both positive and negative regulators under the control of sRNAs, young Arabidopsis seedlings can have a timely but not exaggerated developmental adaptation to light.