Environmental conditions switch alternative micro RNA biogenesis pathways

MANAVELLA PA,

Congreso; 16th HFSP Awardees Meeting; 2016

MicroRNAs (miRNAs) are small RNA molecules that are critical for the normal development of multicellular organisms. The key feature that makes miRNAs fundamental for plant homeostasis is their evolutionary preference to silence transcription factors. These small regulatory molecules are produced from primary miRNA transcripts by a single nuclear enzyme, DICER-LIKE 1 (DCL1). The accurate excision of the miRNA duplexes relies on the interaction of DCL1 with HYPONASTIC LEAVES1 (HYL1). The miRNA-processing complex works as a molecular ruler that recognizes the correct position in the miRNA primary transcript and release the mature miRNA. In the absence of HYL1, DCL1 is unable to recognize the correct cleavage site and produces less, or aberrant, miRNAs leading to severe morphological defects. The activity of HYL1, and therefore the miRNAs production, is regulated by phosphorylation events. This post-transcriptional regulation allows a fast reduction of the miRNA production when necessary.We have found that the absence, or deficiency, of a proper light source triggers the degradation of HYL1 in plants. Such degradation occurs in the cell cytoplasm where only the active form of HYL1 is transported during the night, leaving the phosphorylated HYL1 as an inactive reservoir in the nucleus. As a consequence of the reduction in the synthesis of miRNAs, the silencing of several miRNA-regulated transcriptions factors is released allowing the plant to activate developmental programs aiming to reach the light. Interestingly, upon the detection of a light source the inactive HYL1 reservoir is de-phosphorylated allowing a quick conversion to the active form. On the other hand, such a drastic reduction in miRNAs production could be counterproductive for the plant if the dark condition last too long, a situation that plants normally face during winter. Remarkably, we found that plants grown in dark and cold conditions activate a HYL1-independent miRNA processing mechanism. This alternative pathway is activated after several days of darkness and cold, when the HYL1 active form is absent. In silico analysis suggested that the secondary structure adopted by the miRNA precursors, transcribed and folded at low temperature, is energetically more stable and is the reason why DCL1 can recognize and process them without assistance.