Plastid retrograde regulation of miRNA expression in response to light stress

Background MicroRNAs (miRNAs) are a class of endogenous noncoding RNAs that play a pivotal role in the regulation of plant development and responses to the surrounding environment. Despite the efforts made to elucidate their function in the adaptation of plants to many abiotic and biotic stresses, their role in high light (HL) stress is still vague. HL stress often arises upon plant exposure to full sunlight. Subsequent changes in nuclear gene expression are triggered by chloroplast-derived retrograde signals. Results In this study, we show that HL is involved in miRNA-dependent regulation in Arabidopsis thaliana rosettes. Microtranscriptomic screening revealed a limited number of miRNAs reacting to HL. To explain the miRNA regulation mechanisms at the different biogenesis stages, chemical and genetic approaches were applied. First, we tested the possible role of plastoquinone (PQ) redox changes using photosynthetic electron transport chain inhibitors. The results suggest that increased primary transcript abundance (pri-miRNAs) of HL-regulated miRNAs is dependent on signals upstream of PQ. This indicates that such signals may originate from photosystem II, which is the main singlet oxygen (O-1(2)) source. Nevertheless, no changes in pri-miRNA expression upon a dark-light shift in the conditional fluorescent (flu) mutant producing O-1(2) were observed when compared to wild-type plants. Thus, we explored the O-1(2) signaling pathway, which is initiated independently in HL and is related to beta-carotene oxidation and production of volatile derivatives, such as beta-cyclocitral (beta-CC). Pri-miRNA induction by beta-CC, which is a component of this O-1(2) pathway, as well as an altered response in the methylene blue sensitivity 1 (mbs1) mutant support the role of O-1(2) signaling in miRNA regulation. Conclusions We show that light stress triggers changes in miRNA expression. This stress response may be regulated by reactive oxygen species (ROS)-related signaling. In conclusion, our results link ROS action to miRNA biogenesis, suggesting its contribution to inconsistent pri- and mature miRNA dynamics.

Automated summary

This study reveals that light stress can trigger changes in miRNA expression. This stress response may be regulated by ROS-related signaling.