CURLY LEAF Regulates MicroRNA Activity by Controlling ARGONAUTE 1 Degradation in Plants

RÉ, DELFINA A.; CAMBIAGNO, DAMIAN A.; ARCE, AGUSTIN L.; TOMASSI, ARIEL H.; GIUSTOZZI, MARISOL; CASATI, PAULA; ARIEL, FEDERICO D.; MANAVELLA, PABLO A.

MOLECULAR PLANT

OXFORD UNIV PRESS

Año: 2020 vol. 13 p. 72 - 87

1674-2052

CURLY LEAF (CLF) encodes the methyltransferase subunit of the Polycomb Repressor Complex 2 (PRC2), which regulates the expression of target genes through H3K27 trimethylation. We isolated a new CLF mutant allele (clf-78) using a genetic screen designed to identify microRNA (miRNA) deficient mutants. CLF mutant plants showed impaired miRNA activity caused by increased ubiquitination and enhanced degradation of ARGONAUTE 1 (AGO1) in specific tissues. Such CLF-mediated AGO1 regulation was evident when plants were exposed to UV radiation, which caused increased susceptibility of clf mutants to some UV-induced responses. Furthermore, we showed that CLF directly regulates FBW2, which in turn triggers AGO1 degradation in the clf mutants. Interestingly, AGO1 bound to a target appeared particularly prone to degradation in the mutant plants, a process that was exacerbated when the complex bound a non-cleavable target. Thus, prolonged AGO1–target interaction seems to favor AGO1 degradation, suggesting that non-cleavable miRNA targets may overcome translation inhibition by modulating AGO1 stability in plants. This study found that CURLY LEAF regulates AGO1 degradation and thus impairs microRNA activity in plants. This effect is observed in specific cellular niches during normal conditions as well as during UV stress. It was also found that prolonged AGO1-target interaction favors protein degradation, suggesting a potential pathway that releases translation-inhibited and non-cleavable targets of microRNA-mediated silencing.