HYL1-CLEAVAGE SUBTILASE 1 (HCS1) suppresses miRNA biogenesis in response to light-to-dark transition

Hyun Ju Jung, Suk Won Choi, Kyung Hwan Boo, Jee Eun Kim, Young Kyoung Oh, Min Kyun Han, Moon Young Ryu, Chang Woo Lee, Christian Møller, Pratik Shah, Gu Min Kim, Woorim Yang, Seok Keun Cho, Seong Wook Yang

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Abstract

The core plant microprocessor consists of DICER-LIKE 1 (DCL1), SERRATE (SE), and HYPONASTIC LEAVES 1 (HYL1) and plays a pivotal role in microRNA (miRNA) biogenesis. However, the proteolytic regulation of each component remains elusive. Here, we show that HYL1-CLEAVAGE SUBTILASE 1 (HCS1) is a cytoplasmic protease for HYL1-destabilization. HCS1-excessiveness reduces HYL1 that disrupts miRNA biogenesis, while HCS1-deficiency accumulates HYL1. Consistently, we identified the HYL1K154A mutant that is insensitive to the proteolytic activity of HCS1, confirming the importance of HCS1 in HYL1 proteostasis. Moreover, HCS1-activity is regulated by light/dark transition. Under light, cytoplasmic CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) E3 ligase suppresses HCS1-activity. COP1 sterically inhibits HCS1 by obstructing HYL1 access into the catalytic sites of HCS1. In contrast, darkness unshackles HCS1-activity for HYL1-destabilization due to nuclear COP1 relocation. Overall, the COP1-HYL1-HCS1 network may integrate two essential cellular pathways: the miRNA-biogenetic pathway and light signaling pathway.

Original languageEnglish
Article numbere2116757119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number6
DOIs
Publication statusPublished - 2022 Feb 8

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. We thank Nam-Chon Paek for providing cop1-4/ 35S:COP1WT-GFP and cop1-4/35S:COP1L170A-GFP transgenic plants. This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science, ICT (information and communications technology), and Future Planning (NRF-2020R1A2B5B01002592 and NRF-2018R1A6A1A03025607), and by Samsung Science and Technology Foundation Project SSTF-BA1801-09 (to S.W.Y.). This research was supported in part by NRF-2020R1I1A1A01073842 (to H.J.J.); and Brain Korea 21 (BK21) PLUS program fellowship awards to S.W.C., Y.K.O., M.K.H., C.M., and G.M.K.

Publisher Copyright:
© 2022 National Academy of Sciences. All rights reserved.

All Science Journal Classification (ASJC) codes

  • General

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