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

doi:10.1073/pnas.2116757119

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

Research output: Contribution to journal › Journal article › Research › peer-review

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 HYL1^K154A 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 language	English
Article number	e2116757119
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	119
Issue number	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.2116757119
Publication status	Published - 8 Feb 2022
Externally published	Yes

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.

Keywords

COP1 E3 ligase
HYL1 proteostasis
Light/dark transition
MiRNA biogenesis
Subtilisin-like protease

Link to document

10.1073/pnas.2116757119

Cite this

Jung, H. J., Choi, S. W., Boo, K. H., Kim, J. E., Oh, Y. K., Han, M. K., Ryu, M. Y., Lee, C. W., Møller, C., Shah, P., Kim, G. M., Yang, W., Cho, S. K., & Yang, S. W. (2022). HYL1-CLEAVAGE SUBTILASE 1 (HCS1) suppresses miRNA biogenesis in response to light-to-dark transition. Proceedings of the National Academy of Sciences of the United States of America, 119(6), Article e2116757119. https://doi.org/10.1073/pnas.2116757119

@article{c3e1200b2cc247d78390ae7b4af4a26a,

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

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.",

keywords = "COP1 E3 ligase, HYL1 proteostasis, Light/dark transition, MiRNA biogenesis, Subtilisin-like protease",

author = "Jung, {Hyun Ju} and Choi, {Suk Won} and Boo, {Kyung Hwan} and Kim, {Jee Eun} and Oh, {Young Kyoung} and Han, {Min Kyun} and Ryu, {Moon Young} and Lee, {Chang Woo} and Christian M{\o}ller and Pratik Shah and Kim, {Gu Min} and Woorim Yang and Cho, {Seok Keun} and Yang, {Seong Wook}",

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: {\textcopyright} 2022 National Academy of Sciences. All rights reserved.",

year = "2022",

month = feb,

day = "8",

doi = "10.1073/pnas.2116757119",

language = "English",

volume = "119",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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Jung, HJ, Choi, SW, Boo, KH, Kim, JE, Oh, YK, Han, MK, Ryu, MY, Lee, CW, Møller, C, Shah, P, Kim, GM, Yang, W, Cho, SK & Yang, SW 2022, 'HYL1-CLEAVAGE SUBTILASE 1 (HCS1) suppresses miRNA biogenesis in response to light-to-dark transition', Proceedings of the National Academy of Sciences of the United States of America, vol. 119, no. 6, e2116757119. https://doi.org/10.1073/pnas.2116757119

HYL1-CLEAVAGE SUBTILASE 1 (HCS1) suppresses miRNA biogenesis in response to light-to-dark transition. / Jung, Hyun Ju; Choi, Suk Won; Boo, Kyung Hwan et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 119, No. 6, e2116757119, 08.02.2022.

Research output: Contribution to journal › Journal article › Research › peer-review

TY - JOUR

T1 - HYL1-CLEAVAGE SUBTILASE 1 (HCS1) suppresses miRNA biogenesis in response to light-to-dark transition

AU - Jung, Hyun Ju

AU - Choi, Suk Won

AU - Boo, Kyung Hwan

AU - Kim, Jee Eun

AU - Oh, Young Kyoung

AU - Han, Min Kyun

AU - Ryu, Moon Young

AU - Lee, Chang Woo

AU - Møller, Christian

AU - Shah, Pratik

AU - Kim, Gu Min

AU - Yang, Woorim

AU - Cho, Seok Keun

AU - Yang, Seong Wook

N1 - 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.

PY - 2022/2/8

Y1 - 2022/2/8

N2 - 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.

AB - 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.

KW - COP1 E3 ligase

KW - HYL1 proteostasis

KW - Light/dark transition

KW - MiRNA biogenesis

KW - Subtilisin-like protease

UR - http://www.scopus.com/inward/record.url?scp=85124119447&partnerID=8YFLogxK

U2 - 10.1073/pnas.2116757119

DO - 10.1073/pnas.2116757119

M3 - Journal article

C2 - 35121664

AN - SCOPUS:85124119447

SN - 0027-8424

VL - 119

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 6

M1 - e2116757119

ER -

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

Abstract

Bibliographical note

Keywords

Link to document

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