Light Triggers the miRNA-Biogenetic Inconsistency for De-etiolated Seedling Survivability in Arabidopsis thaliana

Suk Won Choi; Moon Young Ryu; András Viczián; Hyun Ju Jung; Gu Min Kim; Agustin L. Arce; Natalia P. Achkar; Pablo Manavella; Ulla Dolde; Stephan Wenkel; Attila Molnár; Ferenc Nagy; Seok Keun Cho; Seong Wook Yang

doi:10.1016/j.molp.2019.10.011

Light Triggers the miRNA-Biogenetic Inconsistency for De-etiolated Seedling Survivability in Arabidopsis thaliana

Suk Won Choi, Moon Young Ryu, András Viczián, Hyun Ju Jung, Gu Min Kim, Agustin L. Arce, Natalia P. Achkar, Pablo Manavella, Ulla Dolde, Stephan Wenkel, Attila Molnár, Ferenc Nagy, Seok Keun Cho, Seong Wook Yang

Research output: Contribution to journal › Article › peer-review

25 Citations (Scopus)

Abstract

The shift of dark-grown seedlings into light causes enormous transcriptome changes followed by a dramatic developmental transition. Here, we show that microRNA (miRNA) biogenesis also undergoes regulatory changes during de-etiolation. Etiolated seedlings maintain low levels of primary miRNAs (pri-miRNAs) and miRNA processing core proteins, such as Dicer-like 1, SERRATE, and HYPONASTIC LEAVES 1, whereas during de-etiolation both pri-miRNAs and the processing components accumulate to high levels. However, the levels of most miRNAs do not notably increase in response to light. To reconcile this inconsistency, we demonstrated that an unknown suppressor decreases miRNA-processing activity and light-induced SMALL RNA DEGRADING NUCLEASE 1 shortens the half-life of several miRNAs in de-etiolated seedlings. Taken together, these data suggest a novel mechanism, miRNA-biogenetic inconsistency, which accounts for the intricacy of miRNA biogenesis during de-etiolation. This mechanism is essential for the survival of de-etiolated seedlings after long-term skotomorphogenesis and their optimal adaptation to ever-changing light conditions.

Original language	English
Pages (from-to)	431-445
Number of pages	15
Journal	Molecular Plant
Volume	13
Issue number	3
DOIs	https://doi.org/10.1016/j.molp.2019.10.011
Publication status	Published - 2020 Mar 2

Bibliographical note

Funding Information:
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 and Future Planning (NRF- 2017R1A2B4010255 and 2018R1A6A1A03025607 ); NRF- 2017R1A6A3A11035981 to M.Y.R.; and NRF- 2017H1A2A1044209 to S.W.C. The research was supported in part by Brain Korea 21 (BK21) PLUS program; S.W.C. and G.M.K. are fellowship awardees of the BK21 PLUS program. The research in Hungary was supported by grants from the Economic Development and Innovation Operative Program ( GINOP-2.3.2-15-2016-00015 and GINOP-2.3.2-15-2016-00032 ).

Publisher Copyright:
© 2019 The Author

All Science Journal Classification (ASJC) codes

Molecular Biology
Plant Science

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10.1016/j.molp.2019.10.011

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Choi, S. W., Ryu, M. Y., Viczián, A., Jung, H. J., Kim, G. M., Arce, A. L., Achkar, N. P., Manavella, P., Dolde, U., Wenkel, S., Molnár, A., Nagy, F., Cho, S. K., & Yang, S. W. (2020). Light Triggers the miRNA-Biogenetic Inconsistency for De-etiolated Seedling Survivability in Arabidopsis thaliana. Molecular Plant, 13(3), 431-445. https://doi.org/10.1016/j.molp.2019.10.011

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title = "Light Triggers the miRNA-Biogenetic Inconsistency for De-etiolated Seedling Survivability in Arabidopsis thaliana",

abstract = "The shift of dark-grown seedlings into light causes enormous transcriptome changes followed by a dramatic developmental transition. Here, we show that microRNA (miRNA) biogenesis also undergoes regulatory changes during de-etiolation. Etiolated seedlings maintain low levels of primary miRNAs (pri-miRNAs) and miRNA processing core proteins, such as Dicer-like 1, SERRATE, and HYPONASTIC LEAVES 1, whereas during de-etiolation both pri-miRNAs and the processing components accumulate to high levels. However, the levels of most miRNAs do not notably increase in response to light. To reconcile this inconsistency, we demonstrated that an unknown suppressor decreases miRNA-processing activity and light-induced SMALL RNA DEGRADING NUCLEASE 1 shortens the half-life of several miRNAs in de-etiolated seedlings. Taken together, these data suggest a novel mechanism, miRNA-biogenetic inconsistency, which accounts for the intricacy of miRNA biogenesis during de-etiolation. This mechanism is essential for the survival of de-etiolated seedlings after long-term skotomorphogenesis and their optimal adaptation to ever-changing light conditions.",

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note = "Funding Information: 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 and Future Planning (NRF- 2017R1A2B4010255 and 2018R1A6A1A03025607 ); NRF- 2017R1A6A3A11035981 to M.Y.R.; and NRF- 2017H1A2A1044209 to S.W.C. The research was supported in part by Brain Korea 21 (BK21) PLUS program; S.W.C. and G.M.K. are fellowship awardees of the BK21 PLUS program. The research in Hungary was supported by grants from the Economic Development and Innovation Operative Program ( GINOP-2.3.2-15-2016-00015 and GINOP-2.3.2-15-2016-00032 ). Publisher Copyright: {\textcopyright} 2019 The Author",

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AU - Choi, Suk Won

AU - Ryu, Moon Young

AU - Viczián, András

AU - Jung, Hyun Ju

AU - Kim, Gu Min

AU - Arce, Agustin L.

AU - Achkar, Natalia P.

AU - Manavella, Pablo

AU - Dolde, Ulla

AU - Wenkel, Stephan

AU - Molnár, Attila

AU - Nagy, Ferenc

AU - Cho, Seok Keun

AU - Yang, Seong Wook

N1 - Funding Information: 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 and Future Planning (NRF- 2017R1A2B4010255 and 2018R1A6A1A03025607 ); NRF- 2017R1A6A3A11035981 to M.Y.R.; and NRF- 2017H1A2A1044209 to S.W.C. The research was supported in part by Brain Korea 21 (BK21) PLUS program; S.W.C. and G.M.K. are fellowship awardees of the BK21 PLUS program. The research in Hungary was supported by grants from the Economic Development and Innovation Operative Program ( GINOP-2.3.2-15-2016-00015 and GINOP-2.3.2-15-2016-00032 ). Publisher Copyright: © 2019 The Author

PY - 2020/3/2

Y1 - 2020/3/2

N2 - The shift of dark-grown seedlings into light causes enormous transcriptome changes followed by a dramatic developmental transition. Here, we show that microRNA (miRNA) biogenesis also undergoes regulatory changes during de-etiolation. Etiolated seedlings maintain low levels of primary miRNAs (pri-miRNAs) and miRNA processing core proteins, such as Dicer-like 1, SERRATE, and HYPONASTIC LEAVES 1, whereas during de-etiolation both pri-miRNAs and the processing components accumulate to high levels. However, the levels of most miRNAs do not notably increase in response to light. To reconcile this inconsistency, we demonstrated that an unknown suppressor decreases miRNA-processing activity and light-induced SMALL RNA DEGRADING NUCLEASE 1 shortens the half-life of several miRNAs in de-etiolated seedlings. Taken together, these data suggest a novel mechanism, miRNA-biogenetic inconsistency, which accounts for the intricacy of miRNA biogenesis during de-etiolation. This mechanism is essential for the survival of de-etiolated seedlings after long-term skotomorphogenesis and their optimal adaptation to ever-changing light conditions.

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Light Triggers the miRNA-Biogenetic Inconsistency for De-etiolated Seedling Survivability in Arabidopsis thaliana

Abstract

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