Dual function of HYPONASTIC LEAVES 1 during early skotomorphogenic growth in Arabidopsis.
Arabidopsis thaliana
HY5
HYL1
hook unfolding
miRNA
microprocessing
skotomorphogenesis
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
22
08
2019
accepted:
03
01
2020
pubmed:
11
1
2020
medline:
5
2
2021
entrez:
11
1
2020
Statut:
ppublish
Résumé
Seeds germinating underground display a specific developmental programme, termed skotomorphogenesis, to ensure survival of the emerging seedlings until they reach the light. They rapidly elongate the hypocotyl and maintain the cotyledons closed, forming a hook with the hypocotyl in order to protect apical meristematic cells from mechanical damage. Such crucial events for the fate of the seedling are tightly regulated and although some transcriptional regulators and phytohormones are known to be implicated in this regulation, we are still far from a complete understanding of these biological processes. Our work provides information on the diverse roles in skotomorphogenesis of the core components of microRNA biogenesis in Arabidopsis, HYL1, DCL1, and SE. We show that hypocotyl elongation is promoted by all these components, probably through the action of specific miRNAs. Hook development also depends on these proteins however, remarkably, HYL1 exerts its role in an opposite way to DCL1 and SE. Interestingly, we found that a specific HYL1 domain involved in protein-protein interaction is required for this function. Genetic evidences also point to the phosphorylation status of HYL1 as important for this function. We propose that HYL1 help maintain the hook closed during early skotomorphogenesis in a microprocessor-independent manner by repressing the activity of HY5, the transcriptional master regulator that triggers light responses. This work uncovers a previously unnoticed link between components of the miRNA biogenesis machinery, the skotomorphogenic growth, and hook development in Arabidopsis.
Substances chimiques
Arabidopsis Proteins
0
Basic-Leucine Zipper Transcription Factors
0
Cell Cycle Proteins
0
HY5 protein, Arabidopsis
0
HYL1 protein, Arabidopsis
0
MicroRNAs
0
RNA-Binding Proteins
0
DCL1 protein, Arabidopsis
EC 3.1.26.3
Ribonuclease III
EC 3.1.26.3
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
977-991Informations de copyright
© 2020 The Authors The Plant Journal © 2020 John Wiley & Sons Ltd.
Références
Achkar, N.P., Cho, S.K., Poulsen, C. et al. (2018) A quick HYL1-dependent reactivation of MicroRNA production is required for a proper developmental response after extended periods of light deprivation. Dev. Cell, 46, 236-247.e6.
Baumberger, N. and Baulcombe, D.C. (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA, 102, 11928-11933.
Bollman, K.M., Aukerman, M.J., Park, M.Y., Hunter, C., Berardini, T.Z. and Poethig, R.S. (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development, 130, 1493-1504.
Burdisso, P., Milia, F., Schapire, A.L., Bologna, N.G., Palatnik, J.F. and Rasia, R.M. (2014) Structural determinants of Arabidopsis thaliana Hyponastic leaves 1 function in vivo. PLoS ONE, 9, e113243.
Chattopadhyay, S., Ang, L.H., Puente, P., Deng, X.W. and Wei, N. (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell, 10, 673-683.
Chen, C., Ridzon, D.A., Broomer, A.J. et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33, e179.
Chiu, R.S., Pan, S., Zhao, R. and Gazzarrini, S. (2016) ABA-dependent inhibition of the ubiquitin proteasome system during germination at high temperature in Arabidopsis. Plant J, 88, 749-761.
Cho, S.K., Ben Chaabane, S., Shah, P., Poulsen, C.P. and Yang, S.W. (2014) COP1 E3 ligase protects HYL1 to retain microRNA biogenesis. Nat. Commun. 5, 5867.
Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-43.
Dong, Z., Han, M.H. and Fedoroff, N. (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc. Natl. Acad. Sci. USA, 105, 9970-9975.
Fang, Y. and Spector, D.L. (2007) Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol. 17, 818-823.
Gangappa, S.N. and Botto, J.F. (2016) The Multifaceted roles of HY5 in plant growth and development. Mol. Plant, 9, 1353-1365.
Gommers, C.M.M. and Monte, E. (2018) Seedling establishment: a dimmer switch-regulated process between dark and light signaling. Plant Physiol. 176, 1061-1074.
Hardtke, C.S., Gohda, K., Osterlund, M.T., Oyama, T., Okada, K. and Deng, X.W. (2000) HY5 stability and activity in arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J. 19, 4997-5006.
Iwata, Y., Takahashi, M., Fedoroff, N.V. and Hamdan, S.M. (2013) Dissecting the interactions of SERRATE with RNA and DICER-LIKE 1 in Arabidopsis microRNA precursor processing. Nucleic Acids Res. 41, 9129-9140.
Josse, E.M. and Halliday, K.J. (2008) Skotomorphogenesis: the dark side of light signalling. Curr. Biol. 18, R1144-R1146.
Karlsson, P., Christie, M.D., Seymour, D.K., Wang, H., Wang, X., Hagmann, J., Kulcheski, F. and Manavella, P.A. (2015) KH domain protein RCF3 is a tissue-biased regulator of the plant miRNA biogenesis cofactor HYL1. Proc. Natl. Acad. Sci. USA, 112, 14096-14101.
Kurihara, Y., Takashi, Y. and Watanabe, Y. (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA, 12, 206-212.
Laubinger, S., Zeller, G., Henz, S.R., Buechel, S., Sachsenberg, T., Wang, J.W., Ratsch, G. and Weigel, D. (2010) Global effects of the small RNA biogenesis machinery on the Arabidopsis thaliana transcriptome. Proc. Natl. Acad. Sci. USA, 107, 17466-17473.
Lee, J., He, K., Stolc, V., Lee, H., Figueroa, P., Gao, Y., Tongprasit, W., Zhao, H., Lee, I. and Deng, X.W. (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell, 19, 731-749.
Leivar, P., Monte, E., Oka, Y., Liu, T., Carle, C., Castillon, A., Huq, E. and Quail, P.H. (2008) Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr. Biol. 18, 1815-1823.
Leivar, P., Tepperman, J.M., Monte, E., Calderon, R.H., Liu, T.L. and Quail, P.H. (2009) Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell, 21, 3535-3553.
Lorrain, S., Trevisan, M., Pradervand, S. and Fankhauser, C. (2009) Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J. 60, 449-461.
Lu, C. and Fedoroff, N. (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell, 12, 2351-2366.
Machida, S., Chen, H.Y. and Adam Yuan, Y. (2011) Molecular insights into miRNA processing by Arabidopsis thaliana SERRATE. Nucleic Acids Res. 39, 7828-7836.
Manavella, P.A., Hagmann, J., Ott, F., Laubinger, S., Franz, M., Macek, B. and Weigel, D. (2012) Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell, 151, 859-870.
Mazzella, M.A., Casal, J.J., Muschietti, J.P. and Fox, A.R. (2014) Hormonal networks involved in apical hook development in darkness and their response to light. Front. Plant Sci. 5, 52.
Morel, J.B., Godon, C., Mourrain, P., Beclin, C., Boutet, S., Feuerbach, F., Proux, F. and Vaucheret, H. (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell, 14, 629-639.
Osterlund, M.T., Hardtke, C.S., Wei, N. and Deng, X.W. (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature, 405, 462-466.
Park, M.Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H. and Poethig, R.S. (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc. Natl. Acad. Sci. USA, 102, 3691-3696.
Piskurewicz, U. and Lopez-Molina, L. (2011) Isolation of genetic material from Arabidopsis seeds. Methods Mol. Biol. 773, 151-164.
Prigge, M.J. and Wagner, D.R. (2001) The arabidopsis serrate gene encodes a zinc-finger protein required for normal shoot development. Plant Cell, 13, 1263-1279.
Qin, H., Chen, F., Huan, X., Machida, S., Song, J. and Yuan, Y.A. (2010) Structure of the Arabidopsis thaliana DCL4 DUF283 domain reveals a noncanonical double-stranded RNA-binding fold for protein-protein interaction. RNA, 16, 474-481.
Raghuram, B., Sheikh, A.H., Rustagi, Y. and Sinha, A.K. (2015) MicroRNA biogenesis factor DRB1 is a phosphorylation target of mitogen activated protein kinase MPK3 in both rice and Arabidopsis. FEBS J. 282, 521-536.
Rasia, R.M., Mateos, J., Bologna, N.G., Burdisso, P., Imbert, L., Palatnik, J.F. and Boisbouvier, J. (2010) Structure and RNA interactions of the plant MicroRNA processing-associated protein HYL1. Biochemistry, 49, 8237-8239.
Schauer, S.E., Jacobsen, S.E., Meinke, D.W. and Ray, A. (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci. 7, 487-491.
Shin, J., Park, E. and Choi, G. (2007) PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J. 49, 981-994.
Su, C., Li, Z., Cheng, J., Li, L., Zhong, S., Liu, L., Zheng, Y. and Zheng, B. (2017) The protein phosphatase 4 and SMEK1 complex dephosphorylates HYL1 to promote miRNA biogenesis by antagonizing the MAPK cascade in Arabidopsis. Dev. Cell, 41, 527-539.e5.
Sun, Z., Li, M., Zhou, Y., Guo, T., Liu, Y., Zhang, H. and Fang, Y. (2018) Coordinated regulation of Arabidopsis microRNA biogenesis and red light signaling through Dicer-like 1 and phytochrome-interacting factor 4. PLoS Genet. 14, e1007247.
Tsai, H.L., Li, Y.H., Hsieh, W.P., Lin, M.C., Ahn, J.H. and Wu, S.H. (2014) HUA ENHANCER1 is involved in posttranscriptional regulation of positive and negative regulators in Arabidopsis photomorphogenesis. Plant Cell, 26, 2858-2872.
Vazquez, F., Gasciolli, V., Crete, P. and Vaucheret, H. (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr. Biol. 14, 346-351.
Wang, Z., Ma, Z., Castillo-Gonzalez, C., Sun, D., Li, Y., Yu, B., Zhao, B., Li, P. and Zhang, X. (2018) SWI2/SNF2 ATPase CHR2 remodels pri-miRNAs via Serrate to impede miRNA production. Nature, 557, 516-521.
Wu, F., Yu, L., Cao, W., Mao, Y., Liu, Z. and He, Y. (2007) The N-terminal double-stranded RNA binding domains of Arabidopsis HYPONASTIC LEAVES1 are sufficient for pre-microRNA processing. Plant Cell, 19, 914-925.
Yan, J., Wang, P., Wang, B. et al. (2017) The SnRK2 kinases modulate miRNA accumulation in Arabidopsis. PLoS Genet. 13, e1006753.
Yang, L., Liu, Z., Lu, F., Dong, A. and Huang, H. (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J. 47, 841-850.
Yang, S.W., Chen, H.Y., Yang, J., Machida, S., Chua, N.H. and Yuan, Y.A. (2010) Structure of Arabidopsis HYPONASTIC LEAVES1 and its molecular implications for miRNA processing. Structure, 18, 594-605.
Yang, X., Ren, W., Zhao, Q., Zhang, P., Wu, F. and He, Y. (2014) Homodimerization of HYL1 ensures the correct selection of cleavage sites in primary miRNA. Nucleic Acids Res. 42, 12224-12236.
Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R.W., Steward, R. and Chen, X. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science, 307, 932-935.
Yu, B., Bi, L., Zhai, J., Agarwal, M., Li, S., Wu, Q., Ding, S.W., Meyers, B.C., Vaucheret, H. and Chen, X. (2010) siRNAs compete with miRNAs for methylation by HEN1 in Arabidopsis. Nucleic Acids Res. 38, 5844-5850.