A photoregulatory mechanism of the circadian clock in Arabidopsis.
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
received:
09
03
2021
accepted:
03
08
2021
entrez:
15
10
2021
pubmed:
16
10
2021
medline:
6
11
2021
Statut:
ppublish
Résumé
Cryptochromes (CRYs) are photoreceptors that mediate light regulation of the circadian clock in plants and animals. Here we show that CRYs mediate blue-light regulation of N
Identifiants
pubmed: 34650267
doi: 10.1038/s41477-021-01002-z
pii: 10.1038/s41477-021-01002-z
doi:
Substances chimiques
Cryptochromes
0
Photoreceptors, Plant
0
N-methyladenosine
CLE6G00625
Adenosine
K72T3FS567
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1397-1408Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM056265
Pays : United States
Commentaires et corrections
Type : CommentIn
Type : ErratumIn
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Sanchez, S. E., Rugnone, M. L. & Kay, S. A. Light perception: a matter of time. Mol. Plant 13, 363–385 (2020).
doi: 10.1016/j.molp.2020.02.006
pubmed: 32068156
Patke, A., Young, M. W. & Axelrod, S. Molecular mechanisms and physiological importance of circadian rhythms. Nat. Rev. Mol. Cell Biol. 21, 67–84 (2020).
doi: 10.1038/s41580-019-0179-2
pubmed: 31768006
Webb, A. A. R., Seki, M., Satake, A. & Caldana, C. Continuous dynamic adjustment of the plant circadian oscillator. Nat. Commun. 10, 550 (2019).
pubmed: 30710080
pmcid: 6358598
doi: 10.1038/s41467-019-08398-5
Wang, Q. & Lin, C. Mechanisms of cryptochrome-mediated photoresponses in plants. Annu. Rev. Plant Biol. 71, 103–129 (2020).
pubmed: 32169020
pmcid: 7428154
doi: 10.1146/annurev-arplant-050718-100300
Cashmore, A. R. Cryptochromes: enabling plants and animals to determine circadian time. Cell 114, 537–543 (2003).
pubmed: 13678578
Sancar, A. Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. Annu. Rev. Biochem. 69, 31–67 (2000).
doi: 10.1146/annurev.biochem.69.1.31
pubmed: 10966452
Bailey-Serres, J., Zhai, J. & Seki, M. The dynamic kaleidoscope of RNA biology in plants. Plant Physiol. 182, 1–9 (2020).
pubmed: 31908318
pmcid: 6945830
doi: 10.1104/pp.19.01558
Parker, M. T. et al. Nanopore direct RNA sequencing maps the complexity of Arabidopsis mRNA processing and m(6)A modification. eLife; https://doi.org/10.7554/eLife.49658 (2020).
Wang, C. Y., Yeh, J. K., Shie, S. S., Hsieh, I. C. & Wen, M. S. Circadian rhythm of RNA N6-methyladenosine and the role of cryptochrome. Biochem. Biophys. Res. Commun. 465, 88–94 (2015).
doi: 10.1016/j.bbrc.2015.07.135
pubmed: 26239657
Fustin, J. M. et al. RNA-methylation-dependent RNA processing controls the speed of the circadian clock. Cell 155, 793–806 (2013).
pubmed: 24209618
doi: 10.1016/j.cell.2013.10.026
Anderson, S. J. et al. N
pubmed: 30380407
doi: 10.1016/j.celrep.2018.10.020
Wang, X. et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 505, 117–120 (2014).
pubmed: 24284625
doi: 10.1038/nature12730
Zaccara, S., Ries, R. J. & Jaffrey, S. R. Reading, writing and erasing mRNA methylation. Nat. Rev. Mol. Cell Biol. 20, 608–624 (2019).
pubmed: 31520073
doi: 10.1038/s41580-019-0168-5
Shen, L., Liang, Z., Wong, C. E. & Yu, H. Messenger RNA modifications in plants. Trends Plant Sci. 24, 328–341 (2019).
doi: 10.1016/j.tplants.2019.01.005
pubmed: 30745055
Zhao, B. S., Roundtree, I. A. & He, C. Post-transcriptional gene regulation by mRNA modifications. Nat. Rev. Mol. Cell Biol. 18, 31–42 (2017).
doi: 10.1038/nrm.2016.132
pubmed: 27808276
Dominissini, D., Moshitch-Moshkovitz, S., Salmon-Divon, M., Amariglio, N. & Rechavi, G. Transcriptome-wide mapping of N(6)-methyladenosine by m(6)A-seq based on immunocapturing and massively parallel sequencing. Nat. Protoc. 8, 176–189 (2013).
doi: 10.1038/nprot.2012.148
pubmed: 23288318
Wang, Z. Y. & Tobin, E. M. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207–1217 (1998).
doi: 10.1016/S0092-8674(00)81464-6
pubmed: 9657153
Liu, Q. et al. Molecular basis for blue light-dependent phosphorylation of Arabidopsis cryptochrome 2. Nat. Commun. 8, 15234 (2017).
pubmed: 28492234
pmcid: 5437284
doi: 10.1038/ncomms15234
Arribas-Hernandez, L. & Brodersen, P. Occurrence and functions of m(6)A and other covalent modifications in plant mRNA. Plant Physiol. 182, 79–96 (2020).
doi: 10.1104/pp.19.01156
pubmed: 31748418
Ruzicka, K. et al. Identification of factors required for m
pubmed: 28503769
pmcid: 5488176
doi: 10.1111/nph.14586
Zhong, S. et al. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. Plant Cell 20, 1278–1288 (2008).
pubmed: 18505803
pmcid: 2438467
doi: 10.1105/tpc.108.058883
Chen, Y. et al. Regulation of Arabidopsis photoreceptor CRY2 by two distinct E3 ubiquitin ligases. Nat. Commun. 12, 2155 (2021).
pubmed: 33846325
pmcid: 8042123
doi: 10.1038/s41467-021-22410-x
Yu, X. et al. Arabidopsis cryptochrome 2 completes its posttranslational life cycle in the nucleus. Plant Cell 19, 3146–3156 (2007).
pubmed: 17965271
pmcid: 2174722
doi: 10.1105/tpc.107.053017
Liu, Q. et al. Photooligomerization determines photosensitivity and photoreactivity of plant cryptochromes. Mol. Plant 13, 398–413 (2020).
pubmed: 31953223
doi: 10.1016/j.molp.2020.01.002
Liu, H. et al. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322, 1535–1539 (2008).
pubmed: 18988809
doi: 10.1126/science.1163927
Wang, Q. et al. Photoactivation and inactivation of Arabidopsis cryptochrome 2. Science 354, 343–347 (2016).
pubmed: 27846570
pmcid: 6180212
doi: 10.1126/science.aaf9030
Yu, X. et al. Formation of nuclear bodies of Arabidopsis CRY2 in response to blue light is associated with its blue light-dependent degradation. Plant Cell 21, 118–130 (2009).
pubmed: 19141709
pmcid: 2648085
doi: 10.1105/tpc.108.061663
Mas, P., Devlin, P. F., Panda, S. & Kay, S. A. Functional interaction of phytochrome B and cryptochrome 2. Nature 408, 207–211 (2000).
pubmed: 11089975
doi: 10.1038/35041583
Sabari, B. R. et al. Coactivator condensation at super-enhancers links phase separation and gene control. Science https://doi.org/10.1126/science.aar3958 (2018).
Bracha, D. et al. Mapping local and global liquid phase behavior in living cells using photo-oligomerizable seeds. Cell 175, 1467–1480 e1413 (2018).
pubmed: 30500534
pmcid: 6724719
doi: 10.1016/j.cell.2018.10.048
Shin, Y. et al. Spatiotemporal control of intracellular phase transitions using light-activated optodroplets. Cell 168, 159–171 e114 (2017).
doi: 10.1016/j.cell.2016.11.054
pubmed: 28041848
Dignon, G. L., Best, R. B. & Mittal, J. Biomolecular phase separation: from molecular driving forces to macroscopic properties. Annu. Rev. Phys. Chem. 71, 53–75 (2020).
pubmed: 32312191
pmcid: 7469089
doi: 10.1146/annurev-physchem-071819-113553
Alberti, S., Gladfelter, A. & Mittag, T. Considerations and challenges in studying liquid–liquid phase separation and biomolecular condensates. Cell 176, 419–434 (2019).
pubmed: 30682370
pmcid: 6445271
doi: 10.1016/j.cell.2018.12.035
Wang, Q. et al. The blue light-dependent phosphorylation of the CCE domain determines the photosensitivity of Arabidopsis CRY2. Mol. Plant 8, 631–643 (2015).
doi: 10.1016/j.molp.2015.03.005
pubmed: 25792146
Shalitin, D. et al. Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature 417, 763–767 (2002).
doi: 10.1038/nature00815
pubmed: 12066190
Devlin, P. F. & Kay, S. A. Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell 12, 2499–2510 (2000).
pubmed: 11148293
pmcid: 102233
doi: 10.1105/tpc.12.12.2499
Somers, D. E., Devlin, P. F. & Kay, S. A. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282, 1488–1490 (1998).
doi: 10.1126/science.282.5393.1488
pubmed: 9822379
Bodi, Z. et al. Adenosine methylation in Arabidopsis mRNA is associated with the 3ʹ end and reduced levels cause developmental defects. Front. Plant Sci. 3, 48 (2012).
pubmed: 22639649
pmcid: 3355605
doi: 10.3389/fpls.2012.00048
Guo, H., Yang, H., Mockler, T. C. & Lin, C. Regulation of flowering time by Arabidopsis photoreceptors. Science 279, 1360–1363 (1998).
doi: 10.1126/science.279.5355.1360
pubmed: 9478898
Legris, M., Ince, Y. C. & Fankhauser, C. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat. Commun. 10, 5219 (2019).
pubmed: 31745087
pmcid: 6864062
doi: 10.1038/s41467-019-13045-0
Leivar, P. & Quail, P. H. PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16, 19–28 (2011).
doi: 10.1016/j.tplants.2010.08.003
pubmed: 20833098
Bhat, S. S. et al. mRNA adenosine methylase (MTA) deposits m(6)A on pri-miRNAs to modulate miRNA biogenesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 117, 21785–21795 (2020).
pubmed: 32817553
pmcid: 7474595
doi: 10.1073/pnas.2003733117
Aschoff, J. Exogenous and endogenous components in circadian rhythms. Cold Spring Harb. Symp. Quant. Biol. 25, 11–28 (1960).
doi: 10.1101/SQB.1960.025.01.004
pubmed: 13684695
Jang, G. J., Yang, J. Y., Hsieh, H. L. & Wu, S. H. Processing bodies control the selective translation for optimal development of Arabidopsis young seedlings. Proc. Natl Acad. Sci. USA 116, 6451–6456 (2019).
pubmed: 30850529
pmcid: 6442596
doi: 10.1073/pnas.1900084116
Godoy Herz, M. A. et al. Light regulates plant alternative splicing through the control of transcriptional elongation. Mol. Cell 73, 1066–1074 e1063 (2019).
doi: 10.1016/j.molcel.2018.12.005
pubmed: 30661982
Wu, S. H. Gene expression regulation in photomorphogenesis from the perspective of the central dogma. Annu. Rev. Plant Biol. 65, 311–333 (2014).
doi: 10.1146/annurev-arplant-050213-040337
pubmed: 24779996
Paik, I., Yang, S. & Choi, G. Phytochrome regulates translation of mRNA in the cytosol. Proc. Natl Acad. Sci. USA 109, 1335–1340 (2012).
pubmed: 22232680
pmcid: 3268310
doi: 10.1073/pnas.1109683109
Juntawong, P. & Bailey-Serres, J. Dynamic light regulation of translation status in Arabidopsis thaliana. Front. Plant Sci. 3, 66 (2012).
pubmed: 22645595
pmcid: 3355768
doi: 10.3389/fpls.2012.00066
Wang, X. et al. SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 24, 3278–3295 (2012).
pubmed: 22942380
pmcid: 3462631
doi: 10.1105/tpc.112.100081
Mockler, T. C., Guo, H., Yang, H., Duong, H. & Lin, C. Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development 126, 2073–2082 (1999).
pubmed: 10207133
doi: 10.1242/dev.126.10.2073
Harmoko, R. et al. RNA-dependent RNA polymerase 6 is required for efficient hpRNA-induced gene silencing in plants. Mol. Cells 35, 202–209 (2013).
pubmed: 23456296
pmcid: 3887914
doi: 10.1007/s10059-013-2203-2
Clough, S. J. Floral dip: agrobacterium-mediated germ line transformation. Methods Mol. Biol. 286, 91–102 (2005).
pubmed: 15310915
Wu, F. H. et al. Tape-Arabidopsis Sandwich – a simpler Arabidopsis protoplast isolation method. Plant Methods 5, 16 (2009).
pubmed: 19930690
pmcid: 2794253
doi: 10.1186/1746-4811-5-16
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Fang, X. et al. Arabidopsis FLL2 promotes liquid–liquid phase separation of polyadenylation complexes. Nature 569, 265–269 (2019).
pubmed: 31043738
pmcid: 6625965
doi: 10.1038/s41586-019-1165-8
Rapsomaniki, M. A. et al. easyFRAP: an interactive, easy-to-use tool for qualitative and quantitative analysis of FRAP data. Bioinformatics 28, 1800–1801 (2012).
pubmed: 22543368
doi: 10.1093/bioinformatics/bts241
Tseng, Q. et al. A new micropatterning method of soft substrates reveals that different tumorigenic signals can promote or reduce cell contraction levels. Lab Chip 11, 2231–2240 (2011).
pubmed: 21523273
doi: 10.1039/c0lc00641f
Lund, F. W. et al. SpatTrack: an imaging toolbox for analysis of vesicle motility and distribution in living cells. Traffic 15, 1406–1429 (2014).
doi: 10.1111/tra.12228
pubmed: 25243614
Ries, R. J. et al. m(6)A enhances the phase separation potential of mRNA. Nature 571, 424–428 (2019).
pubmed: 31292544
pmcid: 6662915
doi: 10.1038/s41586-019-1374-1
Zielinski, T., Moore, A. M., Troup, E., Halliday, K. J. & Millar, A. J. Strengths and limitations of period estimation methods for circadian data. PLoS ONE 9, e96462 (2014).
pubmed: 24809473
pmcid: 4014635
doi: 10.1371/journal.pone.0096462
Moore, A., Zielinski, T. & Millar, A. J. in Plant Circadian Networks: Methods and Protocols (ed. Staiger, D.) 13–44 (Springer, 2014).
Hutchison, A. L. et al. Improved statistical methods enable greater sensitivity in rhythm detection for genome-wide data. PLoS Comput. Biol. 11, e1004094 (2015).
pubmed: 25793520
pmcid: 4368642
doi: 10.1371/journal.pcbi.1004094
Chantarachot, T. et al. DHH1/DDX6-like RNA helicases maintain ephemeral half-lives of stress-response mRNAs. Nat. Plants 6, 675–685 (2020).
pubmed: 32483330
doi: 10.1038/s41477-020-0681-8
Sorenson, R. S., Deshotel, M. J., Johnson, K., Adler, F. R. & Sieburth, L. E. Arabidopsis mRNA decay landscape arises from specialized RNA decay substrates, decapping-mediated feedback, and redundancy. Proc. Natl Acad. Sci. USA 115, E1485–E1494 (2018).
pubmed: 29386391
pmcid: 5816150
doi: 10.1073/pnas.1712312115
Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45 (2001).
pubmed: 11328886
pmcid: 55695
doi: 10.1093/nar/29.9.e45
Trcek, T., Larson, D. R., Moldon, A., Query, C. C. & Singer, R. H. Single-molecule mRNA decay measurements reveal promoter-regulated mRNA stability in yeast. Cell 147, 1484–1497 (2011).
pubmed: 22196726
pmcid: 3286490
doi: 10.1016/j.cell.2011.11.051
Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
pubmed: 23618408
pmcid: 4053844
doi: 10.1186/gb-2013-14-4-r36
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621–628 (2008).
pubmed: 18516045
doi: 10.1038/nmeth.1226
Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).
pubmed: 22383036
pmcid: 3334321
doi: 10.1038/nprot.2012.016
Luo, G. Z. et al. Unique features of the m6A methylome in Arabidopsis thaliana. Nat. Commun. 5, 5630 (2014).
doi: 10.1038/ncomms6630
pubmed: 25430002
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Yang, Y., Li, Y., Sancar, A. & Oztas, O. The circadian clock shapes the Arabidopsis transcriptome by regulating alternative splicing and alternative polyadenylation. J. Biol. Chem. 295, 7608–7619 (2020).
pubmed: 32303634
pmcid: 7261790
doi: 10.1074/jbc.RA120.013513
Romanowski, A., Schlaen, R. G., Perez-Santangelo, S., Mancini, E. & Yanovsky, M. J. Global transcriptome analysis reveals circadian control of splicing events in Arabidopsis thaliana. Plant J. 103, 889–902 (2020).
doi: 10.1111/tpj.14776
pubmed: 32314836
Li, S. et al. CGDB: a database of circadian genes in eukaryotes. Nucleic Acids Res. 45, D397–D403 (2017).
pubmed: 27789706
Covington, M. F., Maloof, J. N., Straume, M., Kay, S. A. & Harmer, S. L. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9, R130 (2008).
pubmed: 18710561
pmcid: 2575520
doi: 10.1186/gb-2008-9-8-r130