Core clock genes adjust growth cessation time to day-night switches in poplar.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
27 Feb 2024
27 Feb 2024
Historique:
received:
14
08
2023
accepted:
14
02
2024
medline:
28
2
2024
pubmed:
28
2
2024
entrez:
27
2
2024
Statut:
epublish
Résumé
Poplar trees use photoperiod as a precise seasonal indicator, synchronizing plant phenology with the environment. Daylength cue determines FLOWERING LOCUS T 2 (FT2) daily expression, crucial for shoot apex development and establishment of the annual growing period. However, limited evidence exists for the molecular factors controlling FT2 transcription and the conservation with the photoperiodic control of Arabidopsis flowering. We demonstrate that FT2 expression mediates growth cessation response quantitatively, and we provide a minimal data-driven model linking core clock genes to FT2 daily levels. GIGANTEA (GI) emerges as a critical inducer of the FT2 activation window, time-bound by TIMING OF CAB EXPRESSION (TOC1) and LATE ELONGATED HYPOCOTYL (LHY2) repressions. CRISPR/Cas9 loss-of-function lines validate these roles, identifying TOC1 as a long-sought FT2 repressor. Additionally, model simulations predict that FT2 downregulation upon daylength shortening results from a progressive narrowing of this activation window, driven by the phase shift observed in the preceding clock genes. This circadian-mediated mechanism enables poplar to exploit FT2 levels as an accurate daylength-meter.
Identifiants
pubmed: 38413620
doi: 10.1038/s41467-024-46081-6
pii: 10.1038/s41467-024-46081-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1784Subventions
Organisme : Comunidad de Madrid
ID : 2021-5A/BIO-20952
Informations de copyright
© 2024. The Author(s).
Références
Singh, R. K., Svystun, T., AlDahmash, B., Jönsson, A. M. & Bhalerao, R. P. Photoperiod‐ and temperature‐mediated control of phenology in trees—a molecular perspective. N. Phytolog 213, 511–524 (2017).
doi: 10.1111/nph.14346
Ding, J. & Nilsson, O. Molecular regulation of phenology in trees — because the seasons they are a-changin. Curr. Opin. Plant Biol. 29, 73–79 (2016).
doi: 10.1016/j.pbi.2015.11.007
pubmed: 26748352
Triozzi, P. M. et al. Photoperiodic Regulation of Shoot Apical Growth in Poplar. Front. Plant Sci. 9, https://doi.org/10.3389/fpls.2018.01030 (2018).
Ding, J. et al. “GIGANTEA- like genes control seasonal growth cessation in Populus,”. N. Phytolog 218, 1491–1503 (2018).
doi: 10.1111/nph.15087
Ramos-Sánchez, J. M. et al. LHY2 Integrates Night-Length Information to Determine Timing of Poplar Photoperiodic Growth. Curr. Biol. 29, 2402–2406.e4 (2019).
doi: 10.1016/j.cub.2019.06.003
pubmed: 31257141
Gómez-Soto, D., Allona, I. & Perales, M. FLOWERING LOCUS T2 Promotes Shoot Apex Development and Restricts Internode Elongation via the 13-Hydroxylation Gibberellin Biosynthesis Pathway in Poplar. Front. Plant Sci. 12, https://doi.org/10.3389/fpls.2021.814195 (2022).
Ibáñez, C. et al. Circadian Clock Components Regulate Entry and Affect Exit of Seasonal Dormancy as Well as Winter Hardiness in Populus Trees. Plant Physiol. 153, 1823–1833 (2010).
doi: 10.1104/pp.110.158220
pubmed: 20530613
pmcid: 2923903
Yanovsky, M. J. & Kay, S. A. Molecular basis of seasonal time measurement in Arabidopsis. Nature 419, 308–312 (2002).
doi: 10.1038/nature00996
pubmed: 12239570
Gendron, J. M. et al. Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc. Natl Acad. Sci. 109, 3167–3172 (2012).
doi: 10.1073/pnas.1200355109
pubmed: 22315425
pmcid: 3286946
Yan, J. et al. TOC1 clock protein phosphorylation controls complex formation with NF‐YB/C to repress hypocotyl growth. EMBO J. 40, https://doi.org/10.15252/embj.2021108684 (2021).
Tiwari, S. B. et al. The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis ‐element. N. Phytolog. 187, 57–66 (2010).
doi: 10.1111/j.1469-8137.2010.03251.x
Wenkel, S. et al. CONSTANS and the CCAAT Box Binding Complex Share a Functionally Important Domain and Interact to Regulate Flowering of Arabidopsis. Plant Cell 18, 2971–2984 (2006).
doi: 10.1105/tpc.106.043299
pubmed: 17138697
pmcid: 1693937
Cao, S. et al. A Distal CCAAT /NUCLEAR FACTOR Y Complex Promotes Chromatin Looping at the FLOWERING LOCUS T Promoter and Regulates the Timing of Flowering in Arabidopsis. Plant Cell 26, 1009–1017 (2014).
doi: 10.1105/tpc.113.120352
pubmed: 24610724
pmcid: 4001365
Gnesutta, N. et al. CONSTANS Imparts DNA Sequence Specificity to the Histone Fold NF-YB/NF-YC Dimer. Plant Cell 29, 1516–1532 (2017).
doi: 10.1105/tpc.16.00864
pubmed: 28526714
pmcid: 5502446
Hayama, R. et al. PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length. EMBO J. 36, 904–918 (2017).
doi: 10.15252/embj.201693907
pubmed: 28270524
pmcid: 5376961
Kubota, A. et al. TCP4-dependent induction of CONSTANS transcription requires GIGANTEA in photoperiodic flowering in Arabidopsis. PLoS Genet 13, e1006856 (2017).
doi: 10.1371/journal.pgen.1006856
pubmed: 28628608
pmcid: 5495492
Sawa, M., Nusinow, D. A., Kay, S. A. & Imaizumi, T. FKF1 and GIGANTEA Complex Formation Is Required for Day-Length Measurement in Arabidopsis. Science (1979) 318, 261–265 (2007).
Song, Y. H. et al. Distinct roles of FKF1, GIGANTEA, and ZEITLUPE proteins in the regulation of CONSTANS stability in Arabidopsis photoperiodic flowering. Proc. Natl Acad. Sci. 111, 17672–17677 (2014).
doi: 10.1073/pnas.1415375111
pubmed: 25422419
pmcid: 4267339
Sawa, M. & Kay, S. A. GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc. Natl Acad. Sci. 108, 11698–11703 (2011).
doi: 10.1073/pnas.1106771108
pubmed: 21709243
pmcid: 3136272
Valverde, F. et al. Photoreceptor Regulation of CONSTANS Protein in Photoperiodic Flowering. Science (1979) 303, 1003–1006 (2004).
Böhlenius, H. et al. CO/FT Regulatory Module Controls Timing of Flowering and Seasonal Growth Cessation in Trees. Science (1979) 312, 1040–1043 (2006).
Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. & Araki, T. A Pair of Related Genes with Antagonistic Roles in Mediating Flowering Signals. Science (1979) 286, 1960–1962 (1999).
Onouchi, H., Igeño, M. I., Périlleux, C., Graves, K. & Coupland, G. Mutagenesis of Plants Overexpressing CONSTANS Demonstrates Novel Interactions among Arabidopsis Flowering-Time Genes. Plant Cell 12, 885–900 (2000).
doi: 10.1105/tpc.12.6.885
pubmed: 10852935
pmcid: 149091
Hsu, C.-Y. et al. Overexpression of Constans Homologs CO1 and CO2 Fails to Alter Normal Reproductive Onset and Fall Bud Set in Woody Perennial Poplar. PLoS One 7, e45448 (2012).
doi: 10.1371/journal.pone.0045448
pubmed: 23029015
pmcid: 3446887
Pokhilko, A. et al. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol. Syst. Biol. 8, https://doi.org/10.1038/msb.2012.6 (2012).
Seaton, D. D. et al. Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature. Mol. Syst. Biol. 11 https://doi.org/10.15252/msb.20145766 (2015).
Mockler, T. C. et al. The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis. Cold Spring Harb. Symp. Quant. Biol. 72, 353–363 (2007).
doi: 10.1101/sqb.2007.72.006
pubmed: 18419293
Izawa, T. et al. Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev. 16, 2006–2020 (2002).
doi: 10.1101/gad.999202
pubmed: 12154129
pmcid: 186415
André, D. et al. FLOWERING LOCUS T paralogs control the annual growth cycle in Populus trees. Curr. Biol. 32, 2988–2996.e4 (2022).
doi: 10.1016/j.cub.2022.05.023
pubmed: 35660141
Niwa, Y. et al. Genetic Linkages of the Circadian Clock-Associated Genes, TOC1, CCA1 and LHY, in the Photoperiodic Control of Flowering Time in Arabidopsis thaliana. Plant Cell Physiol. 48, 925–937 (2007).
doi: 10.1093/pcp/pcm067
pubmed: 17540692
Nohales, M. A. et al. Multi-level Modulation of Light Signaling by GIGANTEA Regulates Both the Output and Pace of the Circadian Clock. Dev. Cell 49, 840–851.e8 (2019).
doi: 10.1016/j.devcel.2019.04.030
pubmed: 31105011
pmcid: 6597437
Park, M.-J., Kwon, Y.-J., Gil, K.-E. & Park, C.-M. LATE ELONGATED HYPOCOTYL regulates photoperiodic flowering via the circadian clock in Arabidopsis. BMC Plant Biol. 16, 114 (2016).
doi: 10.1186/s12870-016-0810-8
pubmed: 27207270
pmcid: 4875590
Jacobs, T. B., LaFayette, P. R., Schmitz, R. J. & Parrott, W. A. Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol. 15, 16 (2015).
doi: 10.1186/s12896-015-0131-2
pubmed: 25879861
pmcid: 4365529
Ramos-Sánchez, J. M. et al. Real-time monitoring of PtaHMGB activity in poplar transactivation assays. Plant Methods 13, 50 (2017).
doi: 10.1186/s13007-017-0199-x
pubmed: 28638438
pmcid: 5472981
Rohde, A. et al. Bud set in poplar—genetic dissection of a complex trait in natural and hybrid populations. N. Phytolog 189, 106–121 (2011).
doi: 10.1111/j.1469-8137.2010.03469.x
Livak, K. J. & Schmittgen, T. D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 25, 402–408 (2001).
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Pettengill, E. A., Parmentier-Line, C. & Coleman, G. D. Evaluation of qPCR reference genes in two genotypes of Populus for use in photoperiod and low-temperature studies. BMC Res. Notes 5, 366 (2012).
doi: 10.1186/1756-0500-5-366
pubmed: 22824181
pmcid: 3479007
Wang, J. et al. A major locus controls local adaptation and adaptive life history variation in a perennial plant. Genome Biol. 19, 72 (2018).
doi: 10.1186/s13059-018-1444-y
pubmed: 29866176
pmcid: 5985590