Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

FRIGIDA establishes a local chromosomal environment for FLOWERING LOCUS C mRNA production

Nature Plants volume 4, pages 836–846 (2018)Cite this article

Subjects

Abstract

FRIGIDA (FRI) upregulates the expression of the potent floral repressor FLOWERING LOCUS C (FLC) to confer the winter-annual growth habit in Arabidopsis thaliana: accelerated transition to flowering after prolonged cold exposure (vernalization). Here, we show that FRI, histone acetyltransferases, the histone methyltransferase COMPASS-like and other chromatin modifiers are part of a FRI-containing supercomplex enriched in a region around the FLC transcription start site (TSS) to promote its expression. Several FRI partners are also enriched in a 3’ region flanking FLC and, together with FRI, they function to increase the frequency of physical association of the region around TSS with the 3’ region and promote the expression of both sense FLC and antisense non-coding RNAs. Our results show that the FRI supercomplex establishes a local chromosomal environment at FLC with active chromatin modifications and topology to promote transcriptional activation, fast elongation and efficient pre-messenger RNA splicing, leading to a high-level production of FLC mRNAs.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: COMPASS-like forms a complex with FRIc and mediates its binding to FLC chromatin.
Fig. 2: Functional association of COMPASS-like with SWR1c at the FLC locus.
Fig. 3: HAM1 and HAM2 mediates FRI-dependent FLC upregulation.
Fig. 4: FRI interacts with UBC1 and functions to promote its enrichment across the FLC locus.
Fig. 5: Analysis of the roles of FRI and WDR5a in transcription initiation and elongation at FLC.
Fig. 6: Analysis of the binding of FRI partners to the region downstream of FLC TTS and 5’ to 3’ gene looping.

Similar content being viewed by others

Data availability

All relevant data are available from the corresponding author upon reasonable request.

References

  1. Amasino, R. Seasonal and developmental timing of flowering. Plant J. 61, 1001–1013 (2010).

    Article  CAS  PubMed  Google Scholar 

  2. Michaels, S. D., He, Y., Scortecci, K. C. & Amasino, R. M. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 10102–10107 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Johanson, U. et al. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347 (2000).

    Article  CAS  PubMed  Google Scholar 

  4. Choi, K. et al. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23, 289–303 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Michaels, S. D., Bezerra, I. C. & Amasino, R. M. FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc. Natl Acad. Sci. USA 101, 3281–3285 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Schmitz, R. J., Hong, L., Michaels, S. & Amasino, R. M. FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132, 5471–5478 (2005).

    Article  CAS  PubMed  Google Scholar 

  7. Kim, S. Y. & Michaels, S. D. SUPPRESSOR OF FRI 4 encodes a nuclear-localized protein that is required for delayed flowering in winter-annual Arabidopsis. Development 133, 4699–4707 (2006).

    Article  CAS  PubMed  Google Scholar 

  8. Deal, R. B., Topp, C. N., McKinney, E. C. & Meagher, R. B. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell 19, 74–83 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Jiang, D., Gu, X. & He, Y. Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21, 1733–1746 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kim, S. Y. et al. Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17, 3301–3310 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Zhao, Z., Yu, Y., Meyer, D., Wu, C. & Shen, W. H. Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat. Cell Biol. 7, 1256–1260 (2005).

    Article  CAS  PubMed  Google Scholar 

  12. Cao, Y., Dai, Y., Cui, S. & Ma, L. Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20, 2586–2602 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gu, X., Jiang, D., Wang, Y., Bachmair, A. & He, Y. Repression of the floral transition via histone H2B monoubiquitination. Plant J. 57, 522–533 (2009).

    Article  CAS  PubMed  Google Scholar 

  14. Kim, S., Choi, K., Park, C., Hwang, H. J. & Lee, I. SUPPRESSOR OF FRIGIDA 4, encoding a C2H2-Type zinc finger protein, represses flowering by transcriptional activation of Arabidopsis FLOWERING LOCUS C. Plant Cell 18, 2985–2998 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Oh, S., Zhang, H., Ludwig, P. & van Nocker, S. A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family. Plant Cell 16, 2940–2953 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. He, Y., Doyle, M. R. & Amasino, R. M. PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 18, 2774–2784 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bezerra, I. C., Michaels, S. D., Schomburg, F. M. & Amasino, R. M. Lesions in the mRNA cap-binding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA-mediated delayed flowering in Arabidopsis. Plant J. 40, 112–119 (2004).

    Article  CAS  PubMed  Google Scholar 

  18. Choi, K. et al. Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development. Development 134, 1931–1941 (2007).

    Article  CAS  PubMed  Google Scholar 

  19. Xu, L. et al. The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J. 57, 279–288 (2008).

    Article  CAS  PubMed  Google Scholar 

  20. Geraldo, N., Baurle, I., Kidou, S., Hu, X. & Dean, C. FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol. 150, 1611–1618 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Jiang, D., Kong, N. C., Gu, X., Li, Z. & He, Y. Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet. 7, e1001330 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ding, Y. et al. ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes. PLoS Genet. 8, e1003111 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Ko, J. H. et al. Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO J. 29, 3208–3215 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Calero, G. et al. Structural basis of m7GpppG binding to the nuclear cap-binding protein complex. Nat. Struct. Biol. 9, 912–917 (2002).

    Article  CAS  PubMed  Google Scholar 

  25. Li, Z. et al. Coupling of histone methylation and RNA processing by the nuclear mRNA cap-binding complex. Nat. Plants 2, 16015 (2016).

    Article  CAS  PubMed  Google Scholar 

  26. Swiezewski, S., Liu, F., Magusin, A. & Dean, C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462, 799–802 (2009).

    Article  CAS  PubMed  Google Scholar 

  27. Rosa, S., Duncan, S. & Dean, C. Mutually exclusive sense-antisense transcription at FLC facilitates environmentally induced gene repression. Nat. Commun. 7, 13031 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Helliwell, C. A., Robertson, M., Finnegan, E. J., Buzas, D. M. & Dennis, E. S. Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS ONE. 6, e21513 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Liu, C. et al. Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res. 26, 1057–1068 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Crevillen, P., Sonmez, C., Wu, Z. & Dean, C. A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J. 32, 140–148 (2013).

    Article  CAS  PubMed  Google Scholar 

  31. Kim, D. H. & Sung, S. Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Dev. Cell. 40, 302–312 e304 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Jegu, T. et al. The BAF60 subunit of the SWI/SNF chromatin-remodeling complex directly controls the formation of a gene loop at FLOWERING LOCUS C in Arabidopsis. Plant Cell 26, 538–551 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lu, P. Y., Levesque, N. & Kobor, M. S. NuA4 and SWR1-C: two chromatin-modifying complexes with overlapping functions and components. Biochem. Cell. Biol. 87, 799–815 (2009).

    Article  CAS  PubMed  Google Scholar 

  34. Szerlong, H. et al. The HSA domain binds nuclear actin-related proteins to regulate chromatin-remodeling ATPases. Nat. Struct. Mol. Biol. 15, 469–476 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Han, S. K., Song, J. D., Noh, Y. S. & Noh, B. Role of plant CBP/p300-like genes in the regulation of flowering time. Plant J. 49, 103–114 (2007).

    Article  CAS  PubMed  Google Scholar 

  36. Deng, W. et al. Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis. Plant Physiol. 143, 1660–1668 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Xiao, J. et al. Requirement of histone acetyltransferases HAM1 and HAM2 for epigenetic modification of FLC in regulating flowering in Arabidopsis. J. Plant. Physiol. 170, 444–451 (2013).

    Article  CAS  PubMed  Google Scholar 

  38. Fuchs, G., Hollander, D., Voichek, Y., Ast, G. & Oren, M. Cotranscriptional histone H2B monoubiquitylation is tightly coupled with RNA polymerase II elongation rate. Genome Res. 24, 1572–1583 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lolas, I. B. et al. The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and genetically interacts with HUB1/2. Plant J. 61, 686–697 (2010).

    Article  CAS  PubMed  Google Scholar 

  40. Wu, Z. et al. Quantitative regulation of FLC via coordinated transcriptional initiation and elongation. Proc. Natl Acad. Sci. USA 113, 218–223 (2016).

    Article  CAS  PubMed  Google Scholar 

  41. Ratcliffe, O. J., Kumimoto, R. W., Wong, B. J. & Riechmann, J. L. Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15, 1159–1169 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Csorba, T., Questa, J. I., Sun, Q. & Dean, C. Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc. Natl Acad. Sci. USA 111, 16160–16165 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bouche, F., Woods, D. P. & Amasino, R. M. Winter memory throughout the plant kingdom: different paths to flowering. Plant Physiol. 173, 27–35 (2017).

    Article  CAS  PubMed  Google Scholar 

  44. Schubert, V. et al. Sister chromatids are often incompletely aligned in meristematic and endopolyploid interphase nuclei of Arabidopsis thaliana. Genetics 172, 467–475 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Hampsey, M., Singh, B. N., Ansari, A., Laine, J. P. & Krishnamurthy, S. Control of eukaryotic gene expression: gene loops and transcriptional memory. Adv. Enzyme. Regul. 51, 118–125 (2011).

    Article  CAS  PubMed  Google Scholar 

  46. Michaels, S. D. & Amasino, R. M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949–956 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lee, I., Michaels, S. D., Masshardt, A. S. & Amasino, R. M. The late-flowering phenotype of FRIGIDA and luminidependens is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6, 903–909 (1994).

    Article  CAS  Google Scholar 

  48. Papp, I., Mur, L. A., Dalmadi, A., Dulai, S. & Koncz, C. A mutation in the CAP BINDING PROTEIN 20 gene confers drought tolerance to Arabidopsis. Plant Mol. Biol. 55, 679–686 (2004).

    Article  CAS  PubMed  Google Scholar 

  49. Wang, Y., Gu, X., Yuan, W., Schmitz, R. J. & He, Y. Photoperiodic control of the floral transition through a distinct polycomb repressive complex. Dev. Cell. 28, 727–736 (2014).

    Article  CAS  PubMed  Google Scholar 

  50. Louwers, M., Splinter, E., van Driel, R., de Laat, W. & Stam, M. Studying physical chromatin interactions in plants using Chromosome Conformation Capture (3C). Nat. Protoc. 4, 1216–1229 (2009).

    Article  CAS  PubMed  Google Scholar 

  51. Hagege, H. et al. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc. 2, 1722–1733 (2007).

    Article  CAS  PubMed  Google Scholar 

  52. Gu, X. et al. Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues. Nat. Commun. 4, 1947 (2013).

    Article  PubMed  CAS  Google Scholar 

  53. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K. & Scheible, W. R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5–17 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408 (2001).

    Article  CAS  PubMed  Google Scholar 

  55. Hajdukiewicz, P., Svab, Z. & Maliga, P. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989–994 (1994).

    Article  CAS  PubMed  Google Scholar 

  56. Karimi, M., De Meyer, B. & Hilson, P. Modular cloning in plant cells. Trends. Plant. Sci. 10, 103–105 (2005).

    Article  CAS  PubMed  Google Scholar 

  57. Curtis, M. D. & Grossniklaus, U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are very grateful to R. M. Amasino for graciously providing the FRI-Col, FRI flc-2 and FRI efs seeds. We thank A. Jarmolowski for supplying the cbp20 seeds and Y. Ou and F. Huang for assistance. This work was supported in part by the National Natural Science Foundation of China (grant no. 31721001), the National Key Research and Development Program of China (grant no. 2017YFA0503803) and the Chinese Academy of Sciences (grant no. XDPB0404).

Author information

Author notes

  1. Danhua Jiang

    Present address: Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

  2. These authors contributed equally to this work: Zicong Li, Danhua Jiang.

Authors and Affiliations

  1. Shanghai Center for Plant Stress Biology & National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS), Shanghai, China

    Zicong Li & Yuehui He

  2. Department of Biological Sciences, National University of Singapore, Singapore, Singapore

    Danhua Jiang & Yuehui He

Authors
  1. Zicong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Danhua Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuehui He
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y.H. conceived and supervised the research. Z.L. and D.J. conducted the experiments. Z.L., D.J. and Y.H. analysed the data. Y.H. and Z.L. wrote the paper.

Corresponding author

Correspondence to Yuehui He.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figures 1–12 and Supplementary Table 1.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Z., Jiang, D. & He, Y. FRIGIDA establishes a local chromosomal environment for FLOWERING LOCUS C mRNA production. Nature Plants 4, 836–846 (2018). https://doi.org/10.1038/s41477-018-0250-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-018-0250-6

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing