Plant Molecular Biology

, Volume 73, Issue 4–5, pp 493–505 | Cite as

FRIGIDA and related proteins have a conserved central domain and family specific N- and C- terminal regions that are functionally important

Article

Abstract

Arabidopsis accessions are either winter-annuals, which require cold winter temperatures for spring flowering, or rapid-cycling summer annuals. Typically, winter annual accessions have functional FRIGIDA (FRI) and FRIGIDA-LIKE 1 (FRL1) proteins that promote high expression of FLOWERING LOCUS C (FLC), which prevents flowering until after winter. In contrast, many rapid-cycling accessions have low FLC levels because FRI is inactive. Using biochemical, functional and bioinformatic approaches, we show that FRI and FRL1 contain a stable, central domain that is conserved across the FRI superfamily. This core domain is monomeric in solution and primarily α-helical. We analysed the ability of several FRI deletion constructs to function in Arabidopsis plants. Our findings suggest that the C-terminus, which is predicted to be disordered, is required for FRI to promote FLC expression and may mediate protein:protein interactions. The contribution of the FRI N-terminus appears to be limited, as constructs missing these residues retained significant activity when expressed at high levels. The important N- and C-terminal regions differ between members of the FRI superfamily and sequence analysis identified five FRI families with distinct expression patterns in Arabidopsis, suggesting the families have separate biological roles.

Keywords

FRIGIDA FRIGIDA-LIKE 1 FLC Flowering Vernalization Arabidopsis 

Supplementary material

11103_2010_9635_MOESM1_ESM.pdf (1.4 mb)
Supplementary material 1 (PDF 1427 kb)

References

  1. Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664CrossRefPubMedGoogle Scholar
  2. Choi J, Hyun Y, Kang M-J, In Yun H, Yun J-Y, Lister C, Dean C, Amasino RM, Noh B, Noh Y-S, Choi Y (2009) Resetting and regulation of FLOWERING LOCUS C expression during Arabidopsis reproductive development. Plant J 57:918–931CrossRefPubMedGoogle Scholar
  3. Cohen SL, Ferre-D’Amare AR, Burley SK, Chait BT (1995) Probing the solution structure of the DNA-binding protein Max by a combination of proteolysis and mass spectrometry. Protein Sci 4:1088–1099PubMedCrossRefGoogle Scholar
  4. Cooke C, Alwine JC (1996) The cap and the 3’ splice site similarly affect polyadenylation efficiency. Mol Cell Biol 16:2579–2584PubMedGoogle Scholar
  5. De Lucia F, Crevillen P, Jones AME, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105:16831–16836CrossRefPubMedGoogle Scholar
  6. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6:197–208CrossRefPubMedGoogle Scholar
  7. Flaherty SM, Fortes P, Izaurralde E, Mattaj IW, Gilmartin GM (1997) Participation of the nuclear cap binding complex in pre-mRNA 3’ processing. Proc Natl Acad Sci USA 94:11893–11898CrossRefPubMedGoogle Scholar
  8. Furuichi Y, LaFiandra A, Shatkin AJ (1977) 5′-Terminal structure and mRNA stability. Nature 266:235–239CrossRefPubMedGoogle Scholar
  9. Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132:1107–1114CrossRefPubMedGoogle Scholar
  10. Geraldo N, Bäurle I, Kidou S, Hu X, Dean C (2009) FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol 150:1611–1618CrossRefPubMedGoogle Scholar
  11. Gräslund S, Nordlund P, Weigelt J, Hallberg BM, Bray J, Gileadi O, Knapp S, Oppermann U et al (2008) Protein production and purification. Nat Methods 5:135–146CrossRefPubMedGoogle Scholar
  12. Gregory BD, O’Malley RC, Lister R, Urich MA, Tonti-Filippini J, Chen H, Millar AH, Ecker JR (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Dev Cell 14:854–866CrossRefPubMedGoogle Scholar
  13. Hamm J, Mattaj IW (1990) Monomethylated cap structures facilitate RNA export from the nucleus. Cell 63:109–118CrossRefPubMedGoogle Scholar
  14. He Y, Doyle MR, Amasino RM (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18:2774–2784CrossRefPubMedGoogle Scholar
  15. Hecht V, Foucher F, Ferrándiz C, Macknight R, Navarro C, Morin J, Vardy ME, Ellis N, Beltrán JP, Rameau C, Weller JL (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137:1420–1434CrossRefPubMedGoogle Scholar
  16. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42:819–832CrossRefPubMedGoogle Scholar
  17. Hinds MG, Smits C, Fredericks-Short R, Risk JM, Bailey M, Huang DC, Day CL (2007) Bim, Bad and Bmf: intrinsically unstructured BH3-only proteins that undergo a localized conformational change upon binding to prosurvival Bcl-2 targets. Cell Death Differ 14:128–136CrossRefPubMedGoogle Scholar
  18. Izaurralde E, Stepinski J, Darzynkiewicz E, Mattaj IW (1992) A cap binding protein that may mediate nuclear export of RNA polymerase II-transcribed RNAs. J Cell Biol 118:1287–1295CrossRefPubMedGoogle Scholar
  19. Jiang D, Gu X, He Y (2009) Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21:1733–1746CrossRefPubMedGoogle Scholar
  20. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344–347CrossRefPubMedGoogle Scholar
  21. Kierzkowski D, Kmieciak M, Piontek P, Wojtaszek P, Szweykowska-Kulinska Z, Jarmolowski A (2009) The Arabidopsis CBP20 targets the cap-binding complex to the nucleus, and is stabilized by CBP80. Plant J 59:814–825CrossRefPubMedGoogle Scholar
  22. Kim SY, Michaels SD (2006) SUPPRESSOR OF FRIGIDA4 encodes a nuclear-localized protein that is required for delayed flowering in winter-annual Arabidopsis. Development 133:4699–4707CrossRefPubMedGoogle Scholar
  23. Kim S, Choi K, Park C, Hwang HJ, Lee I (2006) SUPPRESSOR OF FRIGIDA4, encoding a C2H2-type zinc finger protein, represses flowering by transcriptional activation of Arabidopsis FLOWERING LOCUS C. Plant Cell 18:2985–2998CrossRefPubMedGoogle Scholar
  24. Kim S, Yang J-Y, Xu J, Jang I-C, Prigge MJ, Chua N-H (2008) Two cap-binding proteins CBP20 and CBP80 are involved in processing primary MicroRNAs. Plant Cell Physiol 49:1634–1644CrossRefPubMedGoogle Scholar
  25. Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299CrossRefPubMedGoogle Scholar
  26. Laubinger S, Sachsenberg T, Zeller G, Busch W, Lohmann JU, Rätsch G, Weigel D (2008) Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:8795–8800CrossRefPubMedGoogle Scholar
  27. Lewis JD, Izaurralde E, Jarmolowski A, McGuigan C, Mattaj IW (1996) A nuclear cap-binding complex facilitates association of U1 snRNP with the cap-proximal 5′ splice site. Genes Dev 10:1683–1698CrossRefPubMedGoogle Scholar
  28. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Tasneem A, Thanki N, Yamashita RA, Zhang D, Zhang N, Bryant SH (2009) CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res 37:D205–D210CrossRefPubMedGoogle Scholar
  29. Martinez-Trujillo M, Limones-Briones V, Cabrera-Ponce J, Herrera-Estrella L (2004) Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Mol Biol Report 22:63–70CrossRefGoogle Scholar
  30. Michaels SD (2009) Flowering time regulation produces much fruit. Curr Opin Plant Biol 12:75–80CrossRefPubMedGoogle Scholar
  31. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956CrossRefPubMedGoogle Scholar
  32. Michaels SD, He Y, Scortecci KC, Amasino RM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci USA 100:10102–10107CrossRefPubMedGoogle Scholar
  33. Michaels SD, Bezerra IC, Amasino RM (2004) FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc Natl Acad Sci USA 101:3281–3285CrossRefPubMedGoogle Scholar
  34. Oh S, Park S, van Nocker S (2008) Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet 4:e1000077CrossRefPubMedGoogle Scholar
  35. Oldfield CJ, Cheng Y, Cortese MS, Brown CJ, Uversky VN, Dunker AK (2005) Comparing and combining predictors of mostly disordered proteins. Biochemistry 44:1989–2000CrossRefPubMedGoogle Scholar
  36. Pien S, Fleury D, Mylne JS, Crevillen P, Inzé D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20:580–588CrossRefPubMedGoogle Scholar
  37. Provencher SW, Glöckner J (1981) Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20:33–37CrossRefPubMedGoogle Scholar
  38. Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. BioEssays 26:363–373CrossRefPubMedGoogle Scholar
  39. Raczynska KD, Simpson CG, Ciesiolka A, Szewc L, Lewandowska D, McNicol J, Szweykowska-Kulinska Z, Brown JWS, Jarmolowski A (2010) Involvement of the nuclear cap-binding protein complex in alternative splicing in Arabidopsis thaliana. Nucleic Acids Res 38:265–278CrossRefPubMedGoogle Scholar
  40. Schlappi MR (2006) FRIGIDA LIKE 2 is a functional allele in Landsberg erecta and compensates for a nonsense allele of FRIGIDA LIKE 1. Plant Physiol 142:1728–1738CrossRefPubMedGoogle Scholar
  41. Schmitz RJ, Hong L, Michaels S, Amasino RM (2005) FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132:5471–5478CrossRefPubMedGoogle Scholar
  42. Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458CrossRefPubMedGoogle Scholar
  43. Sheldon CC, Finnegan EJ, Peacock WJ, Dennis ES (2009) Mechanisms of gene repression by vernalization in Arabidopsis. Plant J 59:488–498CrossRefPubMedGoogle Scholar
  44. Shindo C, Aranzana MJ, Lister C, Baxter CaN C, Nordborg M, Dean C (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 138:1163–1173CrossRefPubMedGoogle Scholar
  45. Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–803CrossRefPubMedGoogle Scholar
  46. Tamada Y, Yun J-Y, Woo S, Amasino R (2009) ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21:3257–3269CrossRefPubMedGoogle Scholar
  47. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-northerns, expression angling, and promoter analyses. Plant J 43:153–163CrossRefPubMedGoogle Scholar
  48. Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci USA 100:13099–13104CrossRefPubMedGoogle Scholar
  49. Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357CrossRefPubMedGoogle Scholar
  50. van Stokkum IH, Spoelder HJ, Bloemendal M, van Grondelle R, Groen FC (1990) Estimation of protein secondary structure and error analysis from circular dichroism spectra. Anal Biochem 191:110–118CrossRefPubMedGoogle Scholar
  51. Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D (2005) FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170:1197–1207CrossRefPubMedGoogle Scholar
  52. Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32:W668–W673CrossRefPubMedGoogle Scholar
  53. Xu L, Zhao Z, Dong A, Soubigou-Taconnat L, Renou J-P, Steinmetz A, Shen W-H (2007) Di- and tri- but not mono-methylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol Cell Biol 28:1348–1360CrossRefPubMedGoogle Scholar
  54. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Biochemistry DepartmentUniversity of OtagoDunedinNew Zealand

Personalised recommendations