Abstract
Main conclusion
Fackel (FK) is involved in the flowering of Arabidopsis mainly via the gibberellin pathway and vernalization pathway. This new function of FK is partially dependent on the FLOWERING LOCUS C ( FLC ).
A common transitional process from vegetative stage to reproductive stage exists in higher plants during their life cycle. The initiation of flower bud differentiation, which plays a key role in the reproductive phase, is affected by both external environmental and internal regulatory factors. In this study, we showed that the Arabidopsis weak mutant allele fk-J3158, impaired in the FACKEL (FK) gene, which encodes a C-14 reductase involved in sterol biosynthesis, had a long life cycle and delayed flowering time in different photoperiods. In addition, FK overexpression lines displayed an earlier flowering phenotype than that of the wild type. These processes might be independent of the downstream brassinosteroid (BR) pathway and the autonomous pathway. However, the fk-J3158 plants were more sensitive than wild type in reducing the bolting days and total leaf number under gibberellic acid (GA) treatment. Further studies suggested that FK mutation led to an absence of endogenous GAs in fk-J3158 and FK gene expression was also affected under GA and paclobutrazol (PAC) treatment. Moreover, the delayed flowering time of fk-J3158 could be rescued by a 3-week vernalization treatment, and the expression of FLOWERING LOCUS C (FLC) was accordingly down-regulated in fk-J3158. We also demonstrated that flowering time of fk-J3158 flc double mutant was significantly earlier than that of fk-J3158 under the long-day (LD) conditions. All these results indicated that FK may affect the flowering in Arabidopsis mainly via GA pathway and vernalization pathway. And these effects are partially dependent on the FLOWERING LOCUS C (FLC).
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Abbreviations
- BL:
-
24-Epibrassinolide
- BR:
-
Brassinosteroid
- LD:
-
Long-day
- FK:
-
FACKEL
- FLC(D):
-
FLOWERING LOCUS C(D)
- FLK:
-
FLOWERING LOCUS KH DOMAIN
- GA:
-
Gibberellic acid
- PAC:
-
Paclobutrazol
- SD:
-
Short-day
- SOC1:
-
SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1
References
Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D, Genschik P, Moritz T, Harberd NP (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. P Natl Acad Sci USA 104:6484–6489
Alexndre CM, Hennig L (2008) FLC or not FLC: the other side of vernalization. J Exp Bot 59:1127–1135
Amasino R (2004) Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16:2553–2559
Amasino RM (2005) Vernalization and flowering time. Curr Opin Plant Biol 16:154–158
Attard G, Cooper CS, de Bono JS (2009) Steroid hormone receptors in prostate cancer: a hard habit to break? Cancer Cell 16:458–462
Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nature Genetic 36:162–166
Azpiroz R, Wu Y, LoCascio JC, Feldmann KA (1998) An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10:219–230
Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664
Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18–S31
Boutté Y, Grebe M (2009) Cellular processes relying on sterol function in plants. Curr Opin Plant Biol 12:705–713
Carland FM, Fujioka S, Takatsuto S, Yoshida S, Nelson T (2002) The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell 14:2045–2058
Chiang GC, Barua D, Kramer EM, Amasino RM, Donohue K (2009) Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. P Natl Acad Sci USA 106:11661–11666
Chory J, Nagpal P, Peto CA (1991) Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell 3:445–459
Clouse SD (2000) Plant development: a role for sterols in embryogenesis. Curr Biol 10:R601–R604
Clouse SD (2008) The molecular intersection of brassinosteroid-regulated growth and flowering in Arabidopsis. P Natl Acad Sci USA 105:7345–7346
Davis SJ (2009) Integrating hormones into the floral-transition pathway of Arabidopsis thaliana. Plant Cell Environ 32:1201–1210
Domagalska MA, Schomburg FM, Amasino RM, Vierstra RD, Nagy F, Davis SJ (2007) Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering. Development 134:2841–2850
Domagalska MA, Sarnowska E, Nagy F, Davis SJ (2010) Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PLoS ONE 5:e14012
Gendall AR, Levy YY, Wilson A, Dean C (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107:525–535
Gilbert LI, Rybczynski R, Warren JT (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 47:883–916
Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2:E311
He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science 302:1751–1754
Hobbs DH, Hume JH, Rolph CE, Cooke DT (1996) Changes in lipid composition during floral development of Brassica campestris. Phytochemistry 42(2):335–339
Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5:887–896
Jang JC, Fujioka S, Tasaka M, Seto H, Takatsuto S, Ishii A, Aida M, Yoshida S, Sheen J (2000) A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev 14:1485–1497
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
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 290:344–347
Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965
Kim HB, Schaller H, Goh C, Kwon M, Choe S, An CS, Durst F, Feldmann KA, Feyereisen R (2005) Arabidopsis cyp51 mutant shows postembryonic seedling lethality associated with lack of membrane integrity. Plant Physiol 138:2033–2047
Koornneef M, Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Peeters AJ (1998) Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148:885–892
Kotchoni SO, Larrimore KE, Mukherjee M, Kempinski CF, Barth C (2009) Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis. Plant Physiol 149:803–815
Lee I, Aukerman MJ, Gore SL, Lohman KN, Michaels SD, Weaver LM, John MC, Feldmann KA, Amasino RM (1994) Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis. Plant Cell 6:75–83
Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14:2366–2376
Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21:397–402
Levy YY (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297:243–246
Li J (2010) Multi-tasking of somatic embryogenesis receptor-like protein kinases. Curr Opin Plant Biol 13:509–514
Li JH, Li YH, Chen SY, An LZ (2010) Involvement of brassinosteroid signals in floral-induction network of Arabidopsis. J Exp Bot 61:4221–4230
Li M, An F, Li W, Ma M, Feng Y, Zhang X, Guo H (2016) DELLA proteins interact with FLC to repress flowering transition. J Integr Plant Biol 58(7):642–655
Lim MH, Kim J, Kim YS, Chung KS, Seo YH, Lee I, Kim J, Hong CB, Kim HJ, Park CM (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16:731–740
Lindsey K, Topping JF, Pullen ML (2003) Importance of plant sterols in pattern formation and hormone signaling. Trends Plant Sci 8:521–525
Men S, Boutte Y, Ikeda Y, Li X, Palme K, Stierhof Y, Hartmann M, Moritz T, Grebe M (2008) Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nature Cell Biol 10:237–244
Michaels SD (2009) Flowering time regulation produces much fruit. Curr Opin Plant Biol 12:75–80
Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956
Michaels SD, Amasino RM (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13:935–941
Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623
Pose D, Castanedo I, Borsani O, Nieto B, Rosado A, Taconnat L, Ferrer A, Dolan L, Valpuesta V, Botella MA (2009) Identification of the Arabidopsis dry2/sqe1-5 mutant reveals a central role for sterols in drought tolerance and regulation of reactive oxygen species. Plant J 59:63–76
Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–857
Qian PP, Han B, Forestier E, Hu ZH, Gao N, Schaller H, Li J, Hou SW (2013) Sterols are required for coordination of daughter cell fates after asymmetric division during Arabidopsis stomatal development. Plant J 74:1029–1044
Schaller H (2003) The role of sterols in plant growth and development. Prog Lipid Res 42:163–175
Schrick K, Mayer U, Horrichs A, Kuhnt C, Bellini C, Dangl J, Schmidt J, Jurgens G (2000) FACKEL is a sterol C-14 reductase required for organized cell expansion in Arabidopsis embryogenesis. Genes Dev 14:1471–1484
Schrick K, Mayer U, Martin G, Bellini C, Kuhnt C, Schmidt J, Jurgens G (2002) Interactions between sterol biosynthesis genes in embryonic development of Arabidopsis. Plant J 31:61–73
Searle I, He YH, Turck F, Vincent C, Fornara F, Krober S, Amasino RA, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signalling in Arabidopsis. Genes Dev 20:898–912
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 11:445–458
Simpson GG (2004) The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr Opin Plant Biol 7:570–574
Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289
Souter MA, Topping JF, Pullen M, Friml J, Palme K, Hackett R, Grierson D, Lindsey K (2002) hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell 14:1017–1031
Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164
Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Wang H, Torres QI, Ward JM, Murthy G, Zhang J, Walker JC, Neff MM (2005) BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J 42:23–34
Wilson RN, Somerville CR (1995) Phenotypic suppression of the gibberellin-insensitive mutant (gai) of Arabidopsis. Plant Physiol 108:495–502
Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408
Wollenberg AC, Strasser B, Cerdan PD, Amasino RM (2008) Acceleration of flowering during shade avoidance in Arabidopsis alters the balance between FLOWERING LOCUS C-mediated repression and photoperiodic induction of flowering. Plant Physiol 148:1681–1694
Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16:367–378
Yu X, Li L, Li L, Guo M, Chory J, Yin YH (2008) Modulation of brassinosteroid- regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. P Natl Acad Sci USA 105:7618–7623
Acknowledgements
This work is supported by the National Natural Science Foundation of China (NSFC) (Grant Nos. 31271460, 31470372, 31670185, 31400245), the Ministry of Agriculture of the People’s Republic of China (Grant No. 2016ZX08009-003-002), the Fundamental Research Funds for the Central Universities (Grant Nos. lzujbky-2015-226, lzujbky-2015-ot09, lzujbky-2016-79).
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B. Huang, P. Qian and N. Gao contributed equally to this work.
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Huang, B., Qian, P., Gao, N. et al. Fackel interacts with gibberellic acid signaling and vernalization to mediate flowering in Arabidopsis . Planta 245, 939–950 (2017). https://doi.org/10.1007/s00425-017-2652-5
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DOI: https://doi.org/10.1007/s00425-017-2652-5