An Arabidopsis thaliana (Ler) inbred line AFDL exhibiting abnormal flower development mainly caused by reduced AP1 expression
Abstract
The genetic network controlling flowering and flower development consists of a set of floral integrator genes that play a role in light sensing, hormone signaling and developmental pathways. These integrators activate the expression of meristem identity genes LEAFY (LFY) and APETALA1 (AP1) to initiate the flowering transition. However, how the expression of key genes, such as AP1, responds to diverse signals during flower development remains largely unknown. Here, we report that an Arabidopsis abnormal flower development inbred line (AFDL) exhibits a phenotype similar to the ap1 mutant, with delayed flowering time and a high frequency of transition of flower meristems into inflorescence meristems after flowering. The flower organs with an abnormal first whorl lack the second whorl and the increased number of inflorescences at the first- and second-whorl positions most closely resembled the phenotypes of ap1/cal double mutants. Interestingly, both normal and abnormal flowers coexisted in a single individual. Microarray and quantitative real-time PCR analysis revealed that the expression of AP1 was significantly reduced, while the expression of its interacting genes TERMINAL FLOWER 1 (TFL1), SHORT VEGETATIVE PHASE (SVP), AGAMOUS-like 24 (AGL24), SEPALLATA (SEP) and CAULIFLOWER (CAL) and upstream genes FLOWERING LOCUS C (FLC) and FLM were increased in AFDL, which could serve to explain its phenotype. The expression of genes responsive to different stimuli dramatically changed in AFDL relative to the wild type, as revealed by the differential display of transcripts, indicating that this expression variation is subject to a threshold, leading to an on/off expression pattern of the master regulatory gene (such as AP1) of flower development.
Keywords
Arabidopsis thaliana gene regulation flower development AP1 microarray RT-PCRReferences
- 1.Yant L, Mathieu J, Schmid M. Just say no: Floral repressors help Arabidopsis bide the time. Curr Opin Plant Biol, 2009, 12: 580–586CrossRefGoogle Scholar
- 2.Engelmann K, Purugganan M. The molecular evolutionary ecology of plant development: Flowering time in Arabidopsis thaliana. Adv Bot Res, 2006, 44: 507–526CrossRefGoogle Scholar
- 3.Komeda Y. Genetic regulation of time to flower in Arabidopsis thaliana. Annu Rev Plant Biol, 2004, 55: 521–535CrossRefGoogle Scholar
- 4.Baurle I, Dean C. The timing of developmental transitions in plants. Cell, 2006, 125: 655–664CrossRefGoogle Scholar
- 5.Michaels S D. Flowering time regulation produces much fruit. Curr Opin Plant Biol, 2009, 12: 75–80CrossRefGoogle Scholar
- 6.Borner R, Kampmann G, Chandler J, et al. A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J, 2000, 24: 591–599CrossRefGoogle Scholar
- 7.Blazquez M A, Weigel D. Integration of floral inductive signals in Arabidopsis. Nature, 2000, 404: 889–892CrossRefGoogle Scholar
- 8.Lee J H, Yoo S J, Park S H, et al. Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev, 2007, 21: 397–402CrossRefGoogle Scholar
- 9.Li D, Liu C, Shen L, et al. A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell, 2008, 15: 110–120CrossRefGoogle Scholar
- 10.Irish V F, Sussex I M. Function of the apetala-1 gene during Arabídopsis floral development. Plant Cell, 1990, 2: 741–753CrossRefGoogle Scholar
- 11.Bowman J L, Alvarez J, Weigel D, et al. Control of flower develop ment in Arabidopsis thaliana by APETALA1 and interacting genes. Development, 1993, 119: 721–743Google Scholar
- 12.Irish V F. Patterning the flower. Dev Biol, 1999, 209: 211–220CrossRefGoogle Scholar
- 13.Liu C, Zhou J, Bracha-Drori K, et al. Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development, 2007, 134: 1901–1910CrossRefGoogle Scholar
- 14.Kempin S A, Savidge B, Yanofsky M F. Molecular basis of the cauliflower phenotype in Arabidopsis. Science, 1995, 267: 522–525CrossRefGoogle Scholar
- 15.Mandel M A, Gustafson-Brown C, Savidge B, et al. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature, 1992, 360: 273–277CrossRefGoogle Scholar
- 16.Parcy F, Nilsson O, Busch M A, et al. A genetic framework for floral patterning. Nature, 1998, 395: 561–566CrossRefGoogle Scholar
- 17.Wagner D, Sablowski R W M, Meyerowitz E M. Transcriptional activation of APETALA1 by LEAFY. Science, 1999, 285: 582–584CrossRefGoogle Scholar
- 18.Ruiz-Garcia L, Madueno F, Wilkinson M, et al. Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell, 1997, 9: 1921–1934CrossRefGoogle Scholar
- 19.Sundstrom J F, Nakayama N, Glimelius K, et al. Direct regulation of the floral homeotic APETALA1 gene by APETALA3 and PISTILLATA in Arabidopsis. Plant J, 2006, 46: 593–600CrossRefGoogle Scholar
- 20.Pelaz S, Ditta G S, Baumann E, et al. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature, 2000, 405: 200–203CrossRefGoogle Scholar
- 21.Pelaz S, Gustafson-Brown C, Kohalmi S E, et al. APETALA1 and SEPALLATA3 interact to promote flower development. Plant J, 2001, 26: 385–394CrossRefGoogle Scholar
- 22.Ditta G, Pinyopich A, Robles P, et al. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol, 2004, 14: 1935–1940CrossRefGoogle Scholar
- 23.Karim M R, Hirota A, Kwiatkowska D, et al. A role for Arabidopsis PUCHI in floral meristem identity and bract suppression. Plant Cell, 2009, 21: 1360–1372CrossRefGoogle Scholar
- 24.Hepworth S R, Valverde F, Ravenscroft D, et al. Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J, 2002, 21: 4327–4337CrossRefGoogle Scholar
- 25.Gao D, Zhang H. A new drying method of plant specimens for scanning electron microscopy the t-butyl alcohol freeze-drying method. Acta Bot Sin, 1989, 31: 770–774Google Scholar
- 26.Gregis V, Sessa A, Colombo L, et al. AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of fower development in Arabidopsis. Plant Cell, 2006, 18: 1373–1382CrossRefGoogle Scholar
- 27.Huang D W, Sherman B T, Lempicki R A. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc, 2009, 4: 44–57CrossRefGoogle Scholar
- 28.Dennis G J, Sherman B T, Hosack D A, et al. DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol, 2003, 4: P3CrossRefGoogle Scholar
- 29.Shannon S, Meeks-Wagner D R. A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell, 1991, 3: 877–892CrossRefGoogle Scholar
- 30.Bradley D, Ratcliffe O, Vincent C, et al. Inflorescence commitment and architecture in Arabidopsis. Science, 1997, 275: 80–83CrossRefGoogle Scholar
- 31.Scortecci K C, Michaels S D, Amasino R M. Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J, 2001, 26: 229–236CrossRefGoogle Scholar
- 32.Buchovsky A S, Strasser B, Cerdan P D, et al. Suppression of pleiotropic effects of functional CRYPTOCHROME genes by TERMINAL FLOWER 1. Genetics, 2008, 180: 1467–1474CrossRefGoogle Scholar
- 33.Fujiwara S, Oda A, Yoshida R, et al. Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell, 2008, 20: 2960–2971CrossRefGoogle Scholar
- 34.Grunewald W, Vanholme B, Pauwels L, et al. Expression of the Arabidopsis jasmonate signalling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO Rep, 2009, 10: 923–928CrossRefGoogle Scholar
- 35.Leibfried A, To J P C, Busch W, et al. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature, 2005, 438: 1172–1175CrossRefGoogle Scholar
- 36.Yu H, Ito T, Zhao Y, et al. Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci USA, 2004, 101: 7827–7832CrossRefGoogle Scholar
- 37.Seo E, Lee H, Jeon J, et al. Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell, 2009, 21: 3185–3197CrossRefGoogle Scholar
- 38.Raj A, Rifkin S A, Andersen E, et al. Variability in gene expression underlies incomplete penetrance. Nature, 2010, 463: 913–919CrossRefGoogle Scholar
- 39.Parcy F. Flowering: A time for integration. Int J Dev Biol, 2005, 49: 585–593CrossRefGoogle Scholar
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