Flower Morphogenesis: Timing Is Key
2009; Elsevier BV; Volume: 16; Issue: 5 Linguagem: Inglês
10.1016/j.devcel.2009.05.005
ISSN1878-1551
Autores Tópico(s)Plant Reproductive Biology
ResumoFlowers are unique parts of plants because they form a predictable number of organs of defined identity. This exquisite regularity defines entire plant families and has been used for taxonomic classification since ancient times. In this issue of Developmental Cell, Liu et al. reveal that timing of the onset of flower differentiation is key for the stereotypic architecture of flowers. Flowers are unique parts of plants because they form a predictable number of organs of defined identity. This exquisite regularity defines entire plant families and has been used for taxonomic classification since ancient times. In this issue of Developmental Cell, Liu et al. reveal that timing of the onset of flower differentiation is key for the stereotypic architecture of flowers. How flowers form organs of defined identity—sepals, petals, stamens and carpels—is well understood and involves the combined activity of four classes (A, B, C, and E) of flower organ identity genes (reviewed by Krizek and Fletcher, 2005Krizek B.A. Fletcher J.C. Nat. Rev. Genet. 2005; 6: 688-698Crossref PubMed Scopus (406) Google Scholar; see also Figure 1C). By contrast, little was known until now about how flowers form a predictable number of organs of a given identity. Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar show that formation of the prescribed complement floral organs of each type requires properly timed activation of the class E flower organ identity gene SEPALLATA3 (SEP3) during flower ontogeny. Precocious SEP3 upregulation is prevented by repressive chromatin modifications to avoid premature differentiation (Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar). In plants, the stem cells in the shoot apical meristem give rise to all above-ground structures, including flowers. Flower ontogeny begins with specification of an incipient primordium at the flanks of the shoot apical meristem to adopt the floral fate, followed by formation of the flower meristem (floral "stem cells") and activation of the four classes of flower organ identity genes during flower differentiation. What is known about the regulatory events during flower ontogeny? Flower initiation starts with upregulation of the plant-specific transcription factor LEAFY (LFY) in the incipient primordium (Figure 1A). Next, LFY and a second, parallel pathway converge to directly activate the class A flower organ identity transcription factor APETALA1 (AP1). LFY and AP1 together specify the floral fate of the primordium. Subsequently, flowers progress through a series of well-defined developmental stages (described by Smyth et al., 1990Smyth D.R. Bowman J.L. Meyerowitz E.M. Plant Cell. 1990; 2: 755-767PubMed Google Scholar; Figure 1A). In flower stages 1 and 2, the floral stem cell pool initiates and proliferates and the stem cell regulator WUSCHEL (WUS) accumulates (Figure 1A). The class E SEP genes are also activated in stage 2 flowers (Figure 1A). After this, differentiation begins in the outer regions of stage 3 flowers, due to the combined activity of class A and class E organ identity regulators, and progresses inwardly (Figure 1A). Differentiation in the central regions of the flower requires activation of the class B genes APETALA3 (AP3) and PISTILLATA (PI) and the class C gene AGAMOUS (AG) in early stage 3 flowers by LFY together with known coactivators that spatially restrict LFY activity (Krizek and Fletcher, 2005Krizek B.A. Fletcher J.C. Nat. Rev. Genet. 2005; 6: 688-698Crossref PubMed Scopus (406) Google Scholar). Finally, in stage 6 flowers, AG represses WUS expression and the floral stem cells differentiate (Krizek and Fletcher, 2005Krizek B.A. Fletcher J.C. Nat. Rev. Genet. 2005; 6: 688-698Crossref PubMed Scopus (406) Google Scholar; Figure 1A). Why does differentiation begin in stage 3 flowers and is this timing important? In this issue of Developmental Cell, Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar demonstrate that three flowering time regulators, SHORT VEGETATIVE PHASE (SVP), AG-LIKE 24 (AGL24) and SUPPRESSOR OF OVEREXPRESSION OF CO1 (SOC1), together delay flower differentiation until stage 3 by directly repressing expression of the class E gene SEP3 (Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar). This repression involves maintenance of repressive chromatin modifications at the SEP3 promoter via recruitment of chromatin regulators (Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar). Loss of SEP3 repression causes precocious differentiation in part by activating class B and class C flower organ identity genes. A qualitatively similar phenotype was reported for agl24 svp double mutants (Gregis et al., 2006Gregis V. Sessa A. Colombo L. Kater M.M. Plant Cell. 2006; 18: 1373-1382Crossref PubMed Scopus (158) Google Scholar). Activation of class B and class C genes by SEP3 is direct: SEP3 binds to the regulatory regions of AP3, PI, and AG (Kaufmann et al., 2009Kaufmann K. Muino J.M. Jauregui R. Airoldi C. Smacziak C. Krajewski P. PLoS Biol. 2009; 7: e1000090Crossref PubMed Scopus (318) Google Scholar). Premature differentiation in svp agl24 soc1 triple mutants results in formation of fewer floral organs in all four whorls (Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar). Thus, failure to maintain SEP3 repression interferes with completion of the flower meristem phase and formation of a sufficient number of stem cells. As a consequence, the prescribed complement of floral organs per whorl cannot form. How is the correct timing of flower differentiation controlled? The regulatory interactions described by Liu et al. provide mechanistic insight into this question. First, the precocious AP3, PI, and AG expression in agl24 soc1 svp triple mutants requires both SEP3 and LFY (Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar; Figure 1B), in agreement with the previous finding that LFY and SEP3 together are sufficient to induce floral organ formation outside of the context of the flower (Castillejo et al., 2005Castillejo C. Romera-Branchat M. Pelaz S. Plant J. 2005; 43: 586-596Crossref PubMed Scopus (97) Google Scholar). Second, expression of SVP, AGL24, and SOC1 must be downregulated after completion of the meristem phase to initiate flower differentiation. Previous data shows that this is achieved by AP1 directly repressing SVP, AGL24, and SOC1 in stage 2 flowers (Liu et al., 2007Liu C. Zhou J. Bracha-Drori K. Yalovsky S. Ito T. Yu H. Development. 2007; 134: 1901-1910Crossref PubMed Scopus (203) Google Scholar, Yu et al., 2004Yu H. Ito T. Wellmer F. Meyerowitz E.M. Nat. Genet. 2004; 36: 157-161Crossref PubMed Scopus (191) Google Scholar). Hence, AP1 indirectly activates SEP3 to initiate differentiation (Figure 1B). This further underscores the importance of the proper timing of flower differentiation; both ap1 and sep loss-of-function mutant flowers initiate additional flower meristems (Ditta et al., 2004Ditta G. Pinyopich A. Robles P. Pelaz S. Yanofsky M.F. Curr. Biol. 2004; 14: 1935-1940Abstract Full Text Full Text PDF PubMed Scopus (536) Google Scholar), likely due to delayed onset of flower differentiation. These findings (Liu et al., 2007Liu C. Zhou J. Bracha-Drori K. Yalovsky S. Ito T. Yu H. Development. 2007; 134: 1901-1910Crossref PubMed Scopus (203) Google Scholar, Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar, Yu et al., 2004Yu H. Ito T. Wellmer F. Meyerowitz E.M. Nat. Genet. 2004; 36: 157-161Crossref PubMed Scopus (191) Google Scholar), as well as additional regulatory interactions uncovered by Kaufmann et al., 2009Kaufmann K. Muino J.M. Jauregui R. Airoldi C. Smacziak C. Krajewski P. PLoS Biol. 2009; 7: e1000090Crossref PubMed Scopus (318) Google Scholar allow formulation of a model for formation of a predictable number of flower organs of a given identity (Figure 1B). We now know that LFY expression leads (indirectly) to activation of SEP3 and that both LFY and SEP3 are required to induce AP3, PI, and AG expression (Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar). This type of interaction corresponds to a known temporal delay module called a coherent feed-forward loop (Alon, 2007Alon U. Nat. Rev. Genet. 2007; 8: 450-461Crossref PubMed Scopus (1991) Google Scholar). Activation of AP3, PI, and AG in this feed-forward loop is further delayed by the requirement for AP1 accumulation and subsequent SVP, AGL24, and SOC1 repression prior to SEP3 upregulation (Figure 1B). On the other hand, SEP3 induction leads to stable activation of differentiation via positive-feedback loops: SEP3 directly upregulates its own expression as well as that of AP1 and directly represses SOC1 and SVP (Kaufmann et al., 2009Kaufmann K. Muino J.M. Jauregui R. Airoldi C. Smacziak C. Krajewski P. PLoS Biol. 2009; 7: e1000090Crossref PubMed Scopus (318) Google Scholar), while AG directly feeds back to SEP3 (reviewed in Krizek and Fletcher, 2005Krizek B.A. Fletcher J.C. Nat. Rev. Genet. 2005; 6: 688-698Crossref PubMed Scopus (406) Google Scholar; Figure 1C). Positive-feedback loops cause irreversible cell fate switches (Alon, 2007Alon U. Nat. Rev. Genet. 2007; 8: 450-461Crossref PubMed Scopus (1991) Google Scholar). In conclusion, two types of regulatory loops ensure that flower differentiation occurs at the right time in development (feed-forward loop) and is stably maintained (positive-feedback loops). The combined activity of these two types of regulatory loops allows proper proliferation of the stem cell pool and formation of the prescribed number of organs of each type. Liu et al. further show that the four SEP proteins redundantly upregulate AP3, PI, and AG expression, yet thus far there is no evidence that expression of SEP1, SEP2, or SEP4 is repressed by SVP1, AGL24, and SOC1 (Liu et al., 2009Liu C. Xi W. Shen L. Tan C. Yu H. Dev. Cell. 2009; 16 (this issue): 711-722Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar). This begs the question of how precocious expression of these SEP genes is prevented. In addition, recent investigations have focused on hormonal regulation of flower meristem formation and differentiation. It will be interesting to indentify the links between hormonal and developmental control of early phases of flower development. Regulation of Floral Patterning by Flowering Time GenesLiu et al.Developmental CellMay 19, 2009In BriefFloral patterning in Arabidopsis requires activation of floral homeotic genes by the floral meristem identity gene, LEAFY (LFY). Here we show that precise activation of expression of class B and C homeotic genes in floral meristems is regulated by three flowering time genes, SHORT VEGETATIVE PHASE (SVP), SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), and AGAMOUS-LIKE 24 (AGL24), through direct control of a LFY coregulator, SEPALLATA3 (SEP3). Orchestrated repression of SEP3 by SVP, AGL24, and SOC1 is mediated by recruiting two interacting chromatin regulators, TERMINAL FLOWER 2/LIKE HETEROCHROMATIN PROTEIN 1 and SAP18, a member of SIN3 histone deacetylase complex. Full-Text PDF Open Archive
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