| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
First published online March 12, 2004; 10.1105/tpc.017038
© 2004 American Society of Plant Biologists Molecular and Genetic Mechanisms of Floral ControlDepartment of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 1 To whom correspondence should be addressed. E-mail thomas.jack{at}dartmouth.edu; fax 603-646-1347.
In the last 15 years, knowledge of the molecular and genetic mechanisms that underlie floral induction, floral patterning, and floral organ identity has exploded. Elucidation of basic mechanisms has derived primarily from work in three dicot species: Antirrhinum majus, Arabidopsis thaliana, and Petunia hybrida. Although Antirrhinum and petunia have contributed fundamental breakthroughs to our understanding of flower development, it is from Arabidopsis that the most detailed and comprehensive picture of the molecular mechanisms underlying flower development has been obtained. In this review, I will outline the present state of knowledge, focusing on molecular and genetic mechanisms revealed in work on Arabidopsis, specifically in three areas: the integration of floral induction signals by a small group of floral integrators, the activation of the floral organ identity genes by the floral meristem identity genes, and interactions among the floral organ identity genes, particularly the A and C class genes. By choosing to focus on progress in Arabidopsis, I do not mean to suggest that work in other species is unimportant or uninformative. To the contrary, without studies in Antirrhinum and petunia, our knowledge and the broad impact of what has been learned would clearly be less. One of the satisfying things about the field of flower development is the applicability of the floral patterning mechanisms to a wide range of plant species; such a conclusion only comes from careful analysis in multiple distantly related species. The general pattern in the field has been that molecular and genetic mechanisms, based on work in model species, serve as the basis for work in other species, many of which are of economic importance. Ultimately, the goal is to use information discovered in the model plants to engineer economically important plants for human and ecological benefit.
The first unifying principle in the flower development field is the ABC model. This model, initially proposed in the early 1990s based on genetic experiments in Antirrhinum and Arabidopsis, is striking in its simplicity and is applicable to a wide range of angiosperm species, both dicots and monocots, including economically important grass species such as rice and maize (Bowman et al., 1991  ; Coen and Meyerowitz, 1991; Ambrose et al., 2000; Fornara et al., 2003). The Arabidopsis flower, like most angiosperm flowers, consists of four organ types that are arranged in a series of concentric rings or whorls. From outside to inside, the flower consists of sepals in whorl 1, petals in whorl 2, stamens in whorl 3, and carpels in whorl 4. The ABC model postulates that three activities, A, B, and C, specify floral organ identity in a combinatorial manner. Specifically, A alone specifies sepals, A+B specifies petals, B+C specifies stamens, and C alone specifies carpels. A second major aspect is that A and C classes are mutually repressive. In the absence of A, C activity is present throughout the flower. Likewise, in the absence of C, A activity is present throughout the flower. Throughout the 1990s, the ABC genes were cloned from a wide range of species, and numerous molecular studies were performed. These molecular experiments largely support the major tenets of the ABC model (reviewed by Weigel and Meyerowitz, 1994; Yanofsky, 1995; Ng and Yanofsky, 2001b; Lohmann and Weigel, 2002).
The second major unifying principle involves the central role of the LEAFY (LFY) gene (Coen et al., 1990 Broadly speaking, flower development can be divided into four steps that occur in a temporal sequence. First, in response to both environmental and endogenous signals, the plant switches from vegetative growth to reproductive growth; this process is controlled by a large group of flowering time genes. Second, signals from the various flowering time pathways are integrated and lead to the activation of a small group of meristem identity genes that specify floral identity. Third, the meristem identity genes activate the floral organ identity genes in discrete regions of the flower. Fourth, the floral organ identity genes activate downstream "organ building" genes that specify the various cell types and tissues that constitute the four floral organs.
The flowering time genes function on four major promotion pathways: long-day photoperiod, gibberellin (GA), autonomous, and vernalization. Mutants in the long-day photoperiod promotion pathway are late flowering when grown in long-day photoperiods. Many long-day pathway genes encode proteins involved in light perception (e.g., PHYTOCHROME A and CRYPTOCHROME2) or components of the circadian clock (e.g., GIGANTEA and ELF3) (reviewed by Reeves and Coupland, 2000 ; Mouradov et al., 2002; Hayama and Coupland, 2003). The light and clock components ultimately lead to the activation of CONSTANS (CO). co mutants are late flowering, particularly in long-day photoperiods (Koornneef et al., 1991). Overexpression of CO results in very early flowering (Simon et al., 1996; Onouchi et al., 2000). CO encodes a nuclear protein that contains two B-box zinc finger domains (Putterill et al., 1995). Despite the presence of zinc finger domains, there is no evidence that CO is a sequence-specific DNA binding protein. Instead, it seems likely that CO is a component of a transcriptional activation complex that is directed to specific target genes by another component of the complex that possesses sequence-specific DNA binding activity.
A second flowering time pathway involves the promotion of flowering by GA. Mutants defective in the biosynthesis of GA, such as ga1, exhibit dramatic delays in the timing of flowering when grown in short days but not long days, suggesting that GA is an important stimulator of flowering in the absence of long-day promotion (Wilson et al., 1992 Genes on the third pathway, the autonomous pathway, function to control flowering in a photoperiod-independent manner. As a facultative long-day plant, Arabidopsis flowers more rapidly when grown in long days, but it does eventually flower when grown in noninductive short-day photoperiods. Autonomous pathway components play a role in this promotion. The fourth major pathway is the vernalization pathway. An extended cold treatment (vernalization) that mimics overwintering stimulates flowering in many Arabidopsis accessions.
The details of the functions and interactions among the flowering time genes have been the focus of several recent reviews (Koornneef et al., 1998
Ultimately, the flowering time genes function to control the activity of a much smaller group of meristem identity genes. The meristem identity genes can be divided into two subclasses: the shoot meristem identity genes and the floral meristem identity genes. Shoot meristem identity genes such as TERMINAL FLOWER1 (TFL1) specify the inflorescence shoot apical meristem as indeterminate and nonfloral (Bradley et al., 1996 , 1997). In tfl1 mutants, the shoot inflorescence meristem develops as a flower, resulting in a terminal flower phenotype in Arabidopsis, a plant that normally develops indeterminate inflorescences (Shannon and Meeks-Wagner, 1991; Alvarez et al., 1992). Ectopic expression of TFL1 (e.g., 35S:TFL1) converts the normally floral lateral meristems that arise on the flanks of the shoot apical meristem into shoots (Ratcliffe et al., 1998).
The second subclass, the floral meristem identity genes, specify lateral meristems in Arabidopsis to develop into flowers rather than leaves or shoots. After bolting, Arabidopsis plants produce between two and five cauline leaves on the primary inflorescence before developing flowers. In the axil of each of the cauline leaves is a secondary inflorescence meristem that gives rise to a secondary shoot. In Arabidopsis, LFY and APETALA1 (AP1) specify the lateral primordia to develop as flowers rather than shoots. Both lfy and ap1 single mutants exhibit a partial conversion of flowers to shoots (Irish and Sussex, 1990
Both LFY and AP1 encode sequence-specific DNA binding transcription factors. AP1 is a member of the MADS family (Huijser et al., 1992
One of the key events in the development of flowers is the activation of LFY and AP1. LFY and AP1 respond, either directly or indirectly, to outputs of flowering time pathways. Some of the outputs of the flowering time pathways are integrated by LFY, whereas others are integrated upstream or in parallel to LFY by FLOWERING LOCUS C (FLC), SUPPRESSOR OF OVEREXPRESSION OF CONSTANS (SOC1), and FLOWERING LOCUS T (FT).
Repressive signals from the autonomous and vernalization pathways are integrated by the floral repressor FLC (Figure 1) (Michaels and Amasino, 1999
Vernalization also results in a reduction in FLC RNA/protein levels. Several lines of evidence suggest that vernalization controls FLC epigenetically, either by altering the methylation state of FLC or by controlling chromatin structure (Sheldon et al., 2000a
In turn, FLC functions to repress the floral activator SOC1 (Figure 1) (Lee et al., 2000
Although the GA-responsive element in the SOC1 promoter has not been defined, it is clear that removal of the FLC repression of SOC1 is not sufficient to result in high SOC1 transcript levels; upregulation of SOC1 also requires positive activation by either the GA or the long-day promotion pathway. The best evidence that the release of FLC repression is not sufficient for SOC1 upregulation comes from an analysis of ga1 mutant plants that express high levels of FLC RNA/protein because they contain functional alleles of both FRI and FLC. When short-day-grown ga1 FRI FLC plants are vernalized, levels of FLC RNA decrease in response to vernalization treatment but levels of SOC1 do not increase. Thus, the upregulation of SOC1 requires activation by the long-day pathway either via CO or via the GA pathway. In short days, the GA pathway is the only pathway that can activate SOC1 (Moon et al., 2003
Like SOC1, LFY is a key integrator of output signals from the long-day promotion and GA pathways (Blazquez et al., 1998
The photoperiod promotion effects on LFY may be mediated by SOC1 or by a second MADS gene, AGAMOUS-LIKE24 (AGL24). Like SOC1 loss- and gain-of-function alleles, agl24 loss-of-function mutants are late flowering, and overexpression of AGL24 results in early flowering (Yu et al., 2002
The third major integrator of flowering time pathways is FT (Kardailsky et al., 1999
The long-day promotion pathway functions by activating LFY and AP1 via separate branches of the photoperiod pathway. Downstream of CO, the pathway splits; one branch functions via SOC1 and LFY, the other via FT. CO is the last identified component of the long-day promotion pathway that is upstream of both LFY and FT. The branch of the pathway that acts via FT appears to promote flowering by ultimately activating AP1 rather than LFY (Ruiz-Garcia et al., 1997
Although AP1 and LFY are necessary to specify floral meristem identity, they do not function independently of one another. Instead, AP1 functions largely downstream of LFY. The best evidence for this comes from analysis of combinations of gain-of-function and loss-of-function alleles of LFY and AP1. The floral promotion effects of 35S:LFY are blocked in an ap1 mutant (Weigel and Nilsson, 1995 ), but the floral promotion effects of 35S:AP1 are not blocked in a lfy mutant (Mandel and Yanofsky, 1995). However, in 35S:AP1 lfy, floral organ identity is not properly specified, demonstrating that LFY is necessary for the proper expression of floral organ identity genes, and this activity of LFY is independent of AP1.
The activation of AP1 by LFY is postulated to be direct. The best evidence for this comes from experiments that use an inducible form of LFY (fusion of LFY to the rat glucocorticoid receptor [LFY-GR]). The induction of LFY-GR in the presence of a protein synthesis inhibitor results in the rapid upregulation of AP1 RNA, suggesting that LFY directly activates AP1 (Wagner et al., 1999
The regulation of the shoot identity gene TFL1 is poorly understood. TFL1 RNA accumulates in subapical cells in the shoot apex before the vegetative-to-reproductive phase transition, at  2 to 3 days of seedling development when plants are grown in long days (Bradley et al., 1997). TFL1 is expressed at low levels in the vegetative shoot meristem and appears to play a role in preventing premature flowering. At later stages, TFL1 is upregulated and plays a role in repressing the expression of floral meristem identity genes such as LFY and AP1 in the shoot meristem. The upstream regulators of TFL1 are unknown. TFL1 encodes a protein that likely plays a role in signaling, perhaps as an inhibitor of mitogen-activated protein kinase pathways (Corbit et al., 2003). TFL1 is closely related to FT; the two proteins are 50% identical (Kardailsky et al., 1999). This high degree of similarity is surprising because FT and TFL1 have opposite effects on flowering timing: ft mutants are late flowering, and tfl1 mutants are early flowering. TFL1 and FT are members of a six-member gene family in Arabidopsis (Mimida et al., 2001). Future work will be aimed at determining the molecular function of this enigmatic group of proteins.
There is a mutually repressive relationship between the shoot identity gene TFL1 and the meristem identity genes LFY and AP1, and the repression is mediated at the transcriptional level. In tfl1 mutants, LFY and AP1 RNAs are expressed ectopically in the shoot apex (Weigel et al., 1992
One of the important functions of the floral meristem identity genes is to activate the ABC floral organ identity genes. The A class genes specify the identity of sepals and petals that develop in whorls 1 and 2, respectively. A second function of A class genes is to repress C class activity in whorls 1 and 2. In Arabidopsis, there are two A class genes: AP1 and AP2. The B class genes AP3 and PISTILLATA (PI) are required to specify the identity of petals in whorl 2 and stamens in whorl 3. The C class gene AGAMOUS (AG) is necessary to specify the identity of whorl 3 stamens and whorl 4 carpels. The second major function of C class is to repress A class activity in whorls 3 and 4.
The general rule for the floral organ identity genes is that the gene products are expressed in the region of the flower that exhibits defects in mutants. For example, AG RNA is expressed in stamen and carpel primordia and throughout these organs once they have formed (Yanofsky et al., 1990
The second A class gene, AP2, is the exception to the general rule stated above. Although AP2 functions only in whorls 1 and 2, AP2 RNA is present in all four floral whorls throughout flower development. This puzzling fact was explained recently by the discovery that AP2 is translationally repressed by a microRNA (miRNA) present in whorls 3 and 4 (Chen, 2004
In the last several years, it has become clear that a fourth set of genes, the SEPALLATA (SEP) genes, are necessary for proper floral organ identity (Pelaz et al., 2000 , 2001a). The first indication that SEP genes played an important role in petal, stamen, and carpel identity came from cosuppression experiments in petunia and tomato (Angenent et al., 1994; Pnueli et al., 1994). In petunia, a transgenic line designed to cosuppress the SEP3 ortholog FLORAL BINDING PROTEIN2 (FBP2) resulted in floral organ identity transformations in whorls 2, 3, and 4 as well as a loss of floral determinacy. In these FBP2 cosuppressed plants, the SEP/FBP2 subfamily member FBP5 also is downregulated, suggesting that both FBP2 and FBP5 are necessary for organ identity specification of petals, stamens, and carpels as well as for proper floral determinacy (Ferrario et al., 2003). These observations were extended with genetic analysis of the three SEP family members in Arabidopsis: SEP1, SEP2, and SEP3. Single and double sep mutant combinations fail to exhibit a dramatic phenotype in floral development. By contrast, sep1 sep2 sep3 triple mutants consist entirely of sepal-like organs, and their flowers are indeterminate (Pelaz et al., 2000). The phenotype of sep1 sep2 sep3 triple mutants is similar to that of double mutants that lack both B and C class activity, such as pi ag and ap3 ag (Bowman et al., 1989). Based on this fact, the three SEP genes are postulated to function redundantly to specify petals, stamens, and carpels as well as floral determinacy.
The discovery of the importance of the SEP genes has led to a revision of the ABC model (Goto et al., 2001
The SEP genes are referred to as E class rather than D class because a second set of genes, initially characterized in petunia, was previously named D class genes (Colombo et al., 1995 ). The two genes FBP7 and FBP11 function to specify placenta and ovule identity in petunia. In FBP7 and FBP11 cosuppressed plants, ovules do not develop and are replaced by carpel-like structures (Angenent et al., 1995). In the cosuppressed lines, both FBP7 and FBP11 are downregulated, and downregulation of both genes appears to be necessary for the ovule-to-carpel transformations, because single loss-of-function fbp7 and fpb11 mutants do not exhibit an ovule phenotype (Vandenbussche et al., 2003). Ectopic expression of FBP11 results in the development of ectopic ovules on whorl 1 sepals and whorl 2 petals (Colombo et al., 1995). Thus, in petunia, FBP11 is necessary and sufficient to specify ovule identity.
The Arabidopsis ortholog of FBP11 is AGL11, recently renamed SEEDSTICK (STK) (Pinyopich et al., 2003
Most ABCDE genes are members of the MADS transcription factor family, including the A class gene AP1, the B class genes AP3 and PI, the C class gene AG, the D class genes STK, SHP1, and SHP2, and the E class genes SEP1, SEP2, and SEP3. The A class gene AP2 is the exception; AP2 encodes a putative transcription factor that is a member of a small plant-specific gene family (Okamuro et al., 1997a ; Riechmann and Meyerowitz, 1998). In addition, several flowering time proteins (FLC, SOC1, AGL24, and SHORT VEGETATIVE PHASE [SVP] [Hartmann et al., 2000]) and meristem identity proteins CAULIFLOWER (CAL and FUL) also are MADS proteins. In Arabidopsis, there are >100 MADS genes (Alvarez-Buylla et al., 2000; de Bodt et al., 2003; Parenicova et al., 2003). The MADS family can be divided into two groups based on molecular evolutionary criteria. The vast majority of plant MADS genes of known function are type II MADS genes. The majority of type II MADS proteins have a characteristic domain structure. The MADS domain is located at the N-terminal end and encodes DNA binding, nuclear localization, and dimerization functions (McGonigle et al., 1996; Riechmann and Meyerowitz, 1997; Immink et al., 2002). A second conserved domain, the K domain, mediates protein–protein interaction and dimerization functions (Fan et al., 1997; Yang et al., 2003a). In a subset of plant MADS proteins, the C domain encodes a transcriptional activation domain (Moon et al., 1999; Honma and Goto, 2001). The C domain also has been reported to play a role in the formation of higher order MADS complexes (Egea-Cortines et al., 1999; Honma and Goto, 2001). Recently, the extreme C-terminal end of AP3 was demonstrated to play a role in functional specificity (Lamb and Irish, 2003).
Type I MADS genes do not encode a K domain. Even though there are
All MADS proteins studied to date bind to DNA as dimers, either homodimers or heterodimers. In Arabidopsis, AG has been demonstrated to bind to DNA either as a homodimer or as a heterodimer with SEP1 (Huang et al., 1996
The failure of floral organs to develop with the correct identity in A, B, C, and E class mutants demonstrates that the ABCE genes are necessary to specify floral organ identity. When expressed ectopically, the ABCE genes are sufficient to direct organ identity in flowers but not in vegetative leaves. For example, ectopic expression of both B class genes (35S:AP3 and 35S:PI) results in flowers that consist of two outer whorls of petals and two inner whorls of stamens, but leaves remain largely vegetative (Krizek and Meyerowitz, 1996 ). Based on this finding, it was concluded that AP3 and PI are sufficient, within the flower, to direct petal and stamen identity. Similarly, 35S:AG, 35S:SEP1, 35S:SEP2, and 35S:SEP3 do not alter the identity of the vegetative leaves. However, when the E class gene SEP3 is expressed ectopically together with AP3 and PI, both rosette and cauline leaves are converted to organs that resemble petals (Honma and Goto, 2001; Pelaz et al., 2001b). Furthermore, when AG is expressed ectopically together with AP3, PI, and SEP3, the cauline leaves are converted to organs that resemble stamens (Honma and Goto, 2001). These studies demonstrate that the E class genes, together with the ABC genes, are sufficient to direct floral organ identity in vegetative organs.
Plant MADS proteins have been demonstrated to associate in complexes larger than dimers (Egea-Cortines et al., 1999 ; Honma and Goto, 2001; Ferrario et al., 2003; Yang et al., 2003b). This has led to a molecular model, the "quartet" model, which has received broad publicity but in fact is supported by only a limited amount of experimental evidence (Jack, 2001; Theissen, 2001; Theissen and Saedler, 2001; Eckardt, 2003).
The quartet model (Theissen, 2001 The quartet model makes predictions about the composition of the tetramers in the four whorls of the flower (Figure 2). Specifically, in whorl 2, a combination of AP3/PI-SEP/AP1 is postulated to specify petals; in whorl 3, AP3/PI-SEP/AG is postulated to specify stamens; and in whorl 4, AG/AG-SEP/SEP is postulated to specify carpels.
One line of evidence that MADS proteins form higher order complexes comes from yeast two-hybrid and three-hybrid experiments. A two-hybrid screen using AG as bait identified SEP1, SEP2, and SEP3 as interacting proteins (Fan et al., 1997
Evidence suggesting that these higher order MADS complexes are functional comes from DNA binding assays performed with Antirrhinum MADS proteins. In one key experiment, a probe containing two MADS binding sites exhibited enhanced DNA binding in the presence of both SQUAMOSA (SQUA) (the AP1 ortholog) and DEFICIENS (DEF)/GLO (the AP3/PI orthologs) compared with DEF/GLO or SQUA alone (Egea-Cortines et al., 1999 At present, the nature of MADS protein complexes in planta is completely uncharacterized. For example, even though there is abundant evidence that AP3 and PI form a heterodimer in vitro and in yeast, an AP3/PI heterodimer has not been isolated from plant cells. Even less is known about other proteins that might be components of plant MADS protein complexes. Future work will focus on the biochemical characterization of MADS protein complexes from plant cells.
Not only are AP1 and LFY necessary to specify floral meristem identity, they also are crucial to activate the floral organ identity genes. During early stages of flower development, both LFY and AP1 are expressed throughout the floral meristem (Mandel et al., 1992 ; Weigel et al., 1992; Gustafson-Brown et al., 1994; Blazquez et al., 1997). Despite the broad expression of LFY and AP1, the B class genes AP3 and PI and the C class gene AG are activated in only a subset of cells in the floral meristem. The B class genes are activated in the precursor cells for petals and stamens in whorls 2 and 3, and the C class gene AG is activated in the precursor cells for the stamens and carpels in whorls 3 and 4. Clearly, other factors must act in concert with LFY and AP1 to properly activate B and C class genes in spatially restricted patterns.
Evidence that LFY is important for the initial activation of AP3 comes from analysis of the AP3 expression pattern in lfy mutants. Both the size of the domain and the level of AP3 expression are reduced in lfy mutants (Weigel and Meyerowitz, 1993 ). Positive regulation of AP3 by LFY may be direct, because LFY binds in vitro to a LFY binding site located in an AP3 promoter element that directs the establishment of AP3 expression during early floral stages (Figure 3) (Hill et al., 1998). Surprisingly, mutation of this LFY binding site does not disrupt LFY activation of AP3 (Lamb et al., 2002). It appears that either this element is not the bona fide LFY binding site in vivo or there are redundant LFY activation elements in the AP3 promoter. Some of these LFY activation elements might function indirectly, thus explaining why LFY fails to bind to other regions of the AP3 promoter.
Proper activation of the B class gene AP3 is also dependent on UNUSUAL FLORAL ORGANS (UFO). ufo mutants resemble B class mutants in that petal and stamen numbers are reduced, which correlates with a reduction in the level of AP3 RNA during early floral stages (Levin and Meyerowitz, 1995 ; Wilkinson and Haughn, 1995). Ectopic expression of UFO (35S:UFO) results in the partial conversion of first whorl sepals to petals and fourth whorl carpels to stamens; these organ identity conversions resemble those in 35S:AP3 and 35S:PI. Not surprisingly, the sepal-to-petal and carpel-to-stamen transformations in 35S:UFO require AP3 and PI activity (Lee et al., 1997).
All known UFO functions require LFY; lfy is epistatic to both ufo and 35S:UFO (Lee et al., 1997
UFO RNA is expressed in three discrete patterns during early floral development. First, although UFO RNA is not detected in very young floral buttresses that have only recently differentiated from the inflorescence shoot meristem (stage 1), UFO RNA is detectable in slightly older floral meristems, before the morphological differentiation of any of the floral organ primordia (stage 2), in the precursor cells for whorls 3 and 4 (Ingram et al., 1995
UFO encodes an F-box protein (Simon et al., 1994
In addition to its role in activating B class genes, UFO has at least two other important functions. ufo mutants exhibit dramatic defects in floral organ positioning; the arrangement of organs, particularly in the second and third whorls, varies dramatically from flower to flower (Levin and Meyerowitz, 1995
A role for UFO in whorl 2 petal development is suggested by analysis of a class of weak ufo alleles, such as ufo-11, that fail to develop petals but have normal floral organ positioning. The fact that these ufo mutants develop normal stamens suggests that the ability of UFO to activate B class genes has not been compromised (Durfee et al., 2003
AP1 also plays a role in activating UFO. Specifically, AP1 is necessary for the accumulation of UFO RNA that occurs at the base of the petals during later floral stages (i.e., stage 5). In ap1 mutants, UFO RNA is not detectable at the base of the petals and whorl 2 organ development is largely suppressed (Ng and Yanofsky, 2001a
Like UFO and LFY, AP1 plays a role in activating B class genes (Figure 3). Although B class expression in whorls 2 and 3 is normal in ap1 mutants during early floral stages (Weigel and Meyerowitz, 1993
Additional evidence that the positive regulatory effects of AP1 on B class activation are dependent on UFO comes from analysis of an activated form of AP1 that contains the strong viral VP16 activation domain. ap1 mutant flowers expressing an AP1:VP16 fusion exhibit a conversion of whorl 1 bracts to petal-like organs. The effects of AP1:VP16 are dependent on UFO because petals fail to develop in AP1:VP16 ufo (Ng and Yanofsky, 2001a
Although our understanding has been clarified considerably in recent years, it remains unclear precisely how B class genes are activated during the early stages of flower development. The long-postulated repressor of AP3 that is the putative target of SCFUFO degradation has not been identified. Also, there are almost certainly additional unidentified activators of AP3, because in strong loss-of-function lfy and ufo mutants, AP3 RNA is still detectable. Even in ap1 lfy double mutants, a low level of AP3 RNA is detectable in a small group of cells (Weigel and Meyerowitz, 1993
LFY is a positive activator not only of AP3 but also of AG. An activated form of LFY, fused to the strong VP16 activation domain, results in flowers with carpels and stamens in whorls 1 and 2, respectively, similar to AG overexpression lines, suggesting that one function of LFY is to activate AG (Parcy et al., 1998 ). Two redundant control regions that mediate the activation of AG by LFY map to the large second intron of AG (Busch et al., 1999). AG is unusual in that its second intron contains regulatory signals that are sufficient to mimic the wild-type AG temporal and spatial expression patterns (Sieburth and Meyerowitz, 1997; Bomblies et al., 1999; Busch et al., 1999; Deyholos and Sieburth, 2000). LFY protein binds in vitro to two elements in the AG second intron. Mutation of the LFY binding sites in these elements severely compromises the ability of LFY to activate AG (Busch et al., 1999).
As is the case with AP3, LFY functions together with a region-specific coactivator to activate AG in whorls 3 and 4. LFY activates AG in a subset of AG-expressing cells, together with the stem cell–promoting gene WUSCHEL (WUS) (Figure 3) (Mayer et al., 1998
After AG is activated in whorls 3 and 4 during early floral stages, AG, in turn, downregulates WUS in whorls 3 and 4. Failure to downregulate WUS in an ag mutant results in a loss of floral determinacy attributable to the meristem proliferation activity of WUS (Lenhard et al., 2001
The ABC genes are activated initially by floral meristem identity genes such as LFY, AP1, and UFO, but later patterns of expression are refined by interactions among the ABC genes themselves. The mutually repressive interaction between A and C class genes is one of the basic tenets of the ABC model (Figure 2). We have a partial understanding of how this repression is mediated. The two A class genes AP1 and AP2 are the first ABC genes to be expressed in the flower. As mentioned above, AP1 is not only an A class gene but also functions to specify floral meristem identity. To perform its role in floral meristem specification, AP1 is expressed in all four whorls of very young flower primordia (stage 1 flowers). Similarly, AP2 RNA accumulates in all four whorls of the flower throughout flower development; the AP2 RNA expression pattern is not spatially restricted in the flower at any stage (Jofuku et al., 1994 ). At the time when floral organs begin to morphologically differentiate from the floral meristem (stage 3), AG is activated in whorls 3 and 4 by LFY and WUS (Lenhard et al., 2001; Lohmann et al., 2001). AG, in turn, represses AP1 in whorls 3 and 4 (Gustafson-Brown et al., 1994). At present, it is not known if the AG protein binds directly to the AP1 promoter to mediate this repression.
By stage 5, AP1 RNA accumulates in whorls 1 and 2 and AG RNA accumulates in whorls 3 and 4. However, AP2 RNA remains detectable in all four floral whorls (Jofuku et al., 1994
To complicate the picture further, the repression of AG does not depend solely on AP2. Several other genes, including LEUNIG (LUG), SUESS (SEU), STERILE APETALA (SAP), and AINTEGUMENTA (ANT), also contribute to AG repression in whorls 1 and 2 (Liu and Meyerowitz, 1995
Several of these putative AG repressors encode proteins that function as repressors in yeast and animals. CLF encodes a homolog of the Drosophila Polycomb group protein Enhancer of Zeste (Goodrich et al., 1997
In whorls 1 and 2, LUG, SEU, ANT, and AP2 function to repress AG. One model suggests that LUG and SEU form a corepressor complex that is targeted to DNA by sequence-specific DNA binding proteins such as AP2 and ANT. It has been shown that LUG and SEU interact in a yeast two-hybrid assay (Franks et al., 2002
For several years, it has been unclear how AG repression is confined to whorls 1 and 2, because RNA for AP2, SEU, LUG, and ANT is detectable in all four whorls of the flower. Recent work suggests that AP2, one of the proteins of the putative AG repression complex, is localized to whorls 1 and 2. Interestingly, this post-transcriptional regulation of AP2 is mediated by translational repression mediated by a miRNA (Chen, 2004
One of the ongoing debates in the field concerns whether AP2 orthologs function as A class genes throughout the angiosperms. A class function was initially postulated based on the phenotype of mutants such as ap2 in Arabidopsis and ovulata in Antirrhinum, both of which result in homeotic conversions of sepals to carpels and petals to stamens (Bowman et al., 1989
The solution to the AG repression dilemma came out of experiments aimed at characterization of the C class pathway. To isolate additional components of the C class pathway, enhancers of a weak ag allele, ag-4, were characterized. ag-4 flowers are indeterminate and exhibit a (sepal-petal-stamen)n repeat pattern (Sieburth et al., 1995 ). By contrast, strong ag alleles such as ag-3 exhibit a (sepal-petal-petal)n repeat pattern. One strong extragenic ag-4 enhancer was identified that produced flowers that resembled ag-3. The enhancer phenotype was attributable to mutations in two unlinked genes named HUA1 and HUA2 (Chen and Meyerowitz, 1999). As single mutants, both hua1 and hua2 exhibit weak enhancement of ag-4. Similarly, hua1 hua2 double mutants (in an AG+ background) exhibit a very weak ag-like phenotype. Surprisingly, both hua1 and hua2 single mutants exhibit a wild-type floral phenotype. In retrospect, it is quite fortunate that both hua1 and hua2 were mutated simultaneously in the original ag-4 enhancer screen, because the hua1 hua2 double mutant served as the basis for the isolation of the next set of very important genes.
The second genetic screen was designed to isolate enhancers of the hua1 hua2 double mutant. A number of enhancers were isolated that exhibited an enhanced ag phenotype. These enhancers were categorized into several loci called the HUA enhancers, HEN1, HEN2, and HEN4 (Chen et al., 2002
The first clue that the HUA and HEN genes might be involved in RNA metabolism came from the cloning of HUA1. HUA1 encodes a nuclear RNA binding protein with six CCCH zinc fingers (Li et al., 2001 ). Similarly, HEN2 encodes a DExH-box RNA helicase, similar to yeast DOB1 (Western et al., 2002). HEN4 encodes a KH domain protein (Cheng et al., 2003); the KH domain has been demonstrated to possess single-stranded RNA binding activity. HUA2 encodes a protein with less obvious similarity to proteins involved in RNA metabolism (Chen and Meyerowitz, 1999).
HUA1, HUA2, HEN2, and HEN4 play roles in the proper processing of AG mRNA. As described above, the large second intron of AG contains critical regulatory signals that mediate activation by LFY and WUS and repression by A class activity. In the hen and hua mutants, partially processed AG RNAs accumulate at the expense of the fully processed AG mRNA. Characterization of these partially processed RNAs reveals that they contain exons 1 and 2 and the majority of the large intron 2, but not intron 1 or exons 3 to 7. These partially processed AG RNAs contain poly(A) sequences adjacent to intron 2 sequences, suggesting that premature transcriptional termination and polyadenylation have occurred within intron 2. Although processing defects were observed in hua1, hua2, and hen4 single mutants, increasingly severe defects were observed in double and triple mutants. Evidence that the ag-like phenotype that is observed in the hen and hua mutants is attributable to a reduction in fully processed AG mRNA comes from experiments showing that transgenic plants that ectopically express an AG cDNA (35S:AGcDNA), which is not dependent on RNA processing for function, is able to rescue the stamen and carpel defects of hua1 hua2 hen4 triple mutants (Cheng et al., 2003
Evidence suggesting that HUA1 and HEN4 function together in a complex comes from the demonstration that the nuclear localization of HEN4 is dependent on HUA1; specifically, in a hua1 mutant, HEN4 is not properly localized to the nucleus. In addition, both fluorescence energy resonance transfer and yeast two-hybrid analyses support the hypothesis that HUA1 and HEN4 exhibit a direct protein–protein interaction (Cheng et al., 2003
The pleiotropic phenotypes of hen and hua mutants suggest that the HUA/HEN genes are not specific for the AG pathway. However, it is not the case that the HEN/HUA genes are general factors that function in RNA processing of all genes, because large aberrantly processed RNAs were not detected for the MADS genes AP3, PI, AP1, and FLC (Cheng et al., 2003 The present model is that HUA1 and HEN4 form a complex that may or may not include HUA2 and that this complex either (1) suppresses cryptic polyadenylation sequences in the AG second intron or (2) promotes the removal of intron 2 before the cryptic polyadenylation sites in intron 2 are activated. Future work on the role of the HEN and HUA genes in AG mRNA processing will distinguish between these two models.
HEN1 encodes a protein that functions similarly to DICERLIKE1 (DCL1), a protein important for the production of miRNAs and small interfering RNAs (reviewed by Bartel and Bartel, 2003 ). Mutations in DCL1 were isolated in a variety of screens for mutants in embryo development (named abnormal suspensor [Golden et al., 2002]), ovule development (named short integuments [Ray et al., 1996]), and flower development (named carpel factory [Jacobsen et al., 1999]). miRNAs are postulated to function to control the expression of specific genes by complementary base pairing with mRNA, resulting in either degradation of the mRNA or translational repression.
The discovery that animal genomes encoded hundreds of miRNAs (Carrington and Ambros, 2003
Additional evidence that miRNA172 regulates AP2 comes from ectopic expression experiments. Ectopic expression of miRNA172 (35S:miRNA172) results in flowers that exhibit an ap2 phenotype, suggesting that miRNA172 downregulates AP2 activity. Surprisingly, AP2 RNA levels are unaffected in 35S:miRNA172 but AP2 protein levels are reduced. This finding suggests that miRNA172, unlike other known plant miRNAs, functions by regulating the translation of AP2, not by promoting the degradation of the AP2 RNA. In situ hybridization experiments indicate that miRNA172 is expressed at the highest levels in whorls 3 and 4 of the flower, the region of the flower where A class activity does not function to repress C activity (Chen, 2004
There is a single putative miRNA172 binding site in AP2 located near the 3' end of the protein coding region. To test whether this putative binding site is functional, mutations were introduced and the mutated AP2 gene was expressed ectopically (35S:
These experiments support the following model (Figure 2). AP2 RNA is expressed in all four floral whorls. In whorls 3 and 4, AP2 RNA is repressed translationally by miRNA172, which is expressed at the highest levels in whorls 3 and 4 (Chen, 2004
The finding in 1994 that the AP2 mRNA was not restricted spatially in the flower (Jofuku et al., 1994
The role of miRNA172 in AP2 repression does help explain another old observation that was puzzling and lacked a satisfactory explanation. In ag mutants, AG mRNA remains expressed in whorls 3 and 4 throughout flower development (Gustafson-Brown et al., 1994
AP2 is not the only target of miRNA172; recent work also demonstrates that miRNA172 also controls an AP2 family gene involved in flowering time control (Aukerman and Sakai, 2003 ). This AP2 family gene, named TARGET OF EAT1 (TOE1), was identified because it exhibited a late-flowering phenotype when it was overexpressed in an activation-tagged line. The late-flowering phenotype could be mimicked by ectopically expressing TOE1 (35S:TOE1). These experiments suggests that TOE1 normally functions as a repressor of the vegetative-to-reproductive floral transition. Consistent with this hypothesis, expression analysis in wild-type flowers revealed that TOE1 RNA levels were downregulated at the floral transition.
A second activation-tagged line, named early activation tagged, dominant (eat-D), exhibited an early-flowering phenotype and produced flowers that resembled ap2 mutant flowers (Aukerman and Sakai, 2003
The progress in the flower development field in the last 15 years has been impressive, but there are still many unanswered questions. Although the idea that the floral control genes function in a temporal hierarchy has been around for more than a decade, there are very few examples in which a regulatory relationship can be backed up with molecular and biochemical data that demonstrate a direct interaction (the gray arrows in Figures 1 and 3 and the red arrow in Figure 2 indicate direct interactions). Part of the problem is attributable to the fact that it has been difficult, until recently, to determine the target genes for transcription factors. Microarray technology should allow the targets of the floral control genes to be determined. Efforts to characterize targets for floral transcription factors are beginning (Zik and Irish, 2003 ) and should accelerate in the next several years. In these efforts, it will be important to distinguish direct from indirect targets. For the direct targets, bioinformatics will play a key role in identifying cis-acting sequences in the promoters for the target genes that are upregulated and downregulated in the presence or absence of a given transcription factor. Another key area of future research is the biochemical characterization of biological complexes. Much better tools are available at present for isolating and purifying proteins from plant extracts. Proteomics approaches such as mass spectroscopy have the potential to define components of biochemical complexes. For a given floral transcription factor, an important future goal is to characterize the types of complexes involved in transcriptional activation and repression in various organs at different stages of development. The long-term goal is to try to correlate cis-acting promoter sequences in target genes (identified by microarray/bioinformatics) with specific protein complexes (identified by protein purification and mass spectrometry). The efforts of many scientists, working with Arabidopsis and many other species, promise to lead to a better understanding of the molecular and genetic mechanisms of floral control in the years to come.
I thank Xuemei Chen for communicating results before publication. I am grateful to laboratory members for comments on the manuscript. T.J. is supported by funds from the National Science Foundation (MCB-0090742) and the U.S. Department of Agriculture (2003-02586).
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.017038. Received September 12, 2003; accepted January 9, 2004.
Alvarez, J., Guli, C.L., Yu, X.-H., and Smyth, D.R. (1992). terminal flower: A gene affecting inflorescence development in Arabidopsis thaliana. Plant J. 2, 103–116.[CrossRef][Web of Science] Alvarez, J., and Smyth, D.R. (1999). CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126, 2356–2375.
Alvarez-Buylla, E.R., Pelaz, S., Liljegren, S.J., Gold, S.E., Burgeff, C., Ditta, G.S., de Pouplana, L.R., Martinez-Castilla, L., and Yanofsky, M.F. (2000). An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl. Acad. Sci. USA 97, 5328–5333. Ambrose, B.A., Lerner, D.R., Ciceri, P., Padilla, C.M., Yanofsky, M.F., and Schmidt, R.J. (2000). Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell 5, 569–579.[CrossRef][Web of Science][Medline] Angenent, G.C., Franken, J., Busscher, M., van Dijken, A., van Went, J.L., Dons, H.J., and van Tunen, A.J. (1995). A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell 7, 1569–1582.[Abstract] Angenent, G.C., Franken, J., Busscher, M., Weiss, D., and van Tunen, A.J. (1994). Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J. 5, 33–44.[CrossRef][Web of Science][Medline]
Aukerman, M.J., and Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15, 2730–2741.
Bartel, B., and Bartel, D.P. (2003). MicroRNAs: At the root of plant development? Plant Physiol. 132, 709–717.
Blazquez, M.A., Green, R., Nilsson, O., Sussman, M.R., and Weigel, D. (1998). Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10, 791–800. Blazquez, M.A., Soowal, L.N., Lee, I., and Weigel, D. (1997). LEAFY expression and flower initiation in Arabidopsis. Development 124, 3835–3844.[Abstract] Blazquez, M.A., and Weigel, D. (2000). Integration of floral inductive signals in Arabidopsis. Nature 404, 889–892.[CrossRef][Medline] Bomblies, K., Dagenais, N., and Weigel, D. (1999). Redundant enhancers mediate transcriptional repression of AGAMOUS by APETALA2. Dev. Biol. 216, 260–264.[CrossRef][Web of Science][Medline] Borner, R., Kampmann, G., Chandler, J., Gleissner, R., Wisman, E., Apel, K., and Melzer, S. (2000). A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24, 591–599.[CrossRef][Web of Science][Medline]
Bowman, J.L., Alvarez, J., Weigel, D., Meyerowitz, E.M., and Smyth, D.R. (1993). Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119, 721–743.
Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1, 37–52. Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1991). Genetic interactions among floral homeotic genes of Arabidopsis. Development 112, 1–20.[Abstract] Bradley, D., Carpenter, R., Copsey, L., Vincent, C., Rothstein, S., and Coen, E. (1996). Control of inflorescence architecture in Antirrhinum. Nature 379, 791–797.[CrossRef][Medline] Bradley, D., Carpenter, R., Sommer, H., Hartley, N., and Coen, E. (1993). Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72, 85–95.[CrossRef][Web of Science][Medline]
Bradley, D., Ratcliffe, O., Vincent, C., Carpenter, R., and Coen, E. (1997). Inflorescence commitment and architecture in Arabidopsis. Science 275, 80–83.
Busch, M.A., Bomblies, K., and Weigel, D. (1999). Activation of a floral homeotic gene in Arabidopsis. Science 285, 585–587.
Byzova, M.V., Franken, J., Aarts, M.G., de Almeida-Engler, J., Engler, G., Mariani, C., Van Lookeren Campagne, M.M., and Angenent, G.C. (1999). Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development. Genes Dev. 13, 1002–1014.
Carpenter, R., and Coen, E.S. (1990). Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev. 4, 1483–1493.
Carrington, J.C., and Ambros, V. (2003). Role of microRNAs in plant and animal development. Science 301, 336–338.
Chen, X. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022–2025.
Chen, X., Liu, J., and Jia, D. (2002). HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129, 1085–1094. Chen, X., and Meyerowitz, E.M. (1999). HUA1 and HUA2 are two members of the floral homeotic AGAMOUS pathway. Mol. Cell 3, 349–360.[CrossRef][Web of Science][Medline] Cheng, Y., Kato, N., Wang, W., Li, J., and Chen, X. (2003). Two RNA binding proteins, HEN4 and HUA1, act in the processing of AGAMOUS pre-mRNA in Arabidopsis thaliana. Dev. Cell 4, 53–66.[CrossRef][Web of Science][Medline] Coen, E.S., and Meyerowitz, E.M. (1991). The war of the whorls: Genetic interactions controlling flower development. Nature 353, 31–37.[CrossRef][Medline] Coen, E.S., Romero, J.M., Doyle, S., Elliot, R., Murphy, G., and Carpenter, R. (1990). Floricula: A homeotic gene required for flower development in Antirrhinum majus. Cell 63, 1311–1322.[CrossRef][Web of Science][Medline] Colombo, L., Franken, J., Koetje, E., van Went, J., Dons, H., Angenent, G., and van Tunen, A. (1995). The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7, 1859–1868.[Abstract]
Conner, J., and Liu, Z. (2000). LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower development. Proc. Natl. Acad. Sci. USA 97, 12902–12907.
Corbit, K.C., Trakul, N., Eves, E.M., Diaz, B., Marshall, M., and Rosner, M.R. (2003). Activation of Raf-1 signaling by protein kinase C through a mechanism involving Raf kinase inhibitory protein. J. Biol. Chem. 278, 13061–13068. de Bodt, S., Raes, J., Florquin, K., Rombauts, S., Rouze, P., Theissen, G., and Van der Peer, Y. (2003). Genomewide structural annotation and evolutionary analysis of the type I MADS-box genes in plants. J. Mol. Evol. 56, 573–586.[CrossRef][Web of Science][Medline]
Deyholos, M., and Sieburth, L. (2000). Separable whorl-specific expression and negative regulation by enhancer elements within the AGAMOUS second intron. Plant Cell 12, 1799–1810. Drews, G.N., Bowman, J.L., and Meyerowitz, E.M. (1991). Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65, 991–1002.[CrossRef][Web of Science][Medline]
Durfee, T., Roe, J.L., Sessions, R.A., Inouye, C., Serikawa, K., Feldmann, K.A., Weigel, D., and Zambryski, P.C. (2003). The F-box-containing protein UFO and AGAMOUS participate in antagonistic pathways governing early petal development in Arabidopsis. Proc. Natl. Acad. Sci. USA 100, 8571–8576.
Eckardt, N.A. (2003). MADS monsters: Controlling floral organ identity. Plant Cell 15, 803–805. Egea-Cortines, M., Saedler, H., and Sommer, H. (1999). Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS, and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J. 18, 5370–5379.[CrossRef][Web of Science][Medline] Elliott, R.C., Betzner, A.S., Huttner, E., Oakes, M.P., Tucker, W.Q., Gerentes, D., Perez, P., and Smyth, D.R. (1996). AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8, 155–168.[Medline] Fan, H.-Y., Hu, Y., Tudor, M., and Ma, H. (1997). Specific interactions between K domains of AG and AGLs, members of the MADS domain family of DNA binding proteins. Plant J. 12, 999–1010.[CrossRef][Web of Science][Medline]
Favaro, R., Pinyopich, A., Battaglia, R., Kooiker, M., Borghi, L., Ditta, G., Yanofsky, M.F., Kater, M.M., and Colombo, L. (2003). MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15, 2603–2611. Ferrandiz, C., Gu, Q., Martienssen, R., and Yanofsky, M.F. (2000). Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127, 725–734.[Abstract]
Ferrario, S., Immink, R.G., Shchennikova, A., Busscher-Lange, J., and Angenent, G.C. (2003). The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell 15, 914–925. Fornara, F., Marziani, G., Mizzi, L., Kater, M., and Colombo, L. (2003). MADS-box genes controlling flower development in rice. Plant Biol. 5, 16–22.
Franks, R.G., Wang, C., Levin, J.Z., and Liu, Z. (2002). SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129, 253–263. Frohlich, M.W., and Parker, D.S. (2000). The mostly male theory of flower evolutionary origins: From genes to fossils. Syst. Bot. 25, 155–170.[CrossRef] Gendall, A.R., Levy, Y.Y., Wilson, A., and Dean, C. (2001). The VERNALIZATION2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107, 525–535.[CrossRef][Web of Science][Medline]
Gocal, G.F., King, R.W., Blundell, C.A., Schwartz, O.M., Andersen, C.H., and Weigel, D. (2001). Evolution of floral meristem identity genes: Analysis of Lolium temulentum genes related to APETALA1 and LEAFY of Arabidopsis. Plant Physiol. 125, 1788–1801.
Golden, T.A., Schauer, S.E., Lang, J.D., Pien, S., Mushegian, A.R., Grossniklaus, U., Meinke, D.W., and Ray, A. (2002). SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol. 130, 808–822. Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E.M., and Coupland, G. (1997). A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386, 44–51.[CrossRef][Medline] Goto, K., Kyozuka, J., and Bowman, J.L. (2001). Turning floral organs into leaves, leaves into floral organs. Curr. Opin. Genet. Dev. 11, 449–456.[CrossRef][Web of Science][Medline]
Goto, K., and Meyerowitz, E.M. (1994). Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8, 1548–1560. Gu, Q., Ferrandiz, C., Yanofsky, M.F., and Martienssen, R. (1998). The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 1509–1517.[Abstract] Gustafson-Brown, C., Savidge, B., and Yanofsky, M.F. (1994). Regulation of the Arabidopsis floral homeotic gene APETALA1. Cell 76, 131–143.[CrossRef][Web of Science][Medline] Hartmann, U., Hohmann, S., Nettesheim, K., Wisman, E., Saedler, H., and Huijser, P. (2000). Molecular cloning of SVP, a negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351–360.[CrossRef][Web of Science][Medline] Hayama, R., and Coupland, G. (2003). Shedding light on the circadian clock and the photoperiodic control of flowering. Curr. Opin. Plant Biol. 6, 13–19.[CrossRef][Web of Science][Medline]
He, Y., Michaels, S.D., and Amasino, R.M. (2003). Regulation of flowering time by histone acetylation in Arabidopsis. Science 302, 1751–1754. Hepworth, S.R., Valverde, F., Ravenscroft, D., Mouradov, A., and Coupland, G. (2002). Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 21, 4327–4337.[CrossRef][Web of Science][Medline] Hill, T.A., Day, C.D., Zondlo, S.C., Thackeray, A., and Irish, V.F. (1998). Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development 125, 1711–1721.[Abstract] Honma, T., and Goto, K. (2001). Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409, 525–529.[CrossRef][Medline] Huang, H., Tudor, M., Su, T., Zhang, Y., Hu, Y., and Ma, H. (1996). DNA binding properties of two Arabidopsis MADS domain proteins: Binding consensus and dimer formation. Plant Cell 8, 81–94.[Abstract] Huijser, P., Klein, J., Lönnig, W.-E., Meijer, H., Saedler, H., and Sommer, H. (1992). Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J. 11, 1239–1249.[Web of Science][Medline] Immink, R.G., Ferrario, S., Busscher-Lange, J., Kooiker, M., Busscher, M., and Angenent, G.C. (2003). Analysis of the petunia MADS-box transcription factor family. Mol. Genet. Genomics 268, 598–606.[Web of Science][Medline]
Immink, R.G., Gadella, T.W., Ferrario, S., Busscher, M., and Angenent, G.C. (2002). Analysis of MADS box protein-protein interactions in living plant cells. Proc. Natl. Acad. Sci. USA 99, 2416–2421. Ingram, G.C., Goodrich, J., Wilkinson, M.D., Simon, R., Haughn, G.W., and Coen, E.S. (1995). Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. Plant Cell 7, 1501–1510.[Abstract]
Irish, V.F., and Sussex, I.M. (1990). Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2, 741–753. Jack, T. (2001). Relearning our ABCs: New twists on an old model. Trends Plant Sci. 6, 310–316.[CrossRef][Web of Science][Medline] Jack, T., Fox, G.L., and Meyerowitz, E.M. (1994). Arabidopsis homeotic gene APETALA3 ectopic expression: Transcriptional and post-transcriptional regulation determine floral organ identity. Cell 76, 703–716.[CrossRef][Web of Science][Medline] Jacobsen, S.E., Running, M.P., and Meyerowitz, E.M. (1999). Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126, 5231–5243.[Abstract] Jofuku, K.D., den Boer, B.G.W., Van Montagu, M., and Okamuro, J.K. (1994). Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6, 1211–1225.[Abstract]
Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R., and Dean, C. (2000). Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347.
Kardailsky, I., Shukla, V.K., Ahn, J.H., Dagenais, N., Christensen, S.K., Nguyen, J.T., Chory, J., Harrison, M.J., and Weigel, D. (1999). Activation tagging of the floral inducer FT. Science 286, 1962–1965. Keck, E., McSteen, P., Carpenter, R., and Coen, E. (2003). Separation of genetic functions controlling organ identity in flowers. EMBO J. 22, 1058–1066.[CrossRef][Web of Science][Medline]
Kempin, S.A., Savidge, B., and Yanofsky, M.F. (1995). Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267, 522–525. Klucher, K.M., Chow, H., Reiser, L., and Fischer, R.L. (1996). The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8, 137–153.[Abstract]
Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M., and Araki, T. (1999). A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960–1962.
Kohler, C., Hennig, L., Spillane, C., Pien, S., Gruissem, W., and Grossniklaus, U. (2003). The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev. 17, 1540–1553. Koornneef, M., Alonso-Blanco, C., Peeters, A.J., and Soppe, W. (1998). Genetic control of flowering time in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 345–370.[CrossRef][Web of Science][Medline] Koornneef, M., Hanhart, C.J., and Vanderveen, J.H. (1991). A genetic and physiological analysis of late flowering mutations in Arabidopsis thaliana. Mol. Gen. Genet. 229, 57–66.[Web of Science][Medline] Krizek, B.A., and Meyerowitz, E.M. (1996). The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 112, 11–22.
Krizek, B.A., Prost, V., and Macias, A. (2000). AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. Plant Cell 12, 1357–1366.
Lamb, R.S., Hill, T.A., Tan, Q.K.-G., and Irish, V.F. (2002). Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129, 2079–2086.
Lamb, R.S., and Irish, V.F. (2003). Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc. Natl. Acad. Sci. USA 100, 6558–6563.
Laufs, P., Coen, E., Kronenberger, J., Traas, J., and Doonan, J. (2003). Separable roles of UFO during floral development revealed by conditional restoration of gene function. Development 130, 785–796. Laux, T., Mayer, K.F.X., Berger, J., and Jürgens, G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87–96.[Abstract]
Lee, H., Suh, S.-S., Park, E., Cho, E., Ahn, J.H., Kim, S.-G., Lee, J.S., Kwon, Y.M., and Lee, I. (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366–2376. Lee, I., Wolfe, D.S., and Weigel, D. (1997). A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS. Curr. Biol. 7, 95–104.[CrossRef][Web of Science][Medline] Lenhard, M., Bohnert, A., Jürgens, G., and Laux, T. (2001). Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105, 805–814.[CrossRef][Web of Science][Medline] Levin, J.Z., and Meyerowitz, E.M. (1995). UFO: An Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7, 529–548.[Abstract]
Li, J., Jia, D., and Chen, X. (2001). HUA1, a regulator of stamen and carpel identities in Arabidopsis, codes for a nuclear RNA binding protein. Plant Cell 13, 2269–2281. Liljegren, S.J., Ditta, G.S., Eshed, Y., Savidge, B., Bowman, J.L., and Yanofsky, M.F. (2000). SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766–770.[CrossRef][Medline]
Liljegren, S.J., Gustafson-Brown, C., Pinyopich, A., Ditta, G.S., and Yanofsky, M.F. (1999). Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11, 1007–1018. Liu, Z., and Meyerowitz, E.M. (1995). LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121, 975–991.[Abstract] Lohmann, J.U., Hong, R.L., Hobe, M., Busch, M.A., Parcy, F., Simon, R., and Weigel, D. (2001). A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105, 793–803.[CrossRef][Web of Science][Medline] Lohmann, J.U., and Weigel, D. (2002). Building beauty: The genetic control of floral patterning. Dev. Cell 2, 135–142.[CrossRef][Web of Science][Medline]
Maes, T., Van De Steene, N., Zethof, J., Karimi, M., D'Hauw, M., Mares, G., Van Montagu, M., and Gerats, T. (2001). Petunia AP2-like genes and their role in flower and seed development. Plant Cell 13, 229–244. Mandel, M.A., Gustafson-Brown, C., Savidge, B., and Yanofsky, M.F. (1992). Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360, 273–277.[CrossRef][Medline] Mandel, M.A., and Yanofsky, M.F. (1995). A gene triggering flower formation in Arabidopsis. Nature 377, 522–524.[CrossRef][Medline] Mayer, K.F.X., Schoof, H., Haecker, A., Lenhard, M., and Jürgens, G. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805–815.[CrossRef][Web of Science][Medline]
McGonigle, B., Bouhidel, K., and Irish, V.F. (1996). Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes Dev. 10, 1812–1821.
Michaels, S.D., and Amasino, R.M. (1999). FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949–956. Michaels, S.D., Ditta, G., Gustafson-Brown, C., Pelaz, S., Yanofsky, M., and Amasino, R.M. (2003). AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J. 33, 867–874.[CrossRef][Web of Science][Medline] Mimida, N., Goto, K., Kobayashi, Y., Araki, T., Ahn, J.H., Weigel, D., Murata, M., Motoyoshi, F., and Sakamoto, W. (2001). Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes Cells 6, 327–336.[Abstract] Moon, J., Suh, S.S., Lee, H., Choi, K.R., Hong, C.B., Paek, N.C., Kim, S.G., and Lee, I. (2003). The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J. 35, 613–623.[CrossRef][Web of Science][Medline]
Moon, Y.-W., Kang, H.-G., Jung, J.-Y., Jeon, J.-S., Sung, S.-K., and An, G. (1999). Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol. 120, 1193–1203.
Mouradov, A., Cremer, F., and Coupland, G. (2002). Control of flowering time: Interacting pathways as a basis for diversity. Plant Cell 14 (suppl.), S111–S130.
Ng, M., and Yanofsky, M.F. (2001a). Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell 13, 739–753. Ng, M., and Yanofsky, M.F. (2001b). Function and evolution of the plant MADS-box gene family. Nat. Rev. Genet. 2, 186–195.[CrossRef][Web of Science][Medline]
Nilsson, O., Lee, I., Blazquez, M.A., and Weigel, D. (1998). Flowering-time genes modulate the response to LEAFY activity. Genetics 150, 403–410.
Noh, Y.S., and Amasino, R.M. (2003). PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell 15, 1671–1682.
Okamuro, J.K., Caster, B., Villarroel, R., Van Montagu, M., and Jofuku, K.D. (1997a). The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc. Natl. Acad. Sci. USA 94, 7076–7081.
Okamuro, J.K., den Boer, B.G., Lotys-Prass, C., Szeto, W., and Jofuku, K.D. (1996). Flowers into shoots: Photo and hormonal control of a meristem identity switch in Arabidopsis. Proc. Natl. Acad. Sci. USA 93, 13831–13836. Okamuro, J.K., Szeto, W., Lotys-Prass, C., and Jofuku, K.D. (1997b). Photo and hormonal control of meristem identity in the Arabidopsis flower mutants apetala2 and apetala1. Plant Cell 9, 37–47.[Abstract] Olsen, P.H., and Ambros, V. (1999). The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671–680.[CrossRef][Web of Science][Medline]
Onouchi, H., Igeno, M.I., Perilleaux, C., Graves, K., and Coupland, G. (2000). Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12, 885–900. Orlando, V. (2003). Polycomb, epigenomes, and control of cell identity. Cell 112, 599–606.[CrossRef][Web of Science][Medline] Parcy, F., Nilsson, O., Busch, M.A., and Weigel, D. (1998). A genetic framework for floral patterning. Nature 395, 561–566.[CrossRef][Medline]
Parenicova, L., de Folter, S., Kieffer, M., Horner, D.S., Favalli, C., Kater, M.M., Davies, B., Angenent, G.C., and Colombo, L. (2003). Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: New openings to the MADS world. Plant Cell 15, 1538–1551. Park, W., Li, J., Song, R., Messing, J., and Chen, X. (2002). CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12, 1484–1495.[CrossRef][Web of Science][Medline] Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E., and Yanofsky, M.F. (2000). B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405, 200–203.[CrossRef][Medline] Pelaz, S., Gustafson-Brown, C., Kohalmi, S.E., Crosby, W.L., and Yanofsky, M.F. (2001a). APETALA1 and SEPALLATA3 interact to promote flower development. Plant J. 26, 385–394.[CrossRef][Web of Science][Medline] Pelaz, S., Tapia-Lopez, R., Alvarez-Buylla, E.R., and Yanofsky, M.F. (2001b). Conversion of leaves into petals in Arabidopsis. Curr. Biol. 11, 182–184.[CrossRef][Web of Science][Medline]
Pineiro, M., Gomez-Mena, C., Schaffer, R., Martinez-Zapater, J.M., and Coupland, G. (2003). EARLY BOLTING IN SHORT DAYS is related to chromatin remodeling factors and regulates flowering in Arabidopsis by repressing FT. Plant Cell 15, 1552–1562. Pinyopich, A., Ditta, G.S., Savidge, B., Liljegren, S.J., Baumann, E., Wisman, E., and Yanofsky, M.F. (2003). Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424, 85–88.[CrossRef][Medline] Pnueli, L., Hareven, D., Broday, L., Hurwitz, C., and Lifschitz, E. (1994). The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6, 175–186.[Abstract] Putterill, J., Robson, F., Lee, K., Simon, R., and 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.[CrossRef][Web of Science][Medline] Quesada, V., Macknight, R., Dean, C., and Simpson, G.G. (2003). Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO J. 22, 3142–3152.[CrossRef][Web of Science][Medline] Ratcliffe, O., Bradley, D.J., and Coen, E.S. (1999). Separation of shoot and floral identity in Arabidopsis. Development 126, 1109–1120.[Abstract] Ratcliffe, O.J., Amaya, I., Vincent, C.A., Rothstein, S., Carpenter, R., Coen, E.S., and Bradley, D.J. (1998). A common mechanism controls the life cycle and architecture of plants. Development 125, 1609–1615.[Abstract] Ray, A., Lang, J.D., Golden, T., and Ray, S. (1996). SHORT INTEGUMENT (SIN1), a gene required for ovule development in Arabidopsis, also controls flowering time. Development 122, 2631–2638.[Abstract] Reeves, P.H., and Coupland, G. (2000). Response of plant development to environment: Control of flowering by daylength and temperature. Curr. Opin. Plant Biol. 3, 37–42.[CrossRef][Web of Science][Medline]
Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., and Bartel, D.P. (2002). MicroRNAs in plants. Genes Dev. 16, 1616–1626. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P. (2002). Prediction of plant microRNA targets. Cell 110, 513–520.[CrossRef][Web of Science][Medline]
Riechmann, J.L., Krizek, B.A., and Meyerowitz, E.M. (1996a). Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc. Natl. Acad. Sci. USA 93, 4793–4798. Riechmann, J.L., and Meyerowitz, E.M. (1997). MADS domain proteins in plant development. Biol. Chem. 378, 1079–1101.[Web of Science][Medline] Riechmann, J.L., and Meyerowitz, E.M. (1998). The AP2/EBEBP family of plant transcription factors. Biol. Chem. 379, 633–646.[Web of Science][Medline]
Riechmann, J.L., Wang, M., and Meyerowitz, E.M. (1996b). DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res. 24, 3134–3141. Rouse, D.T., Sheldon, C.C., Bagnall, D.J., Peacock, W.J., and Dennis, E.S. (2002). FLC, a repressor of flowering, is regulated by genes in different inductive pathways. Plant J. 29, 183–191.[CrossRef][Web of Science][Medline] Ruiz-Garcia, L., Madueno, F., Wilkinson, M., Haughn, G., Salinas, J., and Martinez-Zapater, J.M. (1997). Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell 9, 1921–1943.[Abstract] Samach, A., Klenz, J.E., Kohalmi, S.E., Risseeuw, E., Haughn, G.W., and Crosby, W.L. (1999). The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem. Plant J. 20, 433–445.[CrossRef][Web of Science][Medline]
Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F., and Coupland, G. (2000). Distinct roles of CONSTANS target genes in reproductive development in Arabidopsis. Science 288, 1613–1616.
Schultz, E.A., and Haughn, G.W. (1991). LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3, 771–781.
Shannon, S., and Meeks-Wagner, D.R. (1991). A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3, 877–892.
Sheldon, C.C., Conn, A.B., Dennis, E.S., and Peacock, W.J. (2002). Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14, 2527–2537. Sheldon, C.C., Finnegan, E.J., Rouse, D.T., Tadege, M., Bagnall, D.J., Helliwell, C.A., Peacock, W.J., and Dennis, E.S. (2000a). The control of flowering by vernalization. Curr. Opin. Plant Biol. 3, 418–422.[CrossRef][Web of Science][Medline]
Sheldon, C.C., Rouse, D.T., Finnegan, E.J., Peacock, W.J., and Dennis, E.S. (2000b). The molecular basis of vernalization: The central role of FLOWERING LOCUS C. Proc. Natl. Acad. Sci. USA 97, 3753–3758. Sieburth, L.E., and Meyerowitz, E.M. (1997). Molecular dissection of the AGAMOUS control region shows essential cis elements for spatial regulation are located intragenically. Plant Cell 9, 355–365.[Abstract] Sieburth, L.E., Running, M.P., and Meyerowitz, E.M. (1995). Genetic separation of third and fourth whorl functions of AGAMOUS. Plant Cell 7, 1249–1258.[Abstract] Simon, R., Carpenter, R., Doyle, S., and Coen, E. (1994). Fimbriata controls flower development by mediating between meristem and organ identity genes. Cell 78, 99–107.[CrossRef][Web of Science][Medline] Simon, R., Igeno, M.I., and Coupland, G. (1996). Activation of floral meristem identity genes in Arabidopsis. Nature 384, 59–62.[CrossRef][Medline]
Simpson, G.G., and Dean, C. (2002). Arabidopsis, the Rosetta stone of flowering time. Science 296, 285–289. Simpson, G.G., Dijkwel, P.P., Quesada, V., Henderson, I., and Dean, C. (2003). FY is an RNA 3' end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113, 777–787.[CrossRef][Web of Science][Medline] Theissen, G. (2001). Development of floral organ identity: Stories from the MADS house. Curr. Opin. Plant Biol. 4, 75–85.[CrossRef][Web of Science][Medline] Theissen, G., and Saedler, H. (2001). Floral quartets. Nature 409, 469–471.[CrossRef][Medline] Tilly, J., Allen, D.W., and Jack, T. (1998). The CArG boxes in the promoter of the Arabidopsis floral organ identity gene APETALA3 mediate diverse regulatory effects. Development 125, 1647–1657.[Abstract] Tröbner, W., Ramirez, L., Motte, P., Hue, I., Huijser, P., Lönnig, W.-E., Saedler, H., Sommer, H., and Schwarz-Sommer, Z. (1992). GLOBOSA: A homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J. 11, 4693–4704.[Web of Science][Medline]
Vandenbussche, M., Zethof, J., Souer, E., Koes, R., Tornielli, G.B., Pezzotti, M., Ferrario, S., Angenent, G.C., and Gerats, T. (2003). Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. Plant Cell 15, 2680–2693.
Wagner, D., Sablowski, R.W.M., and Meyerowitz, E.M. (1999). Transcriptional activation of APETALA1 by LEAFY. Science 285, 582–584.
Wang, X., Feng, S., Nakayama, N., Crosby, W.L., Irish, V., Deng, X.W., and Wei, N. (2003). The COP9 signalosome interacts with SCFUFO and participates in Arabidopsis flower development. Plant Cell 15, 1071–1082. Weigel, D., Alvarez, J., Smyth, D.R., Yanofsky, M.F., and Meyerowitz, E.M. (1992). LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843–859.[CrossRef][Web of Science][Medline]
Weigel, D., and Meyerowitz, E.M. (1993). Activation of floral homeotic genes in Arabidopsis. Science 261, 1723–1726. Weigel, D., and Meyerowitz, E.M. (1994). The ABCs of floral homeotic genes. Cell 78, 203–209.[CrossRef][Web of Science][Medline] Weigel, D., and Nilsson, O. (1995). A developmental switch sufficient for flower initiation in diverse plants. Nature 377, 495–500.[CrossRef][Medline]
Western, T.L., Cheng, Y., Liu, J., and Chen, X. (2002). HUA ENHANCER 2, a putative DExH-box RNA helicase, maintains homeotic B and C gene expression in Arabidopsis. Development 129, 1569–1581. Wilkinson, M.D., and Haughn, G.W. (1995). UNUSUAL FLORAL ORGANS controls meristem identity and organ primordia fate in Arabidopsis. Plant Cell 7, 1485–1499.[Abstract]
Wilson, R.N., Heckman, J.W., and Somerville, C. (1992). Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol. 100, 403–408. Yang, Y., Fanning, L., and Jack, T. (2003a). The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins APETALA3 and PISTILLATA. Plant J. 33, 47–59.[CrossRef][Web of Science][Medline] Yang, Y., Xiang, H., and Jack, T. (2003b). pistillata-5, an Arabidopsis B class mutant with strong defects in petal but not stamen development. Plant J. 33, 177–188.[CrossRef][Web of Science][Medline] Yanofsky, M.F. (1995). Floral meristems to floral organs: Genes controlling early events in Arabidopsis flower development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 167–188.[CrossRef][Web of Science] Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldmann, K.A., and Meyerowitz, E.M. (1990). The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346, 35–39.[CrossRef][Medline]
Yu, H., Xu, Y., Tan, E.L., and Kumar, P.P. (2002). AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc. Natl. Acad. Sci. USA 99, 16336–16341.
Zik, M., and Irish, V.F. (2003). Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15, 207–222. This article has been cited by other articles:
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | THE PLANT CELL | PLANT PHYSIOLOGY | |
|---|---|---|---|
TOP
INTRODUCTION
UNIFYING PRINCIPLES OF FLOWER...
miAP2). Control 35S:AP2wt flowers exhibit a wild-type phenotype; this is not surprising because AP2 RNA is expressed throughout the flower in wild-type plants (Jofuku et al., 1994
