JXB Advance Access originally published online on February 10, 2007
Journal of Experimental Botany 2007 58(5):899-907; doi:10.1093/jxb/erm002
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Flowering Newsletter Reviews |
Flowering and determinacy in Arabidopsis
Cell and Developmental Biology, John Innes Centre, Norwich NR4 7UH, UK
* E-mail: Robert.sablowski{at}bbsrc.ac.uk
Received 1 November 2006; Revised 11 December 2006 Accepted 5 January 2007
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Abstract |
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 Top Abstract IntroductionMaintenance of indeterminate...From vegetative to floral...Genetically programmed...Relevance to other speciesReferences |
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Meristems provide new cells to produce organs throughout the life of a plant, and their continuous activity depends on regulatory genes that balance the proliferation of meristem cells with their recruitment to organogenesis. During flower development, this balance is shifted towards organogenesis, causing the meristem to terminate after producing a genetically determined number of organs. In Arabidopsis, WUSCHEL (WUS) specifies the self-renewing cells at the core of the shoot meristems and is a key target in the control of meristem stability. The development of a determinate floral meristem is initiated by APETALA1/CAULIFLOWER (AP1/CAL) and LEAFY (LFY). The latter activates AGAMOUS (AG), partly in co-operation with WUS. AG then directs the development of the innermost floral organs and at the same time antagonizes WUS to terminate the meristem, although the mechanism of WUS repression remains unknown. All these genes participate in a series of regulatory feedback loops that maintain stable expression patterns or promote sharp developmental transitions. Although the regulators of meristem maintenance and determinacy in Arabidopsis are widely conserved, their interactions may vary in other species.
Key words: AGAMOUS, determinacy, flower development, shoot meristem, WUSCHEL
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Introduction |
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TopAbstractIntroductionMaintenance of indeterminate...From vegetative to floral...Genetically programmed...Relevance to other speciesReferences |
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The apical meristems function as the main sources of new cells to sustain plant growth. The regular recruitment of meristem cells to form new organs and tissues is balanced by cell proliferation within the meristem to maintain its size relatively stable. This steady-state can persist throughout the life of the plant, but in many cases the meristem is genetically programmed to stop producing new cells at a specific developmental stage. In these cases, the meristem is said to be determinate. A determinate meristem produces a part of the plant body with a predictable size and form, such as the flower, whereas indeterminate meristems produce parts of the plant whose size and shape depend on the local environment, such as branches and roots that grow to variable lengths. The positioning of determinate and indeterminate meristems varies between species and is a major determinant of plant architecture.
Here, the genetic control of meristem determinacy in Arabidopsis and the applicability of this knowledge to other species is reviewed. In the Arabidopsis shoot, determinacy is a property of the floral meristems, whereas the vegetative and inflorescence meristems are indeterminate. The indeterminate growth of the vegetative and inflorescence meristems requires a specific set of regulatory genes, whose activity is antagonized by flower-specific regulators. For this reason, it is useful to start with a description of how the activity of indeterminate meristems is maintained.
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Maintenance of indeterminate meristems |
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TopAbstractIntroductionMaintenance of indeterminate...From vegetative to floral...Genetically programmed...Relevance to other speciesReferences |
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The indeterminate growth of the vegetative and inflorescence meristems is sustained by small groups of self-renewing cells that are functionally similar to stem cells in animals (Sablowski, 2004). These cells are located in the central zone (CZ) of the meristem, while some of their descendants are displaced to the peripheral zone (PZ), where they are recruited to form new organ primordia (Fig. 1). Below the CZ, the rib meristem (RM) sustains stem growth. The CZ and PZ functions have been well studied in Arabidopsis, although the RM has received much less attention. Superimposed on the CZ/PZ organization, the typical tunica/corpus structure found in angiosperms can also be distinguished, with two external layers (L1 and L2) in which most cell divisions are oriented tangentially to the meristem surface, while the inner layer does not have clearly oriented divisions (Carles and Fletcher, 2003). Although the functional significance of the L1–L3 layering is not well understood, the existence of these clonally distinct layers has been essential to reveal the role of intercellular communication in meristem function.
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SHOOT MERISTEMLESS (STM) and WUSCHEL (WUS) are two regulatory genes with central roles in shoot meristem development. STM and WUS genes function synergistically during meristem development and are required not only for the establishment of the shoot meristem during embryogenesis, but also for subsequent maintenance of the vegetative, inflorescence and floral meristems (Clark et al., 1996; Laux et al., 1996; Long et al., 1996; Gallois et al., 2002; Lenhard et al., 2002). STM encodes a homeodomain protein expressed throughout the meristem (Long et al., 1996) and has been proposed to delay differentiation to allow enough cells to bulk up before recruitment into organogenesis (Lenhard et al., 2002).
WUS also encodes a homeodomain-containing protein and is essential to specify the stem cells present in the CZ: in wus mutants, the defective CZ cannot keep up with organ recruitment in the PZ, and the meristem is quickly consumed (Mayer et al., 1998). Shoot meristem activity is eventually reinitiated in the axils of the leaves, only to terminate again; this intermittent meristem activity can carry on to the reproductive phase, when incomplete flowers are produced because of premature termination of the floral meristem (Fig. 3). Not only is WUS necessary to maintain the CZ cells, but ectopic expression of WUS is also sufficient to convert cells in organ primordia and even root meristems into cells with characteristics of the shoot meristem CZ (Schoof et al., 2000; Gallois et al., 2004). Although WUS is required to maintain stem cells in all layers of the CZ, it is expressed only in a few L3 cells in the centre of the meristem (Mayer et al., 1998) (Fig. 1). Because its effects are seen in cells that do not express WUS, an intercellular signal is believed to mediate these effects. The size and location of the WUS-expressing region of the meristem are maintained in spite of the continuous cell proliferation within the meristem, implying that WUS expression must be adjusted constantly according to the position of cells in the meristem.
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Although both STM and WUS are essential for meristem maintenance, the evidence so far suggests that WUS has a more prominent role in the developmental control of meristem size and stability. One of the mechanisms that fine-tune WUS expression is the CLAVATA (CLV) signalling pathway, which represses WUS (reviewed by Carles and Fletcher, 2003). The signal in this case is the secreted polypeptide CLV3, whose biologically active form has recently been shown to be a dodecapeptide corresponding to the C-terminal region of the CLV3 product (Ito et al., 2006). CLV3 is produced in the L1 and L2 layers of the CZ and moves into the inner layers, where it is perceived by a receptor containing the CLV1 and CLV2 polypeptides. Mutations in any of the clv genes have a similar effect: WUS expression increases and the CZ gradually enlarges. WUS activates expression of CLV3 in the overlying region of the meristem and therefore limits its own expression, so it is believed that meristem size is stabilized by the WUS/CLV regulatory loop (Fletcher et al., 1999; Brand et al., 2000). Consistent with this idea, increases in CLV3 rapidly repress WUS expression and shut down meristem activity (Reddy and Meyerowitz, 2005), but, surprisingly, it has been found that the meristem eventually adjusts to changes in CLV3 expression and that plants can grow normally with CLV3 levels ranging from 3-fold lower to 3-fold higher than the wild type (Muller et al., 2006). The implication is that additional mechanisms, independent of the CLV loop, stabilize WUS expression and meristem size. It has also been revealed that CLV3 itself has multiple functions, including the control of cell division rates in the meristem and repression of CZ identity in neighbouring PZ cells (Reddy and Meyerowitz, 2005).
A number of additional regulatory genes control the position and number of cells expressing WUS and therefore also have a role in controlling meristem stability. One of them is ULTRAPETALA (ULT) (Carles et al., 2004), which antagonizes WUS; accordingly, ult mutants have enlarged inflorescence meristems and supernumerary floral organs. The HD-ZIPIII genes CORONA (CNA), PHABULOSA (PHAB), and PHAVOLUTA (PHAV) (the latter two better known for their role in controlling organ polarity) also restrict the size of the WUS-expressing domain and meristem size (Prigge et al., 2005; Williams et al., 2005). Chromatin remodelling factors participate in preventing WUS expression outside its normal domain (Kaya et al., 2001; Bertrand et al., 2003; Takeda et al., 2004) and in directly activating it in its normal region (Kwon et al., 2005). Another known positive regulator of WUS is STIMPY (STIP), which encodes a protein of the same family as WUS and is required to maintain WUS expression in the meristem; STIP, however, has a more general role in maintaining cell divisions in the meristem, a role that can be bypassed by exogenously added sucrose (Wu et al., 2005). To integrate all these inputs, WUS could be expected to have complex cis-regulatory sequences. Surprisingly, however, much of the WUS expression pattern can be directed by a short (57 bp) sequence, suggesting that the integration of multiple inputs converges at a relatively simple regulatory element in the WUS gene (Baurle and Laux, 2005).
From the work reviewed above, WUS emerges as a central regulator of shoot meristem identity and stability. To balance the recruitment of cells away from the meristem with the supply of new meristem cells, a constant and precise pattern of WUS expression must be maintained within a population of cells that proliferates continuously. This is achieved by multiple regulatory inputs, many of which act to repress WUS outside its normal expression domain.
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From vegetative to floral meristems |
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TopAbstractIntroductionMaintenance of indeterminate...From vegetative to floral...Genetically programmed...Relevance to other speciesReferences |
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The dynamic balance between shoot meristem activity and organ initiation is maintained during most of the plant's growth, but it is eventually tipped in favour of organogenesis during floral development. The suppression of indeterminate growth in the floral meristem depends on floral-specific regulatory genes, whose expression is embedded within a programme of gene expression that is initiated at the transition to reproductive development. During this transition, the vegetative meristem is initially converted into the inflorescence meristem, which then produces floral meristems on its flanks. The transition from vegetative to reproductive development is controlled by multiple environmental and endogenous signals that ultimately converge on key regulators of floral identity: APETALA1 (AP1)/CAULIFLOWER (CAL) and LEAFY (LFY) (reviewed by Komeda, 2004; Blazquez et al., 2006) (Fig. 2).
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AP1 and CAL encode closely related MADS-domain transcription factors that are necessary and sufficient for the transition from inflorescence to floral meristem. In the double mutant ap1-1 cal-1, the primordia produced on the flanks of the inflorescence meristem fail to develop as flowers, and instead function as new inflorescence meristems, which go on to produce their own primordia, repeating the process until a large mass of meristems accumulates at the inflorescence apex, which resembles a cauliflower curd (Bowman et al., 1993). Conversely, overexpression of AP1 is sufficient to convert the inflorescence meristem into a terminal flower (Mandel and Yanofsky, 1995). Consistent with their role in specifying floral meristems, AP1 and CAL are expressed as soon as the floral primordium emerges from the inflorescence meristem (Kempin et al., 1995).
LFY also encodes a transcriptional regulator that specifies floral identity and consequently promotes determinacy (Weigel et al., 1992). This has been shown both by loss of lfy function, which converts floral meristems to inflorescence shoots (Schultz and Haughn, 1991), and by the effect of ectopic LFY expression, which converts the inflorescence meristem into a terminal floral meristem (Weigel and Nilsson, 1995). LFY promotes the transition from inflorescence to floral meristem largely by activating AP1 (Mandel and Yanofsky, 1995; Wagner et al., 1999), but subsequently has a central and AP1-independent role in controlling floral development.
In addition to being activated by LFY, AP1/CAL are redundantly activated by the FT gene (Ruiz-Garcia et al., 1997) (Fig. 2). Recent evidence suggests that FT is expressed in leaves and that its RNA or protein is transported to the apex as part of a mobile flowering signal that is produced in response to long days (Abe et al., 2005; Huang et al., 2005). After reaching the apex, FT is believed to interact with the bZIP protein FD to activate AP1/CAL (Abe et al., 2005; Wigge et al., 2005). LFY itself is also activated by FT (Huang et al., 2005), besides being activated by gibberellin, which also functions as a signal to promote the shift to reproductive development (Blazquez et al., 1998).
As mentioned above, to maintain the indeterminate inflorescence meristem, AP1/CAL and LFY must be activated only in the floral primordia. The expression of LFY and AP1/CAL in the inflorescence meristem is prevented by TERMINAL FLOWER (TFL), which encodes a homologue of FT but has the opposite function, i.e. it antagonizes floral development (Bradley et al., 1997; Kardailsky et al., 1999; Kobayashi et al., 1999) (Fig. 2). In the tfl mutant, ectopic expression of LFY and AP1 transforms the whole inflorescence meristem into a floral meristem. TFL is expressed just below the inflorescence meristem, indicating that it functions non-cell-autonomously to prevent LFY and AP1 expression and the consequent termination of the inflorescence meristem.
The interactions between FT, AP1/CAL, LFY, and TFL not only delimit where floral meristems develop, but also establish regulatory loops that ensure a sharp and stable transition to floral identity. After the initial activation by FT/FD, LFY and AP1/CAL reinforce each other's expression: LFY activates AP1 directly (Wagner et al., 1999) and AP1 helps to maintain LFY expression in part by antagonizing TFL (Liljegren et al., 1999). Together, LFY and AP1/CAL then activate the floral development programme.
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Genetically programmed termination of the floral meristem |
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TopAbstractIntroductionMaintenance of indeterminate...From vegetative to floral...Genetically programmed...Relevance to other speciesReferences |
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As described above, AP1 and LFY promote floral meristem identity and consequently determinacy. Termination of the meristem, however, is not a direct effect of these regulatory genes, but part of the flower development programme set in motion by AP1 and LFY.
After being initiated on the flanks of the inflorescence meristem, the floral meristem produces four whorls of organs, which in wild-type Arabidopsis typically contain four sepals, four petals, six stamens, and two fused carpels (Fig. 3). The identity of each type of organ is specified by a specific combination of MADS-domain proteins that are believed to form multiprotein complexes, each complex able to control the set of target genes required for the development of a particular organ type (reviewed by Krizek and Fletcher, 2005). One of these MADS-domain proteins is AP1 which, after its earlier role in specifying floral identity, participates in the development of the perianth organs (sepals and petals). LFY also remains active after floral initiation and activates genes encoding MADS-domain proteins required for stamen and carpel development: APETALA3 (AP3), PISTILLATA (PI), and AGAMOUS (AG) (Fig. 2). Among these, AG is especially relevant here because it has the additional role of controlling meristem determinacy. In strong ag mutants such as ag-1 or ag-3 (Fig. 3), stamens are replaced by petals (reflecting the organ identity function) and carpels are replaced by a reiteration of the sequence sepals–petals–petals, produced by an active meristem at the centre of the flower (revealing both the organ identity and the determinacy functions of AG).
To terminate the meristem, AG would be expected to antagonize the function of meristem maintenance genes such as STM or WUS. Given the prominent role of WUS in the control of meristem size and stability, an attractive idea would be that AG adds a further negative input to shut down WUS and terminate the floral meristem. Several lines of evidence have confirmed that this is the case. WUS is initially expressed in the floral meristem, but its expression decreases at the stage when AG is activated and disappears by the time carpel primordia are initiated (Mayer et al., 1998). In contrast, WUS remains active in the centre of the indeterminate floral meristem of the ag-1 mutant (Lenhard et al., 2001; Lohmann et al., 2001). As mentioned before, WUS is required for the maintenance of all shoot meristems, including the floral meristem; the premature termination of the floral meristem in the wus-1 mutant (Fig. 3) is opposite to the extended meristem activity in ag mutants. WUS is essential for the indeterminacy seen in ag flowers, because the flowers of the double mutant wus-1 ag-1 look indistinguishable from those of wus-1 (Laux et al., 1996). Conversely, forcing an increase in WUS expression in the floral meristem (using LFY, AG, or AP3 promoters to express WUS) promotes indeterminacy in spite of AG activity (Lenhard et al., 2001).
The experiments described above also revealed that WUS activated AG: ectopic WUS not only prolonged meristem activity, but also led to ectopic stamen and carpel development in an AG-dependent way (Lenhard et al., 2001; Lohmann et al., 2001). Supporting the suggestion that it can activate AG, the WUS protein bound in vitro to regulatory sequences present in AG and activated transcription of a reporter containing these sequences in yeast cells (Lohmann et al., 2001). In the yeast experiments, however, transcription was only activated when WUS and LFY were combined, and not by either protein alone. The activation of AG by WUS and LFY combined would explain why AG is activated by WUS only during floral development. It must be noted, however, that WUS must be a redundant activator of AG, which still functions in wus mutant flowers to direct the development of stamens (Fig. 3). Moreover, the AG expression domain is wider than that of WUS, so direct activation by WUS can only occur in a subset of the AG-expressing cells (so far, there is no evidence that the WUS protein moves between cells). Nevertheless, the overall conclusion is that AG functions in a negative feedback loop that terminates WUS expression and meristem activity in the floral bud.
While the activation of AG by WUS (at least in part of the floral meristem) appears to result from direct binding of WUS to the AG gene, the repression of WUS by AG is unlikely to be direct. Experiments using mosaic expression of AG have shown that determinacy is lost when AG expression is absent from the L2 layer of the floral meristem (Sieburth et al., 1998), where WUS is not expressed (Mayer et al., 1998). This implies that AG must function across cell boundaries to antagonize WUS, and that coincident expression of AG and WUS in the L3 layer is not sufficient to terminate the flower. Another reason why the repression of WUS by AG is probably indirect is that there is a delay between the activation of AG in the floral bud (stages 2–3) and down-regulation of WUS (stage 6, which occurs 
12 h later; Smyth et al., 1990). Such a delay would be unexpected if AG functioned in a simple transcriptional cascade to down-regulate WUS.
What could be the signal that mediates the repression of WUS by AG? Non-cell-autonomous repression of WUS brings to mind the CLV pathway, so AG might stimulate the negative feedback loop involving CLV3. However, clv mutants have a much milder effect on floral determinacy than ag mutations; in other words, AG is still largely able to terminate the meristem in the absence of CLV function. In addition, the ag-2 clv1-1 double mutant has a stronger increase in floral meristem activity than ag-2 or clv1-1 alone (Clark et al., 1993), indicating that CLV and AG functions converge to limit meristem activity. Therefore, the CLV pathway appears unlikely to play a major role in mediating the determinacy effect of AG.
Other genes are known to promote floral determinacy, but are also unlikely to mediate AG functions. One of them is SUPERMAN (SUP), which limits stamen number and is believed to function non-cell-autonomously to control cell proliferation in the centre of the floral meristem (Schultz et al., 1991; Bowman et al., 1992; Sakai et al., 1995). WUS is required for the decreased determinacy seen in the sup mutant, because the meristem termination in wus-1 flowers is epistatic over the increase in organ number seen in the sup-6 mutant (Laux et al., 1996). The interaction between sup-1 and ag-1 mutations, however, is synergistic, indicating that they control meristem activity through parallel pathways (Bowman et al., 1992). The ULT gene, which as described above antagonizes WUS, also limits the number of floral organs. In this case, strong ag mutations are epistatic over ult (Carles et al., 2004), suggesting that the role of ULT in floral determinacy is contained within the functions activated by AG. However, as in the case of clv mutants, the loss of determinacy in ult mutants is much weaker than in ag mutants, showing that ult is largely dispensable for the determinacy function of AG.
One way to reveal the downstream effectors that mediate the determinacy role of AG is to use expression arrays to screen for genes regulated by AG. Gomez-Mena et al. (2005) used inducible AG in an ap1-1 cal mutant background to screen for AG targets during the early stages of stamen and carpel development. Among the genes activated by AG in this study was GA4, whose product catalyses the final step in the biosynthesis of bioactive gibberellin, suggesting that one of the early functions of AG is to activate gibberellin biosynthesis. Because gibberellin is believed to antagonize meristem activity (reviewed by Shani et al., 2006), a localized increase in gibberellin levels might mediate the meristem-antagonizing function of AG. To test this idea, it would be necessary to see whether floral meristems become indeterminate in the absence of gibberellin, but this has not been possible so far because even severe gibberellin-deficient mutants such as ga1-3 are believed still to produce low levels of gibberellin (Hedden and Phillips, 2000).
Activation of GA4 in the early stages of floral development was confirmed by Wellmer et al. (2006), who used inducible AP1 in the ap1-1 cal-1 background to produce a time-course of changes in gene expression during early floral development. This study, however, also showed activation of genes that encode GA2-oxidases, which inactivate gibberellin. In the vegetative meristem, GA2-oxidases are expressed at the base of the meristem and organ primordia, and have been proposed to prevent diffusion of gibberellin from developing organs into the meristem (Jasinski et al., 2005). Thus it is possible that GA2-oxidases are required to protect the floral meristem from gibberellin produced by the organ primordia before meristem termination is due. The exact location and timing of GA4 and GA2-oxidase expression during early flower development, however, remain unknown.
Gibberellin appears unlikely to be the only phytohormone whose levels are relevant to meristem termination. It has been proposed that meristem activity requires at the same time low gibberellin levels and cytokinin biosynthesis, both of which are promoted by STM (Jasinski et al., 2005; Yanai et al., 2005). The positive role of cytokinin in meristem maintenance is also consistent with the finding that one of the functions of WUS is to repress genes that antagonize cytokinin responses (Leibfried et al., 2005). Therefore, it might be expected that termination of the floral meristem would be associated not only with an increase in gibberellin activity, but also with a decrease in the levels or sensitivity to cytokinin. So far, however, no connection has been noted between AG and genes involved in cytokinin production or responses.
In summary, during floral development, the repressive input that restricts the location and level of WUS expression is increased by genes such as AG and SUP to promote meristem determinacy. Precisely how these regulators antagonize WUS is still unknown, although phytohormones are plausible candidates to mediate the non-cell-autonomous effect of AG on meristem termination.
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Relevance to other species |
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TopAbstractIntroductionMaintenance of indeterminate...From vegetative to floral...Genetically programmed...Relevance to other speciesReferences |
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Of the regulators of meristem maintenance and determinacy described above, AG has been the most intensively studied from the evolutionary point of view (Theissen et al., 2000; Irish, 2003). One of the interesting twists of AG function in other species is that the organ identity and determinacy functions are not always carried out by a single gene: in maize, these functions are performed by different AG paralogues (Mena et al., 1996). The organ identity and determinacy functions of AG are also separable in Arabidopsis: loss of determinacy, but not of organ identity, occurs in plants with partial loss of AG function caused by antisense RNA or by a weak allele (ag-4, which produces a mutant AG protein with an internal deletion) (Mizukami and Ma, 1995; Sieburth et al., 1995). The fact that the two functions of AG are genetically separable suggests that the organ identity function does not overlap significantly with the meristem termination function. This in turn is compatible with the idea that these functions of AG were acquired at different times during evolution (and were subsequently separated again in maize), although it is not clear what the ancestral function was. The association between AG homologues and reproductive shoot development in gymnosperms has been used to suggest that the role of AG in reproductive organ identity is ancient, but at the same time it has been noted that these reproductive shoots are determinate (Irish, 2003).
The large increase in the number of perianth organs seen in ag mutants is reminiscent of double flowers, such as roses and carnations, that have been selected in many species by horticulturalists. The resemblance raises the question of whether similar genes are involved, and in some examples this appears to be the case. In Japanese morning glory, a double mutant flower phenotype first described in the 18th century is caused by mutation of an AG homologue (Nitasaka, 2003). In rose, two AG homologues have been identified, one of which has the same type of internal deletion as the ag-4 allele, which as described above causes loss of determinacy (Kitahara and Matsumoto, 2000). Whether this allele has played a role in the selection of modern double roses, however, remains to be seen. It must be noted that the much increased number of petals and stamens and eventual termination of the floral meristem in roses could also be caused by a localized enlargement of the floral meristem, as seen in the sup or ult mutants.
Other key players in meristem identity and determinacy, such as WUS, LFY, and TFL, are also clearly conserved and carry out comparable functions in other species (Stuurman et al., 2002; Schwarz-Sommer et al., 2003; Angenent et al., 2005; Kieffer et al., 2006). Some of the regulatory connections between these genes, however, are variable. In tomato, for example, the TFL orthologue SELF-PRUNING maintains indeterminacy in the inflorescence meristem, but does not do so by antagonizing expression of the LFY orthologue, FALSIFLORA (Pnueli et al., 1998; Molinero-Rosales et al., 1999). The floral-specific repression of WUS may also differ in plants in which the central region of the floral meristem gives rise to the placenta instead of carpel primordia. This is the case in Impatiens, where AG does not appear to be sufficient to terminate the floral meristem (Ordidge et al., 2005; Chiurugwi, 2007). Similarly, it has been noted in petunia that repression of WUS does not coincide with the activation of AG orthologues, but occurs later, when other MADS proteins are expressed in the centre of the flower to specify ovule identity. When expressed during the vegetative phase, these ovule identity genes terminate the meristem, suggesting that they could mediate WUS repression (Ferrario et al., 2006).
Other aspects of meristem determinacy are even more clearly divergent, particularly when determinacy is controlled during developmental steps that have no obvious equivalent in Arabidopsis. In maize, the inflorescence meristem does not give rise to floral meristems directly, but instead gives rise to two intermediate types of meristems, the spikelet pair and the spikelet meristem (see review by Bortiri and Hake, 2007). The regulatory genes ramosa1 (Vollbrecht et al., 2005), ramosa2 (Bortiri et al., 2006), and branched silkless1 (Chuck et al., 2002) control the determinacy of the spikelet pair and spikelet meristems, and do not appear to have counterparts that control meristem determinacy in dicotyledonous plants.
Another way in which the control of determinacy differs across plants is in its reversibility. In an annual plant such as Arabidopsis, it is clear why commitment to flowering and floral development should be irreversible and followed by death of the plant. In perennial plants, reversion to vegetative growth after the flowering season occurs from meristems that have not been converted to reproductive development (i.e. there is no reversion), but in some cases true reversion occurs, exemplified by plants showing pseudovivipary and by Impatiens shifted to long days after flowering (reviewed by Tooke et al., 2005). Stable developmental transitions are often caused by autoregulatory loops that translate a transient stimulus into a stable regulatory change (Davidson et al., 2002). In Arabidopsis, such autoregulatory loops occur in multiple stages in the control of flowering and determinacy, including autoactivation by FT (Huang et al., 2005), the reciprocal activation of LFY and AP1/CAL mentioned above, and positive autoregulation of AG (Gomez-Mena et al., 2005). In Impatiens, reversion to vegetative development in long days correlates with the interrupted production of a leaf-derived flowering signal (Tooke et al., 2005) and could be due to a failure to establish autoregulatory loops, such as the FT autoactivation loop.
In conclusion, to understand evolutionary variation in meristem determinacy and in plant development in general, a future challenge will be to reveal not only the conserved and divergent regulators of meristem activity, but also how diversity is created by changes in the regulatory connections between those genes.
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Acknowledgements |
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Work in my laboratory is funded by the Biotechnology and Biological Sciences Research Council and by the European Union.
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References |
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TopAbstractIntroductionMaintenance of indeterminate...From vegetative to floral...Genetically programmed...Relevance to other speciesReferences |
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