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The beauty of flowers requires proper floral patterning, during which the temporal and spatial expression of floral homeotic genes are regulated to specify floral organs in floral meristems. Regulation of floral patterning early occurs in emerging floral primordia, which is prior to the emergence of floral organs and mediated by an ever-expanding list of regulators. We have recently reported the regulation of floral patterning by a new genetic pathway governed by three flowering time genes, SHORT VEGETATIVE PHASE (SVP), SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and AGAMOUS-LIKE 24 (AGL24). Here we show that another key flowering time gene, FLOWERING LOCUS T (FT), is also involved in regulating floral patterning. Our results suggest that flowering time genes are important regulators in the whole process of flower ontogeny from initial specification of incipient floral primordia to flower differentiation.
When plants initiate flowering, the vegetative shoot apical meristem (SAM) is transformed into an inflorescence meristem (IM) in response to environmental and endogenous flowering signals. The IM, in turn, generates a collection of undifferentiated cells called floral meristems (FMs) that give rise to various types of floral organs.
Several previous studies have revealed the involvement of flowering time genes in floral organ patterning, suggesting an intimate molecular link between two successive developmental events: flowering time control and early phases of flower development. AGAMOUS-LIKE 24 (AGL24) and SHORT VEGETATIVE PHASE (SVP) encoding MADS-box transcription factors are two flowering time genes acting downstream of several flowering pathways.1–3 When svp agl24 double mutant is cultured at 30°C, floral patterning is severely deregulated, resulting in floral homeotic transformation.4 Furthermore, another flowering time gene, SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) that is a floral pathway integrator controlled by several flowering genetic pathways, also functions in regulating floral patterning.5 These observations raise the possibility that some other flowering time genes, especially those functioning as floral pathway integrators, may also play additional roles in flower development.
Previously we found that the triple mutant soc1-2 agl24-1 svp-41 exhibited striking floral defects with loss of most floral organs and generation of various chimeric floral structures, which resulted from derepression of the class E gene SEPALLATA3 (SEP3) and precocious activation of class B and C genes in emerging FMs.5 To examine whether other two key flowering time genes, FLOWERING LOCUS T (FT) and FLOWERING LOCUS C (FLC), are also involved in flower development, we crossed soc1-2 agl24-1 svp-41 with ft-1 and flc-3, respectively. FLC was expressed extremely low in Col wild-type plants.6 As expected, there was no significant change in floral phenotypes when FLC was further mutated in soc1-2 agl24-1 svp-41 background (data not shown). On the contrary, we found the alleviation of floral defects in soc1-2 agl24-1 svp-41 ft-1 as compared with soc1-2 agl24-1 svp-41 (Fig. 1). The most significant phenotypic difference was the recovery of stamen formation in soc1-2 agl24-1 svp-41 ft-1. In soc1-2 agl24-1 svp-41 triple mutants, only the first few flowers produced immediately after bolting developed normal-looking stamens, whereas flowers generated later completely lacked stamens or produced deformed stamens that were unable to fertilize carpels (Fig. 1A and D).D). However, properly developed stamens could always been found from the flowers of soc1-2 agl24-1 svp-41 ft-1 quadruple mutants (Fig. 1B and D).D). To confirm the relevance of this rescued phenotype with FT activity, we cultured soc1-2 agl24-1 svp-41 under short-day conditions, where FT is considered as inactive.7 Similarly, growth of stamens was largely restored as revealed in soc1-2 agl24-1 svp-41 ft-1 under long-day conditions (Fig. 1C). These genetic data, which are consistent with a previous observation that the photoperiod regulates FM development,8 suggesting a role of FT in regulating flower development.
Because the number of all types of floral organs decreased in soc1-2 agl24-1 svp-41,5 we asked if such phenotype could be partially due to the reduction of floral stem cells. To test this hypothesis, we performed in situ hybridization to check the expression pattern of WUSCHEL (WUS), a well-known indicator of stem cell pool, during flower development of soc1-2 agl24-1 svp-41. In wild-type plant, WUS was expressed in the center of IMs underneath the two or three outmost cell layers, and later in emerging FMs with a similar pattern till stage 6 (Fig. 2A).9 WUS expression pattern was almost not altered in IMs or emerging FMs of soc1-2 agl24-1 svp-41 (Fig. 2A). However, in the triple mutants WUS expression disappeared in the flowers at stage 3 (Fig. 2B), where sepal primordia started to arise.10 This observation suggests a precocious suppression of WUS in FMs of the triple mutants, which may result in the depletion of stem cells and subsequently the reduction of floral organ number.
The expression of WUS is negatively regulated by CLAVATA genes.11 In addition, AG is required to terminate WUS transcription during flower development to prevent meristem indeterminacy.12,13 Based on the observation of indeterminate flowers on soc1-2 agl24-1 svp-41 ag-1,5 we assumed that suppression of WUS in flowers of soc1-2 agl24-1 svp-41 might be mainly due to the ectopic AG activity. Previously we have shown that SEPALLATA3 (SEP3) is a key factor involved in activating ectopic AG expression in soc1-2 agl24-1 svp-41.5 Furthermore, FT has been shown to promote SEP3 expression in leaves,14 which is mediated by FD that encodes a b-ZIP transcription factor physically interacting with FT.15 Thus, in soc1-2 agl24-1 svp-41 flowers, FT activity may contribute to AG ectopic expression through promoting SEP3 expression. This eventually affects the expression of WUS in floral meristems of soc1-2 agl24-1 svp-41, thus causing the depletion of floral stem cells and reduced number of floral organs.
FMs are exclusively produced by IMs, suggesting a unique capacity of IMs in specifying FMs. Since flowering time genes mediate the transformation of vegetative SAMs into IMs during the floral transition, we hypothesize that prior to and during the establishment of floral patterning, flowering time genes play much more important roles than expected in mediating the communications between IMs and FMs. Further studies on this aspect will shed more light on the function of flowering time genes in FM specification and subsequent flower development.
Preparation of this research article was supported by the Academic Research Fund T208B3113 from the Ministry of Education, Singapore and by the intramural research funds from Temasek Life Sciences Laboratory.
Previously published online: www.landesbioscience.com/journals/psb/article/9901