by Cristina Ferrándiz
Instituto de Biología Molecular y Celular de Plantas. CSIC-UPV.Valencia, Spain
In spite of what their sessile lifestyle could suggest, or maybe perhaps as a consequence of it, plants appear to be big decision-makers. Developmental decisions such as dormancy/germination, growth/arrest, branching/suppression-of-branches, vegetative-growth/flowering, senescence, fate … are key factors for their survival and reproductive success. Clearly, messengers are crucial to take action in a coordinated manner, and therefore the central role that plant hormones play in this coordination is no wonder. Among plant hormones, and among decisions too, a strong connection can be made between those that involve fate determination or life cycle transitions and gibberellins (GAs). The role of GAs in organ growth, cell differentiation and flowering promoting pathways has been well established and, somehow, GAs can be viewed as ‘coaches’ towards a grown-up stage.
Arabidopsis thaliana is an annual species that forms a vegetative rosette before entering into the reproductive phase. Flowering involves the bolting of the stem, which bears a small number of cauline leaves with axillary inflorescences, and above these the flowers grow. This particular type of growth, where in the bolting stem two different zones can be easily delimited, has led to two contrasting models to explain flowering transition, each of them based on different experimental evidence (Figure 1).
The acropetal model proposes that the shoot apical meristem undergoes two consecutive transitions: at bolting, the vegetative (V) meristem takes a first-phase-inflorescence identity (I1) and laterally produces leaves subtending flowering branches before undergoing a second phase change, where the I1 becomes an I2 meristem that directly produces flowers (Ratcliffe et al., 1998). Alternatively, the bidirectional model proposes that there is a single transition (V-to-I), after which the I meristem produces flowers acropetally while promoting internode elongation and branch development basipetally (Hempel and Feldman, 1994). No definitive proof has been found yet that fully supports one model over the other. One of the consequences is that many studies consider rosette leaf number as an indicator of flowering time, while many others quantify total leaf number (rosette+cauline).
The recent paper by Yamaguchi et al. (2014), which nicely advances our knowledge on GAs’ role in reproductive transition, might also shed light on this discussion. Or maybe not. The authors find that LEAFY (LFY), a floral meristem identity gene, directly up-regulates ELA1, a cytochrome P450 involved in GA4 catabolism. ELA1 up-regulation allows accumulation of gibberellin-sensitive DELLA proteins that, through their interaction with the flowering promoting factor SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9 (SPL9), activate the transcription of APETALA1 (AP1), another meristem identity gene that ultimately confers floral identity to the lateral primordia produced by the apical meristem. Therefore, it would appear that GAs act as floral repressors, since they have to be inactivated to produce flowers. However, it has been known for a long time that GAs are essential to promote flowering under short days in Arabidopsis and that they work in part by up-regulating LFY expression (Blázquez and Weigel, 2000). So there is an apparent contradiction here: GAs are important to switch on LFY, at least in some conditions, but after that, they have to be eliminated to allow flower formation. Accordingly, this paper shows how GA defective mutants or treatments that cause DELLA accumulation have more rosette leaves but less cauline leaves. This and other evidence in the paper can be easily integrated in the biphasic acropetal model of flowering: GAs contribute to the V-to-I1 transition and LFY up-regulation. Once this is established, LFY in turn directs GAs degradation and allows AP1 up-regulation and thus I1-I2 transition. In addition, and under this view, this work contributes another nice example of dual behaviour in floral business. So far, several transcription factors have been characterized to show this type of ‘mercurial’ temperament. For example, AP1 itself works promoting floral meristem identity and then, by changing interacting partners goes on to repress meristem identity and directs the differentiation of floral organs (Gregis et al., 2009)
While this dual biphasic behaviour seems to be a likely scenario, other interpretations could also be proposed that similarly fit the single-transition bidirectional model. It is possible that after GAs promote the reproductive transition, LFY action on GAs degradation could be local, restricted to acropetal lateral primordia, while basipetally GAs are not depleted from the stem and act on internode elongation. GA defective mutants would delay transition as a whole (explaining the increase observed in total leaf number described in Yamaguchi et al. paper) but then the basipetal signal to promote internode elongation would be weak and could explain the reduction on cauline leaf number of these mutants.
In any case, in addition to food-for-thought, this work provides new and interesting evidence and further confirms our impression: transition to adulthood is also a hormonal matter.
Blázquez M, Weigel D. 2000. Integration of floral inductive signals in Arabidopsis. Nature 404, 889-892.
Gregis V, Sessa A, Dorca-Fornell C, Kater MM. 2009. The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes. The Plant Journal 60, 626-637.
Hempel FD, Feldman LJ. 1994. Bi-directional inflorescence development in Arabidopsis thaliana: Acropetal initiation of flowers and basipetal initiation of paraclades. Planta 192, 276-286.
Ratcliffe O, Amaya I, Vincent C, Rothstein S, Carpenter R, Coen E, Bradley D. 1998. A common mechanism controls the life cycle and architecture of plants. Development 125, 1609-1615.
Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M, Wagner D. 2014. Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344, 638-641.