L. Conti

English

AIR Universita degli studi di Milano

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TITLE PAGE 
 
Spotlight review on:  
 
Hwang, K., Susila, H., Nasim, Z., Jung, J.-Y., and Ahn, J. H. (2019). Arabidopsis ABF3 
and ABF4 Transcription Factors Act with the NF-YC Complex to Regulate SOC1 
Expression and Mediate Drought-Accelerated Flowering. Mol. Plant Advance Access 
published 2019, doi:10.1016/j.molp.2019.01.002. 
 
 
Title: The A-B-A of the floral transition: the to do list for the perfect escape 
 
Running Title: Defining the regulatory events of drought escape 
 
Author: Lucio Conti 
 
Affiliation: Department of Biosciences, Università degli Studi di Milano, 
Via Celoria, 26, 20133 Milano, Italy 
 
Contact: Lucio.Conti@unimi.it 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
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The transition to flowering marks the initiation of reproductive competence in plants. 
After the floral transition the shoot apical meristem (SAM) ceases to produce leaf 
primordia and starts generating floral primordia, the reproductive organs of plants. To 
maximize reproductive success, the timing of this transition needs to be precisely 
aligned with the most favourable environmental conditions (Blackman, 2017). 
Daylength and cold temperature variations usually act as predictable seasonal signals 
to initiate flowering. However, due to the complexity of natural conditions, plants must 
gage a much wider array of information before committing to reproductive 
development. A striking example of this developmental plasticity is the drought escape 
(DE) response, where drought conditions experienced during vegetative growth cause 
an accelerated flowering time compared with optimal watering conditions (Fig 1A). 
Among the strategies to cope with drought stress, DE may provide ephemeral plants 
like Arabidopsis a simple “exit strategy” to anticipate seed set before drought 
conditions become incompatible with their survival.  
 
Two signalling cascades are required for DE; the photoperiodic pathway and the 
drought-related phytohormone abscisic acid (ABA) signalling (Riboni et al., 2013; 
Hwang et al., 2019). The photoperiodic pathway allows plants to flower according to 
particular day length and in Arabidopsis it is activated upon exposure to long day 
conditions, typical of spring/summer in temperate climates. Key photoperiodic 
signalling genes are GIGANTEA (GI) and CONSTANS (CO). Light-stabilized CO 
protein cascades into the activation of the florigen genes FLOWERING LOCUS T (FT) 
and TWIN SISTER OF FT (TSF) constituting a systemic flowering signal produced in 
the leaf vasculature and translocated in the SAM (Golembeski and Imaizumi, 2015). 
The florigen genes are necessary for DE activation and their transcript levels increase 
upon drought conditions through a poorly understood mechanism that involves the 
stimulation of GI function by ABA (Riboni et al., 2016). Major gaps thus exist in the 
definition of the molecular components that allow plants to integrate drought signals 
in the floral network. An exciting step towards this goal is described in a recent study, 
identifying the class of ABA-related bZIP transcription factors (TFs) ABRE-BINDING 
FACTORS (ABFs) as major drivers of DE (Hwang et al., 2019).   
 
 
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ABF3/4 integrate ABA signals into the floral network 
 
Great progresses have been made in the definition of the core ABA signalling 
components. ABA is perceived by the PYR/PYL/RCAR (PYRABACTIN 
RESISTANCE1/PYR1-LIKE/REGULATORY COMPONENTS OF ABA RECEPTORS) 
family of soluble receptors which, upon ABA binding, indirectly stimulate the activity of 
the SnRK2 (SNF1-related protein kinases 2) kinase family. The SnRK2s activate a 
complex network of posttranslational modifications that affect virtually all biological 
functions. The ABFs are key targets of the SnRK2s-mediated phosphorylation and 
regulate the ABA gene expression network (Yoshida et al., 2014; Song et al., 2016). 
Phenotypic analyses indicate that besides being impaired in ABA responses, mutant 
combinations of abf2, abf3, and abf4 are also late flowering (with ABF3 and 4 playing 
a major role) (Yoshida et al., 2014; Hwang et al., 2019). Conversely, the ectopic 
expression of ABF3 conferred an early flowering phenotype. ABF3/4 transcripts 
accumulation was consistent with their positive role in flowering, increasing during the 
vegetative phase and preceding that of known floral markers. The pattern of ABFs 
expression was in sharp contrast with that of other ABA-related TFs known to act as 
floral repressors. Thus, while ABA can have both positive and negative effects in 
flowering regulation, the evidence presented points to a predominantly positive role, 
mediated by the ABFs (Hwang et al., 2019). 
 
Defining SOC1 as target of ABF3/4  
 
A major observation of this study is that abf3/4 mutants are impaired in DE, supporting 
the key role of ABA signalling in this process. The authors further elaborate on the 
definition of the MADS box type TF SUPPRESSOR OF OVEREXPRESSION OF 
CONSTANS1 (SOC1) as bona fide floral target of ABF3/4. They compared datasets 
profiling the binding of 21 ABA-related transcription factors to chromatin and exploring 
the ABA-regulated gene networks to glean a short list of 12 targets. About half were 
identified as floral repressors and thus unlikely to activate DE. Among the other 
candidates, only SOC1 survived further experimental validations, as its transcript 
levels were significantly down-regulated in abf3/4 mutants as compared with the wild 
type under any watering conditions. Consistent with previous reports, soc1 mutants 
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were impaired in DE and could completely suppress the early flowering phenotype 
conferred by the overexpression of ABF3 (Hwang et al., 2019). These data led the 
authors to conclude that SOC1 hyper activation, triggered by ABA-stimulated ABF3/4, 
has a major contribution to DE.  
 
ABA activation of SOC1: NF-Y takes centre stage 
 
An intriguing observation of this study concerns the mode of activation of SOC1 by 
ABF3/4 (Hwang et al., 2019). At the SOC1 promoter the ABF3/4-bound DNA region 
did not display the usual ABA responsive cis-element, but rather a non-canonical 
NUCLEAR FACTOR-Y binding element (NF-Y BE). NF-Y is a hetero-trimeric complex 
consisting of NF-YB and NF-YC histone-fold domain subunits and one NF-YA subunit 
responsible for NF-Y sequence specificity of CCAAT-box elements. NF-Y acts as 
pioneer transcription factor, promoting chromatin accessibility and thus binding of 
other TFs (Gnesutta et al., 2018). In plants, genes encoding the different NF-Y 
subunits are remarkably expanded and functional redundancy exists. Since NF-Ys 
control ABA-responses as well as flowering time they are prime candidates to take 
part to the DE mechanism (Song et al., 2016). In support of this idea, NF-YC3/4 
subunits could physically interact with ABF3/4. Moreover, nf-yc3/4/9 mutants were 
impaired in the drought mediated SOC1 upregulation as well as DE, indicating that in 
the absence of NF-Y function, ABF3/4 activities alone were insufficient to trigger DE. 
CO directly contributes to SOC1 activation in combination with NF-Y (Hou et al., 2014). 
However, under drought conditions CO was completely dispensable for SOC1 
activation, indicating that while different protein complexes may assemble at the SOC1 
promoter, some are specifically engaged by ABA, yet still licensed by NF-Y binding 
(Fig 1B).  
 
Towards the definition of the DE regulatory events  
 
In short, this study identifies the ABFs/SOC1 module as key driver of DE, which begs 
the question of its connection with the florigen genes (Hwang et al., 2019). 
Histochemical analyses coupled with mis-expression studies indicate that the 
ABFs/SOC1 module operates in the leaf vasculature, where FT is activated, and not 
in the SAM. FT transcript levels were elevated in ABF3 overexpressing lines, but again 
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reduced when combined in the soc1 mutant background. Thus, the link between ABFs 
and FT is an indirect one, as neither ABFs nor SOC1 are enriched at the FT promoter. 
Several mechanisms may enable this cross-talk, as SOC1 directly represses a variety 
of well-known negative regulators of FT (Hwang et al., 2019). Thus, the ABFs/SOC1 
module may craft an accessible chromatin environment at the FT promoter for other 
activators to take over, among which GI, CO and the same NF-YB/C subunits that 
regulate SOC1, as CO (resembling the NF-YA subunit) promotes their assembly at 
specific cis-elements (Riboni et al., 2016; Gnesutta et al., 2018). These are still poorly 
understood layers of transcriptional regulations that contribute to bolster FT levels 
appropriate with the dry environment (Fig 1B).  
 
Our increasing knowledge of DE improves our understanding of plants survival 
strategies in nature, as the balance between the duration of the vegetative and 
reproductive phases is usually a major driver of fitness (Kenney et al., 2014). The 
connection of DE with ABA has also practical consequences, as improvements to rice 
yields under certain irrigation scenarios may be achieved by reducing ABA responses 
(Miao et al., 2018). This is associated with an increased duration of the vegetative 
phase, likely caused by reductions in florigen expression (Du et al., 2018). These 
studies will offer opportunities to identify targets for a more precise breeding strategy 
for plants under suboptimal conditions. 
 
 
Acknowledgments 
Research in the author’s lab is supported by the Cariplo Foundation through the 
FLORIMAIZE project (AF 1301-006/FC 2013-1889) jointly supported under the Ceres 
initiative of Fondazione Cariplo and Agropolis Fondation and the linea 2/2018 starting 
grant from the Università degli Studi di Milano.  
 
References 
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of Drought Escape through ABA-Dependent and -Independent Pathways in Rice. 
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Gnesutta, N., Mantovani, R., and Fornara, F. (2018). Plant Flowering: Imposing DNA 
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Hwang, K., Susila, H., Nasim, Z., Jung, J.-Y., and Ahn, J. H. (2019). Arabidopsis 
ABF3 and ABF4 Transcription Factors Act with the NF-YC Complex to Regulate 
SOC1 Expression and Mediate Drought-Accelerated Flowering. Mol. Plant 
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Figure Legend 
 
Figure 1. A hypothetical model for DE regulation in Arabidopsis. (A) Low soil moisture 
elicits DE under long days, causing an early entry in the reproductive phase. (B) 
Drought stress triggers ABA production and signalling, causing changes in gene 
expression through the ABFs. In the leaf, ABA-stimulated ABFs engage the NF-Y 
complex at the NF-Y binding element (NF-Y BE) region to trigger SOC1 transcriptional 
activation. The SOC1 gene product acts as transcriptional repressor of several 
negative regulators of FT, thus facilitating its transcriptional activation (dotted arrow) 
by the CO-NF-Y complex which assembles at the CO-responsive element (CORE). 
ABA stimulates GI in an unknown manner which might relocate at the FT promoter in 
association with the CO-coordinated NF-Y complex. 


The A-B-A of the floral transition: the to do list for the perfect escape

https://air.unimi.it/retrieve/handle/2434/628134/1177402/Final%20version_Conti.pdf

The A-B-A of the floral transition: the to do list for the perfect escape

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