Complex regulation of flowering by high temperatures

Global warming is expected to threaten plant growth and crop production (Nicotra et al., 2010; C. Zhao et al., 2017), making it essential to understand how plants respond and adapt to high temperatures. Flowering is a critical developmental transition that needs to be properly timed based on environmental signals, such as temperature, to ensure plant reproductive success. In nature, plants that fail to adjust their flowering time in response to temperature have decreased in their abundance (Willis et al., 2008). Similarly, flowering time optimization in modern crops is crucial for yield and farming practice but is now challenged by rising temperatures (Muleke et al., 2022). Although studies with a wide range of British and Massachusetts (USA) plant species suggest that climate warming is generally associated with flowering acceleration (Fitter and Fitter, 2002; Miller-Rushing and Primack, 2008), some others investigating individual plant species and their accessions have found that temperature elevation may promote, delay or have only little effect on flowering (Table 1). In this issue of Plant, Cell & Environment, Abelenda et al. (Abelenda et al., 2023) investigate the impacts of high temperature on flowering in oilseed rape (Brassica napus L, AACC) and reveal diversified responses and regulatory mechanisms among different B. napus varieties, highlighting the complexity of flowering time control by high temperatures. B. napus is a leading oil crop that originated from the hybridization between Brassica rapa (AA) and Brassica oleracea (CC) (Lu et al., 2019). The authors started their investigation by taking several spring B. napus cultivars to measure their flowering time under optimal (21°C) and high (28°C) temperatures. Most of the tested varieties showed delayed flowering at high temperatures, except for Wesway, which flowered earlier at warmth. Their flowering behaviours seem also to be associated with their fitness changes at high temperatures, with Wesway becoming taller and others becoming shorter. This general delay of flowering by high temperatures in B. napus is similar to that observed in B. rapa (del Olmo et al., 2019), but different from their close relative Arabidopsis thaliana, in which most accessions flower earlier at high temperatures (Balasubramanian et al., 2006). Transcriptomic comparison of Wesway with Drakkar and Dux, two B. napus cultivars with strong and mild flowering delays induced by temperature elevation, respectively, revealed that Drakkar and Dux were always grouped together and separated from Wesway at 21°C and 28°C. However, identifying the key genes responsible for the different flowering responses to high temperature using the transcriptomic data proven to be difficult, as none of the known flowering time or temperature response genes showed differential expression consistent with the observed flowering behaviours. FLOWERING LOCUS T (FT) is an evolutionarily and functionally conserved floral integrator that promotes flowering (Putterill and Varkonyi-Gasic, 2016). Abelenda et al. (2023) reasoned that FT-like genes are normally expressed at low levels and with diurnal patterns, and their expression differences may not be well reflected in transcriptome analysis. Therefore, they focused on FT-like genes for detailed analyses and eventually identified BnaFTA2 as a main candidate accountable for differential flowering regulation by high temperatures in B. napus. In Drakkar, BnaFTA2 expression was repressed by temperature elevation, but this was not observed in Wesway, especially at the later stage of development when flowering is about to initiate. Histone variant H2A.Z is considered to play a repressive role at responsive genes (Coleman-Derr and Zilberman, 2012), and its deposition/eviction has been linked to temperature-mediated gene expression dynamics (Kumar and Wigge, 2010; Xue et al., 2021). In Arabidopsis and B. rapa, H2A.Z enrichment levels at the FT locus are reduced and increased, respectively, at high temperatures, consistent with the observed FT expression changes (Figure 1). These findings led the authors to examine H2A.Z accumulation at the BnaFTA2 locus under optimal and high temperatures. H2A.Z enrichment levels at BnaFTA2 were reduced by high temperatures in Wesway, in agreement with its flowering phenotypes. However, in accessions with delayed flowering at high temperatures, H2A.Z accumulation at the BnaFTA2 locus was not significantly altered by temperature elevation, despite a reduction in BnaFTA2 transcription (Figure 1). The lack of a clear connection between H2A.Z dynamics and flowering phenotypes was further verified using a mutant that is deficient in H2A.Z deposition, in which temperature elevation still triggered flowering delay and a reduction in BnaFTA2 expression levels. Collectively, these results suggest the presence of H2A.Z independent pathways in flowering time control by high temperatures. This work reminds us that we are still at the beginning of understanding the complex influences and regulatory mechanisms of temperature on flowering, and knowledge acquired from the model plant such as Arabidopsis may not be readily transferable to other species, even closely related ones. In addition, current studies of temperature effects on flowering often only consider temperature changes, while neglecting their interactions with other environmental cues such as photoperiod and biotic and abiotic stresses that together with temperature, are constantly changing in nature. A study in Brachypodium distachyon has shown that high temperature does not affect flowering under constant photoperiod conditions, but only when day-length shifting occurs (Boden et al., 2013), suggesting the intricate interaction and integration of temperature with other flowering signals. The reason for diversification in flowering responses to high temperatures is not clear, and it may be attributed to plant-specific growth habits, life cycles, and breeding backgrounds that eventually differentiate the regulatory mechanisms of flowering by high temperatures. Nevertheless, studies so far all suggest a central role of FT-like genes in integrating thermal signals, as works in Arabidopsis and several other plant species have demonstrated that changes in transcript levels of FT-like genes always correlate with flowering phenotypes induced by high temperatures (Abelenda et al., 2023; del Olmo et al., 2019; Kumar and Wigge, 2010; Nakano et al., 2013; Noy-Porat et al., 2013). These results highlight the importance of transcriptional regulation of FT-like genes in thermal-controlled flowering. In Arabidopsis, warmth affects FT transcription via two major mechanisms. Transcription factors SHORT VEGETATIVE PHASE (SVP) and FLOWERING LOCUS M (FLM) form a repressive complex at the FT locus, which becomes deactivated when temperature increases. Moreover, H2A.Z represses FT transcription and gets evicted from its locus at high temperatures (reviewed in Lippmann et al., 2019). Whether H2A.Z eviction is connected with the deactivation of the SVP-FLM complex is unknown, but at some other thermal-responsive loci, the removal of H2A.Z depends on a transcription factor PIF4 that recruits the INO80 chromatin remodelling complex. H2A.Z eviction per se is not sufficient for transcriptional activation, rather, it is linked with the deposition of another histone variant H3.3 and an active histone modification H3K4me3 (Xue et al., 2021; Zhao et al., 2023). These findings highlight the coordination of transcription factors with multiple epigenetic modifiers in modulating the transcription of temperature-responsive genes. In this sense, it is not surprising that different plants may utilize distinct transcription factors employing unique sets of epigenetic modifications to achieve proper FT regulation at high temperatures. Indeed, in their study, Abelenda et al. (2023) have found that the promoter of BnaFTA2 (where transcription factors normally bind) is responsible for its regulation by high temperatures, and the levels of chromatin accessibility and H3K4me3 at the BnaFTA2 locus positively correlate with its expression changes. Key basic knowledge breakthroughs in understanding thermal regulation of flowering will be made by identifying transcription factors that directly control thermal-mediated FT transcription in different plant species, followed by characterizing their regulatory mechanisms. For example, how do they regulate FT transcription, and how are they themselves regulated by high temperatures? In terms of application purposes, multiplexed CRISPR-Cas9 promoter editing of FT genes in crops may generate a series of alleles with diversified flowering responses to temperature and other environmental conditions, allowing the selection of crops ideal for future climate. Danhua Jiang was supported by the National Natural Science Foundation of China (32150610472). The authors declare no conflict of interest.