Brassinosteroids Dominate Hormonal Regulation of Plant Thermomorphogenesis via BZR1

Abstract

Thermomorphogenesis is defined as the suite of morphological changes that together are likely to contribute to adaptive growth acclimation to usually elevated ambient temperature [1, 2]. While many details of warmth-induced signal transduction are still elusive, parallels to light signaling recently became obvious (reviewed in [3]). It involves photoreceptors that can also sense changes in ambient temperature [3-5] and act, for example, by repressing protein activity of the central integrator of temperature information PHYTOCHROME-INTERACTING FACTOR 4 (PIF4 [6]). In addition, PIF4 transcript accumulation is tightly controlled by the evening complex member EARLY FLOWERING 3 [7, 8]. According to the current understanding, PIF4 activates growth-promoting genes directly but also via inducing auxin biosynthesis and signaling, resulting in cell elongation. Based on a mutagenesis screen in the model plant Arabidopsis thaliana for mutants with defects in temperature-induced hypocotyl elongation, we show here that both PIF4 and auxin function depend on brassinosteroids. Genetic and pharmacological analyses place brassinosteroids downstream of PIF4 and auxin. We found that brassinosteroids act via the transcription factor BRASSINAZOLE RESISTANT 1 (BZR1), which accumulates in the nucleus at high temperature, where it induces expression of growth-promoting genes. Furthermore, we show that at elevated temperature BZR1 binds to the promoter of PIF4, inducing its expression. These findings suggest that BZR1 functions in an amplifying feedforward loop involved in PIF4 activation. Although numerous negative regulators of PIF4 have been described, we identify BZR1 here as a true temperature-dependent positive regulator of PIF4, acting as a major growth coordinator.

PIF 4‐induced BR synthesis is critical to diurnal and thermomorphogenic growth

“…We showed that warm temperatures cause up-regulated expression of BR biosynthetic genes, and that this response is compromised in the pifq mutant, which fails to show temperature-mediated hypocotyl elongation at 28°C (Fig 5 and Appendix Fig S6). In agreement with a prevalent role of this regulation in temperature-induced hypocotyl growth, mutations affecting the DWF7 and ROT3 genes were recently identified in a screen for okapi mutants that reversed the hypersensitive thermo-response of Arabidopsis Rrs-7 accessions (Ibanez et al, 2018). In agreement with a prevalent role of this regulation in temperature-induced hypocotyl growth, mutations affecting the DWF7 and ROT3 genes were recently identified in a screen for okapi mutants that reversed the hypersensitive thermo-response of Arabidopsis Rrs-7 accessions (Ibanez et al, 2018).…”

“…Notably, BL restores thermomorphogenic growth of pif4pif5 and pifq mutants, while the inhibitor BRZ blocks enhanced elongation of wild-type plants (Appendix Fig S6), hence demonstrating that the elongation defects of pifq mutants are caused by impaired thermo-responsive activation of BR biosynthetic genes. Defects in these BR biosynthetic genes also block response to temperature in the Col-0 background, whereas BL rescues thermomorphogenic defects of these mutants (Ibanez et al, 2018), evidencing that temperature-induced hypocotyl elongation is strictly dependent on BRs. Defects in these BR biosynthetic genes also block response to temperature in the Col-0 background, whereas BL rescues thermomorphogenic defects of these mutants (Ibanez et al, 2018), evidencing that temperature-induced hypocotyl elongation is strictly dependent on BRs.…”

“…Defects in BR synthesis or BR signaling result in de-etiolated growth in the dark, severe dwarfism, delayed senesce, and increased stress tolerance, highlighting a central role of these hormones in the control of plant growth and development (Chory et al, 1991;Clouse et al, 1996;Li et al, 1996;Szekeres et al, 1996). In a screen for mutants impaired in thermomorphogenic growth, independent mutations in BR biosynthetic genes have also been identified, indicating that enhanced hypocotyl growth in response to elevated temperatures relies on increased BR levels (Gray et al, 1998;Ibanez et al, 2018). The mechanism by which external light and temperature signals are integrated into BR signaling is, however, not fully understood.…”

Molecular mechanisms governing plant responses to high temperatures

“…Meanwhile, HT induces the nuclear translocation of BZR1, enabling it to bind directly to the promoter of PIF4 to regulate its expression. This produces a feed‐forward loop that amplifies thermoresponsive growth (Ibañez et al ). Phosphorylated BZR1 cannot bind to DNA (He et al ); however, HT cannot induce the dephosphorylation of BZR1 in vivo (Oh et al ; Ibañez et al ), raising the intriguing question of how phosphorylated BZR1 regulates the expression of PIF4 at 28 °C.…”

Temperature-induced changes in the wheat phosphoproteome reveal temperature-regulated interconversion of phosphoforms

“…This includes photoreceptors that function as thermosensors in A. thaliana (Jung et al , 2016; Legris et al , 2016; Hayes et al , 2017), transcriptional regulators such as ELF3 and PIF4 in A. thaliana (Kumar et al , 2012; Box et al , 2015; Raschke et al , 2015), the role of plant hormones (Gray et al , 1998; Franklin et al , 2011; Sun et al , 2012; Wang et al , 2016 a ; Ibañez et al , 2018), and H2A.Z-containing nucleosomes that provide thermosensory information, which is used to co-ordinate the temperature transcriptome in A. thaliana and Brachypodium (Kumar and Wigge, 2010; Boden et al , 2013). However, our knowledge of high temperature-associated signalling in crops, especially wheat, remains limited.…”