Abstract
Small increases in temperature result in enhanced elongation of the hypocotyl and petioles and hyponastic growth, in an adaptive response directed to the cooling of the leaves and to protect the shoot meristem from the warm soil. This response, collectively termed as thermomorphogenesis, relies on the faster reversion of phyB Pfr at warmer temperatures, which leads to enhanced activity of the basic-helix-loop-helix PHYTOCHROME INTERACTING FACTOR 4 (PIF4). PIF4 acts as a molecular hub integrating light and temperature cues with endogenous hormonal signaling, and drives thermoresponsive growth by directly activating auxin synthesis and signaling genes. Growth promotion by PIF4 depends on brassinosteroid (BR) signaling, as indicated by the impaired thermoresponse of BR-defective mutants and the partial restoration of pifq thermoresponsive defects by brassinolide (BL) application. Also, phyB limits thermomorphogenic elongation through negative regulation of the E3 ubiquitin ligase COP1 that triggers nuclear degradation of multiple photomorphogenesis-promoting factors acting antagonistically to PIF4. COP1 is indeed observed to accumulate in the nucleus in darkness, or in response to warm temperatures, with constitutive photomorphogenic cop1 mutants failing to respond to temperature. Here we explored the role of BR signaling on COP1 function, by growing cop1 seedlings on BL or the inhibitor brassinazole (BRZ), under different light and temperature regimes. We show that weak cop1 alleles exhibit a hyposensitive response to BL. Furthermore, while cop1-6 mutants display as described a wild-type response to temperature in continuous darkness, this response is abolished by BRZ. Application of this inhibitor likewise suppressed temperature-induced COP1 nuclear accumulation in N. benthamiana leaves. Overall these results demonstrate that cop1-6 is not a temperature-conditional allele, but this mutation allows for a partially active protein which unveils a pivotal role of active BR signaling in the control of COP1 activity.
Highlights
Light and temperature are key environmental factors regulating plant growth and development
The cop1-6 allele was previously described as a temperatureconditional mutation (Hsieh et al, 2000), given that this mutant exhibits a constitutively photomorphogenic development in the dark when grown at temperatures below 28°C, but elongated hypocotyls above 28°C
The CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1)/SPA complex was recently established to repress BRASSINOSTEROID INSENSITIVE 2 (BIN2)-mediated phosphorylation of the PHYTOCHROME INTERACTING FACTORS (PIFs) transcription factors (Bernardo-Garcıá et al, 2014; Ling et al, 2017), indicating that antagonism between light and BR signaling in photomorphogenic development may potentially depend on COP1 regulation of BR signaling
Summary
Light and temperature are key environmental factors regulating plant growth and development. Warm temperatures produce morphological changes in the light, which contribute to protect the shoot meristem from the warm soil and to avoid heat-induced damage of the photosynthetic machinery (Quint et al, 2016). This adaptive response, known as thermomorphogenesis, leads to elongation of the hypocotyl and the petioles, and hyponastic growth, and relies on the ability of plants of integrating external light and temperature cues with the inner circadian clock, to the coordinated regulation of endogenous plant hormones such as auxin, gibberellin and brassinosteroids (Casal and Balasubramanian, 2019; Gil and Park, 2019). Lightinduced nuclear translocation of phytochrome B (phyB) mediates phosphorylation and subsequent degradation of these regulators that function as central hubs of a hypocotyl elongation regulatory cascade leading to direct activation of the auxin biosynthetic TAA1 and YUCCA genes, in addition to the modulation of multiple cell wall loosening enzymes with a role in directional cell expansion (Zhang et al, 2013)
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