Degrading to inhibit: a role for Phytochrome Interacting Factors in determining hypocotyl growth under UV-B.

Abstract

Plants perceive light through specific photoreceptors for red/far-red, blue, and UV-B wavelengths of the electromagnetic spectrum, regulating physiological responses such as hypocotyl elongation, in a process known as photomorphogenesis. Over the last two decades, a diverse panel of mutants exhibiting defects in light-regulated hypocotyl elongation has been used to elucidate the molecular links between photoreceptor signalling and its downstream physiological responses (de Wit et al., 2016a). At the molecular level, this link involves the interplay of three transcription factor families: EIN3, PIFs, and HY5 (Shi et al., 2018). The latter is a positive regulator of photomorphogenesis whilst the former two are repressors and, as such, promote hypocotyl elongation. The UVR8 photoreceptor and its signalling pathway also serve as a regulatory signal for plant morphogenesis, and its interaction with the E3 ubiquitin ligase COP1 induces HY5 induction and stability (Podolec and Ulm, 2018). However, the mechanisms by which UVR8 triggers hypocotyl growth inhibition have only just begun to be clarified. In their study in this issue of The Plant Journal, (Tavridou et al., 2019) show that UVR8-mediated inhibition of PIF4 and PIF5 is an important and intrinsic part of UVR8 photomorphogenic signalling. The laboratory of Roman Ulm, Professor at the Department of Botany and Plant Biology at the University of Geneva (Geneva, Switzerland), has been carrying out seminal work on the plant responses to UV-B radiation for several years. Roman joined the University of Geneva in 2010 and has been the Director of the department since 2017, previously having been an independent group leader at the University of Freiburg (Freiburg, Germany). The work described in this article took over 3 years for the joint co-authors, postdocs Eleni Tavridou and Marie Pireyre, who joined the project in 2017. The major goal of their work was to investigate if there is a role for UVR8 photoreceptor-induced destabilization of PIF4 and PIF5 in UV-B-induced gene repression and hypocotyl growth inhibition. Previous work described an effect of UV-B on PIF4 and PIF5 stability, particularly when plants are grown in shade conditions (high FR; very low R:FR ratio of 0.05) or under elevated temperature (28°C), and associated shade and thermomorphogenic responses were antagonized by UV-B (Hayes et al., 2014, 2017). However, a role for PIF4 and PIF5 destabilization in a standard hypocotyl growth assay and UV-B-induced gene repression had not been described before. Their work thus reveals a novel role for PIF4 and PIF5 degradation as part of the core UVR8 signalling pathway. Tavridou and colleagues achieved this by discovering of a role for UVR8 photoreceptor-induced destabilization of PIF4 and PIF5 in UV-B-induced gene repression and hypocotyl growth inhibition (Tavridou et al., 2019). PIF4 and PIF5 are bHLH transcription factors that play crucial roles in the regulation of genes associated with hypocotyl elongation. UV-B-induced inhibition of hypocotyl growth is a broadly used phenotypic assay to study the activity of the UVR8 photoreceptor and its signalling pathway. UV-B exposure results in monomerization of UVR8, leading to its interaction with COP1 (Rizzini et al., 2011), which affects the targeting of PIF4 and PIF5 to the proteasome via an unknown mechanism (see Figure). The results provide evidence for a mechanism underlying hypocotyl growth inhibition that involves UVR8-induced degradation of PIF4 and PIF5. In agreement, binding of PIF4 and PIF5 to promoters of elongation marker genes is reduced under UV-B exposure, concurring with the transcriptional downregulation of these genes under UV-B. Moreover, pif4pif5 mutants have a short hypocotyl phenotype, in agreement with the conclusion that UVR8-induced PIF4 and PIF5 degradation contributes to hypocotyl growth inhibition under UV-B. Not only are these conclusions immensely informative in their own right, they also raise a number of important questions, for example: Which E3 ubiquitin ligase(s) is responsible for the degradation of PIF4 and PIF5 in response to UV-B? and What mechanistically links UVR8 photoreceptor activation to PIF4 and PIF5 degradation? Regarding the second question, there is currently no evidence that UVR8 interacts directly with PIFs in a manner analogous to that of phytochromes and cryptochromes (Ma et al., 2016; de Wit et al., 2016b). However, a recent publication (Sharma et al., 2019) suggests that PIF5 is stabilized by direct interaction with COP1, and that UVR8 disrupts this stabilization through its UV-B-activated interaction with COP1. The above questions notwithstanding, the highlighted paper provides compelling evidence linking PIF4 and PIF5 to UV-dependent hypocotyl inhibition and, as such, adds this function to the vast range of roles displayed by these enigmatic proteins.