Phytochrome‐mediated inhibition of shade avoidance involves degradation of growth‐promoting bHLH transcription factors

Abstract

SummaryPlant growth and development are particularly sensitive to changes in the light environment and especially to vegetational shading. The shade-avoidance response is mainly controlled by the phytochrome photoreceptors. In Arabidopsis, recent studies have identified several related bHLH class transcription factors (PIF, for phytochrome-interacting factors) as important components in phytochrome signaling. In addition to a related bHLH domain, most of the PIFs contain an active phytochrome binding (APB) domain that mediates their interaction with light-activated phytochrome B (phyB). Here we show that PIF4 and PIF5 act early in the phytochrome signaling pathways to promote the shade-avoidance response. PIF4 and PIF5 accumulate to high levels in the dark, are selectively degraded in response to red light, and remain at high levels under shademimicking conditions. Degradation of these transcription factors is preceded by phosphorylation, requires the APB domain and is sensitive to inhibitors of the proteasome, suggesting that PIF4 and PIF5 are degraded upon interaction with light-activated phyB. Our data suggest that, in dense vegetation, which is rich in far-red light, shade avoidance is triggered, at least partially, as a consequence of reduced phytochrome-mediated degradation of transcription factors such as PIF4 and PIF5. Consistent with this idea, the constitutive shadeavoidance phenotype of phyB mutants partially reverts in the absence of PIF4 and PIF5.

Photobody Localization of Phytochrome B Is Tightly Correlated with Prolonged and Light-Dependent Inhibition of Hypocotyl Elongation in the Dark

“…There is still no direct evidence showing that PIF3 degradation occurs on photobodies. Therefore, we cannot exclude the possibility that photobodies are only involved in a posttranslational modification of PIFs, such as phosphorylation (Al-Sady et al, 2006;Lorrain et al, 2008;Shen et al, 2008;Bu et al, 2011;Ni et al, 2013), and that PIF degradation occurs elsewhere . It is also important to note that although our data show a clear separation between PIF3 degradation and the regulation of its transcriptional activity in the R-FR-D transition (Fig.…”

“…The current model suggests that phytochromes inhibit PIFs by at least two mechanisms. First, most PIF proteins are stable only in the dark; in the light, photoactivated phytochromes bind directly to PIFs and trigger their phosphorylation and subsequent degradation in the light (Al-Sady et al, 2006;Lorrain et al, 2008;Shen et al, 2008;Leivar and Quail, 2011;Ni et al, 2013). Second, phytochromes can inhibit the transcriptional activity of PIF1 and PIF3 by removing them from the promoters of their target genes (Park et al, 2012).…”

Phytochromes and Phytochrome Interacting Factors

“…Among all known PIFs, PIF4 uniquely regulates hypocotyl elongation in response to light, shade, temperature, and diurnal conditions Lorrain et al, 2008;Franklin et al, 2011;Kumar et al, 2012). It does so by binding to the promoter sequences and activating the expression of target genes, including regulatory genes involved in auxin biosynthesis.…”

PIFs: Systems Integrators in Plant Development

“…In dark-grown seedlings (i.e., etiolated), PIF proteins accumulate, whereas upon exposure to light (deetiolation response), photoactivated phy Pfr translocates into the nucleus and induces a rapid decline in the abundance of PIFs (particularly the PIF quartet [PIFq] members PIF1, PIF3, PIF4, and PIF5), with half-lives of 5 to 20 min (Bauer et al, 2004;Monte et al, 2004;Shen et al, 2005Shen et al, , 2007Al-Sady et al, 2006;Nozue et al, 2007;Lorrain et al, 2008). This pathway involves direct interaction of the PIFs with phyA and/or phyB in nuclear speckles (Bauer et al, 2004;Al-Sady et al, 2006;Shen et al, 2008), which results in rapid phosphorylation, ubiquitylation, and degradation via the ubiquitin-proteasome system Al-Sady et al, 2006;Shen et al, 2007Shen et al, , 2008Lorrain et al, 2008). Whereas both phyA and phyB dominate the rapid light-induced degradation of the PIFs (Bauer et al, 2004;Al-Sady et al, 2006;Shen et al, 2007Shen et al, , 2008), phyB appears to have a prominent function under prolonged light conditions (Leivar et al, 2012a;Soy et al, 2012).…”