Light perception and signalling by phytochrome A

Journal of Experimental Botany, Vol. 65, No. 11, pp. 2835–2845, 2014 doi:10.1093/jxb/ert379 Advance Access publication 12 November, 2013 REVIEW PAPER Light perception and signalling by phytochrome A J. J. Casal1,2,*, A. N. Candia1 and R. Sellaro1 1 IFEVA, Facultad de Agronomía, Universidad de Buenos Aires and CONICET, 1417 Buenos Aires, Argentina Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires–CONICET, C1405BWE Buenos Aires, Argentina 2 Received 30 August 2013; Revised 11 October 2013; Accepted 14 October 2013 Abstract In etiolated seedlings, phytochrome A (phyA) mediates very-low-fluence responses (VLFRs), which initiate de-etiolation at the interphase between the soil and above-ground environments, and high-irradiance responses (HIR), which complete de-etiolation under dense canopies and require more sustained activation with far-red light. Lightactivated phyA is transported to the nucleus by FAR-RED ELONGATED HYPOCOTYL1 (FHY1). The nuclear pool of active phyA increases under prolonged far-red light of relatively high fluence rates. This condition maximizes the rate of FHY1–phyA complex assembly and disassembly, allowing FHY1 to return to the cytoplasm to translocate further phyA to the nucleus, to replace phyA degraded in the proteasome. The core signalling pathways downstream of nuclear phyA involve the negative regulation of CONSTITUTIVE PHOTOMORPHOGENIC 1, which targets for degradation transcription factors required for photomorphogenesis, and PHYTOCHROME-INTERACTING FACTORs, which are transcription factors that repress photomorphogenesis. Under sustained far-red light activation, released FHY1 can also be recruited with active phyA to target gene promoters as a transcriptional activator, and nuclear phyA signalling activates a positive regulatory loop involving BELL-LIKE HOMEODOMAIN 1 that reinforces the HIR. Key words: CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1), high-irradiance response (HIR), nuclear translocation, phytochrome, PHYTOCHROME INTERACTING FACTOR (PIF), very-low-fluence response (VLFR). Introduction Plant phytochromes are a family of red/far-red light photoreceptors that bear a linear tetrapyrrole chromophore attached through a cysteine residue to their N-terminal domain (Vierstra and Zhang, 2011). This review is focused on phytochrome A (phyA), a key member of the family with specific and shared functions. Phytochromes are synthesized in the inactive Pr form. Pr absorbs maximally in red light and, after excitation, relaxes into the active, Pfr form. In turn, Pfr has its maximum absorbance in far-red, which back-converts the molecule into Pr. Due to the partial overlap between Pr and Pfr absorption spectra (Fig. 1, inset), far-red light is able to transform a small proportion of the Pr molecules into Pfr. phyA monomers have a mol. wt of ~120 kDa and form phyA–phyA homodimers but no heterodimers with other family members (Sharrock and Clack, 2004). Subcellular localization of phyA In darkness, phyA is dispersed in the cytoplasm (Kircher et al., 2002; Toledo-Ortiz et al., 2010). There is nuclear phyB but no detectable nuclear phyA in dark-grown seedlings, and in chimeric phyA–phyB phytochromes this differential pattern is defined by the C-terminal domain (Oka et al., 2012). Nuclear localization of phyA can be detected after 5 min of irradiation with red or far-red light that transform part of the Pr pool into Pfr (Toledo-Ortiz et al., 2010). phyA lacks a known © The Author 2013. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: * To whom correspondence should be addressed. E-mail: 2836 | Casal et al. nuclear localization signal, and its nuclear presence depends primarily on FAR-RED ELONGATED HYPOCOTYL1 (FHY1) and secondarily on its homologue FHY1-LIKE (FHL) (Hiltbrunner et al., 2005, 2006). The nuclear localization signal and the phyA-interaction domain of FHY1 (present in the N- and the C-terminus, respectively) are conserved in different species and are sufficient for FHY1 to transport phyA to the nucleus (Genoud et al., 2008). Under daily photoperiods of far-red light, the number of nuclei with speckles containing phyA is higher during daytime than during the night, but the levels increase before the beginning of the day, arguing in favour of a circadian control of phyA localization (Kircher et al., 2002). phyA abundance In dark-grown seedlings, phyA is the most abundant member of the phytochrome family (Sharrock and Clack, 2002). Light down-regulates the abundance of phyA at transcriptional and post-transcriptional levels. Compared with full darkness, light perceived by phyA or phyB represses the expression of the PHYA gene (Quail, 1994; Cantón and Quail, 1999). This repression is accompanied by a rapid decrease in H3K4me3 and H3K9/14ac activating chromatin marks and a rapid increase in the H3K27me3 repressive mark at the PHYA promoter (Jang et al., 2011). These chromatin modifications are mediated in part by phyB (Jang et al., 2011). While phyA is stable in the Pr form, the half-life of phyA Pfr is 0.5–2 h due to phyA ubiquitination and 26S proteasome degradation (Clough and Vierstra, 1997; Hennig et al., 1999). Both, nuclear and cytoplasmic pools are degraded in the proteasome, but nuclear degradation is faster (Debrieux and Fankhauser, 2010; Toledo-Ortiz et al., 2010). Degradation of phyA depends primarily on CULLIN1-based ubiquitin E3 ligases (Quint et al., 2005; Debrieux et al., 2013) and, under certain conditions, on CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) ubiquitin E3 ligase (Seo et al., 2004; Debrieux et al., 2013). Under light/dark cycles, phyA accumulates during the night and becomes rapidly degraded during the day (Sharrock and Clack, 2002), despite the fact that PHYA promoter activity is maximal during the light phase due to the control by the circadian clock (Tóth et al., 2001). phyA purified from dark-grown oat seedlings is phosphorylated (Lapko et al., 1999), and purified recombinant oat phyA autophosphorylates (Han et al., 2010). When expressed in Arabidopsis, mutations or deletions involving phosphorylation sites present at the N-terminal extension of phyA enhance the stability of oat phyA (Han et al., 2010) but reduce the stability of Arabidopsis phyA (Trupkin et al., 2007). These discrepancies might reflect the use of oat versus Arabidopsis phyA in the Arabidopsis background. Pfr to Pr thermal reversion Dark reversion is the light-independent conversion of Pfr into Pr and reveals the instability of Pfr likely when it is forming a heterodimer with Pr. This process affects the abundance of Pfr but not that of total phyA. In Arabidopsis only some accessions show thermal reversion of phyA Pfr, and the source of this natural variation is extragenic to PHYA, indicating that the cellular environment strongly affects Pfr stability (Hennig et al., 1999; Eichhenberg et al., 2000). Molecular and c (...truncated)