Phytochrome Signaling Networks

Abstract

The perception of light signals by the phytochrome family of photoreceptors has a crucial influence on almost all aspects of growth and development throughout a plant's life cycle. The holistic regulatory networks orchestrated by phytochromes, including conformational switching, subcellular localization, direct protein-protein interactions, transcriptional and posttranscriptional regulations, and translational and posttranslational controls to promote photomorphogenesis, are highly coordinated and regulated at multiple levels. During the past decade, advances using innovative approaches have substantially broadened our understanding of the sophisticated mechanisms underlying the phytochrome-mediated light signaling pathways. This review discusses and summarizes these discoveries of the role of the modular structure of phytochromes, phytochrome-interacting proteins, and their functions; the reciprocal modulation of both positive and negative regulators in phytochrome signaling; the regulatory roles of phytochromes in transcriptional activities, alternative splicing, and translational regulation; and the kinases and E3 ligases that modulate PHYTOCHROME INTERACTING FACTORs to optimize photomorphogenesis.

Keywords: E3 ligase; PHYTOCHROME INTERACTING FACTOR; PIF; kinase; light signaling; light-regulated alternative splicing; phytochrome.

Figure 1

Structural domains of phytochromes and their roles in perception of environmental signals and downstream signaling. Light sensing is mediated by the N-terminal photosensory module of phytochrome through the bilin chromophore in the GAF domain and subsequent conformational changes of the tongue. The knot lasso of the N-terminal module interacts with PIFs upon photoactivation and induces light signaling by repressing the transcriptional activity of PIFs. Both the GAF domain and HKRD are responsible for dimerization between each monomer. The C-terminal output module directly interacts with PIF and mediates its degradation. The PRD mediates the nuclear accumulation of phytochrome, and the entire output module is required for photobody localization. Pink arrows indicate domains involved in thermal reversion, and green arrows indicate domains involved in photoconversion. Adapted with permission from Reference . Abbreviations: NTE, N-terminal extension; PΦB, phytochromobilin.

Figure 2

Models of phytochrome signaling pathways regulated by their interacting proteins. (a) Phytochrome signaling proteins regulate the size and stability of photobodies. Formation of these photobodies (shown inside dashed circles) are promoted independently by coregulators such as PCH1, PCHL, HMR, NCP, and RCB. (b) Photobodies are also sites for the degradation of PIFs. phyB,PIFs, and kinases, such as PPKs and SPAs, colocalize within the photobodies, resulting in the phosphorylation of PIFs. PIFs are subsequently ubiquitinated and degraded. (c) phyA and phyB colocalize with SPA1 within the photobodies to sequester SPA1 from COP1, suppressing COP1 activity. (d) Phosphorylated phytochromes are also targets of the COP1/SPA1 complex and the E3 ligase LRB. Phytochromes are subsequently ubiquitinated and degraded. Phosphorylated phytochromes can be dephosphorylated by phosphatases, such as FyPP and PAPPs. Abbreviations: FR, far red; FyPP, FLOWER-SPECIFIC PHYTOCHROME-ASSOCIATED PROTEIN PHOSPHATASE; phy, phytochrome; R, red; TF, transcription factor.

Figure 3

Present models of phytochrome-mediated transcriptional regulation. (a) Phytochromes interact with transcription factors (e.g., PIFs) to sequester or block their DNA-binding domain to inhibit downstream gene expression. (b) Phytochromes interact with transcription factors such as PIFs and regulate their transcriptional activities with the aid of coregulators. (c) Light triggers interactions between photoreceptors and Aux/IAA, interfering with the auxin-induced degradation of Aux/IAA by the E3 ligase SCF^TIR and thereby promoting ARF activity and related auxin signaling. (d) Phytochromes interact with transcriptional activators, such as TZP, and enhance their transcriptional activity. (e) Light-signaling-related transcription factors recruit chromatin-remodeling proteins and histone-modifying factors to regulate light-responsive gene expression. It is not known how photoreceptors regulate this recruitment. The histone-modifying factors establish or read histone marks at the chromatin, whereas the chromatin remodelers alter histone-DNA contacts, leading to a new state, with the binding of light-signaling-related transcription factors occurring at light-responsive elements. Abbreviations: FT, FLOWERING TIME; phy, phytochrome; TF, transcription factor.

Figure 4

Phytochromes directly associate with chromatin through TFs, coregulators, or both and control gene expression. (a) phyB is enriched to temperature-regulated genes at lower temperature possibly through interaction with PIFs, other TFs, or both. (b) phyA and FHY1 together associate with TFs to regulate their specific binding to different cis elements. (c) phyA and (d) FHY1 interact with TFs to regulate their specific binding to different cis elements independently. (c) phyA and (f) FHY1 interact with TFs and regulate their specific binding with the aid of unknown factors. Different DNA colors indicate different cis elements. X and Y indicate unknown factors that are involved in specific associations. Abbreviations: phy, phytochrome; TF, transcription factor.

Figure 5

Present models of light-regulated alternative splicing of pre-mRNAs. Dark conditions are shown by a dark gray background, and light conditions are shown by a white background. (a) phyB can induce alternative splicing in light-grown plants that results in the retention of intronAS within the UTR of PIF3 mRNA. The uORFs inside the intronAS sequence inhibit translation of the PIF3 main ORF. Panel a adapted with permission from Reference . (b) SFPS and RRC1 directly interact with phyB and regulate pre-mRNA splicing. (c) In Physcomitrella patens, phytochromes directly regulate alternative splicing by interacting with splicing regulators in the spliceosome. Panel c adapted with permission from Reference . (d) Light regulates alternative splicing through the control of transcriptional elongation. Plants exposed to light show faster gene transcription than plants in the dark. This serves as a control for alternative mRNA splicing decisions. Panel d adapted with permission from Reference . Abbreviations: hnRNP, heterogenous nuclear ribonucleoprotein; intronAS, intron alternative splicing; phy, phytochrome; pre-mRNA, precursor messenger RNA; RNAPII, RNA polymerase II; SS, splice site; snRNP, small nuclear ribonucleoprotein; uORF, upstream open reading frame; UTR, untranslated region.

Figure 6

Present models of translational control by phytochromes. (a) Active phytochrome (Pfr form) interacts with the cytosolic protein PNT1 and inhibits the translation of PORA mRNA. (b) TOR and RPS6 transmit light signals to enhance protein translation in de-etiolating Arabidopsis seedlings. (c) P-bodies control the selective translation for optimal development of young Ambidopsis seedlings. Abbreviations: CRY, cryptochrome; P-body, processing body.