Review
doi: 10.1038/s41467-019-13045-0.
Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants
Affiliations
- PMID: 31745087
- PMCID: PMC6864062
- DOI: 10.1038/s41467-019-13045-0
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Review
Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants
Nat Commun.
.
Abstract
Phytochromes are bilin-binding photosensory receptors which control development over a broad range of environmental conditions and throughout the whole plant life cycle. Light-induced conformational changes enable phytochromes to interact with signaling partners, in particular transcription factors or proteins that regulate them, resulting in large-scale transcriptional reprograming. Phytochromes also regulate promoter usage, mRNA splicing and translation through less defined routes. In this review we summarize our current understanding of plant phytochrome signaling, emphasizing recent work performed in Arabidopsis. We compare and contrast phytochrome responses and signaling mechanisms among land plants and highlight open questions in phytochrome research.
Conflict of interest statement
The authors declare no competing interests.
Figures
Control of phytochrome activity. a Factors controlling phytochrome activity. Phytochromes exist in two conformations, Pr and Pfr, the latter being the active form. They exist as dimers so three species can be found. Each monomer can be activated by red light (R) and inactivated by far-red light (FR) or by thermal reversion, a process that depends on temperature (T). At least in the case of phyB, Pfr in heterodimers reverts much faster than that in homodimers, allowing phyB to perceive temperature both during the day and during the night. b Plant phytochrome absorption spectra of the Pr and Pfr conformations. In dark-adapted seedlings phytochromes are in the Pr form. Upon a saturating R pulse, due to overlapping absorption spectra of Pr and Pfr, only 87% of Pfr is achieved. c Action spectra for phyA and phyB in the control of hypocotyl elongation. Data from Klose et al.. Fluence rate response curves are measured at different wavelengths and fluence rate that leads to 40% inhibition compared with dark control is determined. In order to specifically determine action spectra for phyA and phyB, for phyB the curve was performed with phyB-GFP/phyAphyB seedlings, and for phyA using phyB-5 seedlings. Values are relative to the response obtained at the most efficient wavelength in each case
Structural domains of phytochromes and their role in perception of environmental signals and downstream signaling. NTE N-terminal extension, PSM photosensory module, CTM C-terminal module. Modified from Burgie et al.
Simplified mechanism for phytochrome control of transcription factors in different light environments. a Below the soil surface during etiolated growth. For simplicity we consider that phytochromes remain inactive (Pr) below the soil surface, which results in accumulation of transcription factors PIFs, EIN3, and ARFs and subsequent induction of etiolation and auxin response genes. The COP1/SPA ubiquitin E3 ligase accumulates in dark and leads to proteasome-mediated degradation of HY5, a transcription factor that suppresses the expression of genes required for etiolation and induces expression of genes required for de-etiolation. b During de-etiolation upon light perception. Light perception activates phytochromes (Pfr) which promote de-etiolation by directly inhibiting PIFs and EIN3, and indirectly inhibiting ARFs by stabilizing Aux/IAA proteins. The Pfr form of either phyA or phyB interacts with SPA proteins, resulting in inhibition of COP1/SPA. This results in stabilization of HY5 leading to induction of de-etiolation related gene expression and repression of etiolation genes. c In a deetiolated plant in response to shade (reduced R/FR). Low R/FR in shade reduces the fraction of active phytochrome (Pfr/Ptot). PIFs accumulate and induce growth-promoting gene expression. In addition, PIFs induce a negative feedback loop exemplified by HFR1 expression. HFR1 (and other HLH proteins) binds to PIFs forming non-DNA-binding heterodimers. COP1/SPA is also involved in this loop by leading HFR1 to proteasome-mediated degradation. Arrows indicate positive regulation, blunt-ended arrows indicate negative regulation, and dotted-lined arrows indicate nucleo-cytoplasmatic relocalization
Mechanisms of phytochrome-mediated regulation of transcription factors. a From top to bottom, sequential steps by which Pfr inhibits PIFs. Top: PfrA interacts with PIF1 and PIF3 while PfrB interacts with PIF1–PIF8. Middle left: for PIF1, 3 and 4 phytochrome inhibits DNA binding. Middle right: Interaction with Pfr leads to phosphorylation of PIFs. Many kinases have been found to phosphorylate PIFs (see text) with PPKs phosphorylating PIFs in response to light. Bottom: after light-induced phosphorylation, PIF3 is degraded by LRBs and EBFs with phyB co-degradation occurring in the LRB-mediated process (left, center), phosphorylated PIF7 interacts with 14-3-3 proteins and remains in the cytoplasm (right). b Other mechanisms of transcriptional control by phytochromes. Left: PfrA and PfrB interact with SPA and inhibit the COP1/SPA complex. Center: PfrB interacts with EIN3 to promote ERF-mediated EIN3 degradation. Right: PfrA and PfrB interact with Aux/IAA to prevent their degradation by SCFTIR1/AFB. c Patterns of PIF abundance depending on the developmental state and growth conditions. In etiolated seedlings PIFs accumulate to high levels, promoting etiolated growth. Upon light exposure, PIFs are rapidly degraded in a phytochrome-dependent manner, with half-lives of ~5 min for PIF1 and PIF5, and ~10 min for PIF3 and PIF4 (left). In contrast, in light-grown seedlings PIFs are under strong transcriptional control, allowing accumulation of the protein even in conditions when phytochrome activity is predicted to be high (right), SD (short days), LD (long days)
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