Trends in Plant Science
Dissecting the phytochrome A-dependent signaling network in higher plants
Section snippets
Molecular properties and functional roles of phyA
Historically, phyA was the first phytochrome discovered in higher plants [1] and all higher plants have a distinct phyA among phytochrome families of variable sizes. All known phyAs from higher plants are abundant in dark-grown plants and are rapidly degraded upon light exposure. They are therefore classified as a light-labile phytochrome. The purified phyA molecule is a soluble, dimeric chromoprotein that consists of two ∼125-kDa polypeptides with a single covalently attached tetrapyrrole
PhyA control of gene expression
In response to the far-red light signal, it is thought that phyA leads to photomorphogenic development largely by controlling far-red-light-responsive nuclear gene expression. Traditional approaches have revealed several dozen individual genes whose expression is regulated by light 11, 12, 13. Recently, DNA-microarray technology has been used to investigate genome-wide gene-expression profiles controlled by phyA 14, 15. These studies provided substantial evidence for the notion that phyA is the
Light-induced nuclear import of phyA
Because phytochromes are synthesized in the cytoplasm, we must address the question of how the photoactivated phytochromes control light-responsive gene expression in the nucleus. Early studies using an immunohistological approach and cell fractionation assays supported the notion that phytochromes are predominantly localized outside the nucleus [1]. Recently, it was shown that upon photoconversion of Pr to Pfr, all phytochrome species tagged with green fluorescent protein (GFP) can translocate
PhyA as a light-regulated kinase
How does photoactivated phyA transfer the light signal to its downstream targets? Does phyA have enzymatic activity? Recent studies using recombinant DNA technology have added much convincing evidence to the longstanding view of phytochromes as light-regulated kinases 19, 20. Furthermore, the recent discovery of phytochrome-like photoreceptors in bacteria has also provided strong evolutionary evidence in support of such a view [21]. Bacteriophytochromes can perceive light signals and relay
Genetically identified phyA-specific signaling intermediates
Detailed genetic analyses have suggested that phyA signal transduction has at least two branches, which correspond to VLFR and HIR signaling. The Columbia (Col) ecotype does not respond to very low light fluences [31]. Two quantitative trait loci, VLF1 and VLF2, are responsible for the expression of VLFR [31] but their molecular nature is currently unknown. Mutants for several components affected in the HIR branch of phyA signaling pathway have been identified (Fig. 2), including FHY1, FHY3 [32]
PhyA can directly target light signals to light-responsive promoters
The finding that PIF3, a member of the bHLH superfamily of transcriptional regulators, can interact directly with both phyA and phyB suggests that phytochromes might regulate nuclear gene expression via direct interaction with transcription factors 53, 54. In support of this notion, phyB can bind specifically and photoreversibly to PIF3 that is already bound to its cognate DNA-binding site (the light-responsive G-box DNA sequence CACGTG). Furthermore, the expression of CCA1 and LHY1, which have
Regulated proteolysis in phyA signaling
There is accumulating evidence that regulated proteolysis plays a crucial role in controlling the timing and amplitude of phyA signaling processes. First, phyA itself is rapidly degraded upon photoconversion to the Pfr form and this degradation involves the ubiquitin–proteasome pathway [57]. This downregulation of the intracellular phyA levels in response to light probably provides an adaptation mechanism to the ambient light environment.
Far-red-light activation of phyA also regulates
How are the COP proteins inactivated?
It is generally assumed that light-induced photomorphogenic development requires the inactivation of these COP/DET/FUS proteins. However, little is known about how the light-activated photoreceptors regulate the activities of those downstream COP/DET/FUS proteins to bring about the physiological responses. Although it has been shown that nuclear abundance of COP1 is regulated by light acting through these photoreceptors [71], the mechanisms governing this process are largely unknown. Recent
Conclusions and prospects
Dramatic progress has been made during the past decade in understanding phyA signaling mechanism, largely owing to the use of molecular genetics in the model plant Arabidopsis. However, it has also become clear that our information about the nature and extent of the phyA-mediated signaling network is still limited and fragmented. Much remains to be learned to build a connected phyA signaling network with an understanding of how the various nodes of the network interact to transmit the light
Acknowledgements
We thank Jessica Habashi for reading and commenting on this manuscript. Our research on phytochrome signaling was supported by a grant from the US National Institutes of Health (GM-47850) to X.W.D. H.Y.W. was supported by a US National Institutes of Health postdoctoral fellowship.
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