IN THIS ISSUE

SPA-rring Partner for Phytochrome A?

Plants are capable of detecting many wavelengths of light at intensities that vary over several orders of magnitude (Kendrick and Kronenberg 1994 ). Although the structure and function of the photoreceptors plants use to do this are becoming increasingly well understood, the molecular details of the signal transduction pathways they activate remain poorly defined (for reviews, see Ahmad and Cashmore 1996a ; von Arnim and Deng 1996 ; Barnes et al. 1997 ; Chory 1997 ; Huala et al. 1997 ; Ahmad et al. 1998 ). Without detailed information on early events in these pathways, it is difficult to determine how light perception by specific photoreceptors interfaces with other environmental signals and with endogenous cues to shape plant growth and development.

Investigations of the phytochromes, the photoreceptors primarily responsible for directing plant responses to red light (R) and far-red light (FR), have uncovered a number of explanations for the complexity inherent in light signal transduction. For example, most plant species possess several related phytochromes that absorb light at similar wavelengths. The downstream responses triggered by each phytochrome can vary, with the specific contribution of individual phytochromes to the overall response depending upon the light conditions. Nevertheless, by varying light regimes and carefully dissecting the subsequent developmental and transcriptional responses in different phy mutants and transgenics, it has been possible to define light conditions under which the majority of the signaling can be ascribed to a single phytochrome.

This kind of detailed information is a prerequisite for studying the signal transduction pathways that link an activated photoreceptor with a response. One useful application has been in the design of screens that alter signal transduction from only one phytochrome–such screens have led to the identification of loci that appear to mediate phyB-specific R-induced signal transduction (Ahmad and Cashmore 1996b ; Wagner et al. 1997 ) and phyA-specific FR-induced signal transduction (Whitelam et al. 1993 ) in Arabidopsis.

As they report on pages 19-33 of this issue, Hoecker et al. have exploited a rather different strategy–a screen for extragenic mutations that suppress several phyA mutant phenotypes in continuous FR–to identify a novel phyA-specific signaling intermediate. The authors show that the five recessive phyA suppressor mutations isolated during their screen all fall in a single gene, termed SUPPRESSOR OF PHYA (SPA1), which appears to encode an early acting negative regulator of phyA-specific signal transduction.

Hoecker et al. identified the spa1 mutations on the basis of their ability to restore a number of developmental and physiological responses in a partial loss-of-function phyA mutant, phyA-105 (Xu et al. 1995 ). The most obvious of these, and the one the authors used in their primary screen, is the phyA-mediated inhibition of hypocotyl elongation in continuous FR–under these conditions, spa1 phyA-105 double mutants are much shorter than are their phyA-105 progenitors. However, in addition to exhibiting reduced hypocotyl growth, spa1 phyA-105 mutants accumulate significant levels of anthocyanins in continuous FR (phyA-105 single mutants do not), and they exhibit the block in chlorophyll biosynthesis ("greening") that is conditioned by exposing wild-type seedlings to FR before switching them to white light (Barnes et al. 1996 ).

The authors go on to show that in continuous R and FR, the spa1 mutations also condition phenotypes in plants carrying wild-type alleles of PHYA. These phenotypes are similar to those displayed by transgenic Arabidopsis seedlings overexpressing phyA (Boylan and Quail 1991 ) and by the tomato high pigment mutants (Kendrick et al. 1997 ); however, Hoecker et al. present immunodetection data to demonstrate that the spa1 mutations do not increase phyA protein levels. Instead, the authors suggest that spa1 mutations may act to increase the sensitivity of phyA to continuous FR and R. In other words, for a given amount of light, the signal triggered by phyA in the presence of the spa1 mutation is amplified.

Hoecker et al. back up this conclusion with data showing that the potency of the spa1 phenotypes depends on the activity of the phyA allele: spa1 phenotypes are more pronounced in the wild-type PHYA background than they are in the phyA-105 mutant. Further supporting evidence comes from experiments demonstrating that the spa1 mutations have no detectable effect in the absence of functional phyA (i.e., in a phyA null mutant). These latter experiments also serve to illustrate that SPA1 activity depends on light detection by phyA. Moreover, because they show that SPA1 does not affect the transduction of signals from other photoreceptors, the data from Hoecker et al.'s experiments with phyA null mutants provide a strong indication that SPA1 plays a specific role in phyA-triggered signaling.

The authors offer two potential models to explain their observations. In the first, they propose that SPA1 may interact directly with phyA, either to prevent the binding of a positive regulator or to directly modulate the signaling activity of phyA. One possibility is that SPA1 may encode (or modify the activity of) a kinase that phosphorylates the N terminus of phyA to reduce its signaling capacity. This hypothesis ties in nicely with previous structure-function studies suggesting that the phosphorylation of Ser residues near the N terminus of phyA may attenuate phyA-mediated signaling (see, e.g., Stockhaus et al. 1992 ; Jordan et al. 1995 ), biochemical evidence for which has been published (McMichael and Lagarias 1990 ; Lapko et al. 1997 ).

Another indication that phosphorylation/dephosphorylation reactions may mediate early steps in phytochrome-mediated signaling comes from the recent identification of cyanobacterial proteins with structural and functional similarities to higher plant phytochromes–these proteins also exhibit sequence similarity to histidine kinases and are capable of phosphorylating a small response regulator (Lamparter et al. 1997 ; Yeh et al. 1997 ).

In their second model, Hoecker et al. propose that SPA1 may act on a positive regulator of phyA signal transduction to attenuate its activity. Among the testable possibilities suggested by the authors are FHY1 and FHY3, recessive mutations in which appear to lead to reductions in flux through phyA-mediated signaling pathways (Whitelam et al. 1993 ; Barnes et al. 1996 ). Quantitative trait loci that may define additional positively acting regulators of phyA-mediated signal transduction have also been reported recently (Yanovsky et al. 1997 ).

The authors' work on the spa1 mutants adds to the accumulating body of information suggesting that light signaling is not "all-or-nothing" and that many of the photomorphogenetic and transcriptional responses to light are governed quantitatively by flux through specific signaling pathways. These refinements to a straightforward "on/off" activity may facilitate input from other light signaling pathways. If this is so, signaling components that appear to function at later steps in light signal transduction, such as the COP/DET/FUS complex (von Arnim and Deng 1996 ), Ca²⁺, calmodulin, and GTPases (Barnes et al. 1997 ; see also Calenberg et al. 1998 , in this issue), may define points at which signaling pathways triggered by different photoreceptors interact.

Light signals also interface with other environmental signals, as well as endogenous cues such as the circadian clock (Anderson et al. 1997 ) and the plant's metabolic status (e.g., Dijkwel et al. 1997 ; Van Oosten et al. 1997 ). Moreover, recent evidence that the illumination of small clusters of cells at the base of dark-grown tobacco cotyledons can trigger the activation of a light-regulated reporter construct throughout the cotyledon (Bischoff et al. 1997 ) suggests that signals from photoreceptors can be propagated over some distance. Together with the work reported by Hoecker et al. and other ongoing efforts to identify and characterize the molecules that directly modify the signaling capacity of individual photoreceptors, these data will help to explain how light perception and signal transduction fit in with the bigger picture of plant growth and development.

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