Characterization of spa mutants in the moss Physcomitrella provides evidence for functional divergence of SPA genes during the evolution of land plants

Abstract

The Arabidopsis COP1/SPA complex is a key repressor of photomorphogenesis that suppresses light signaling in the dark. Both COP1 and SPA proteins are essential components of this complex. Although COP1 also exists in humans, SPA genes are specific to the green lineage.To elucidate the evolution of SPA genes we analyzed SPA functions in the moss Physcomitrella patens by characterizing knockout mutants in the two Physcomitrella SPA genes PpSPAa and PpSPAb.Light-grown PpspaAB double mutants exhibit smaller gametophores than the wild-type. In the dark, PpspaAB mutant gametophores show enhanced continuation of growth but etiolate normally. Gravitropism in the dark is reduced in PpspaAB mutant protonemata. The expression of light-regulated genes is mostly not constitutive in PpspaAB mutants. PpSPA and PpCOP1 interact; PpCOP1 also interacts with the transcription factor PpHY5 and, indeed, PpHY5 is destabilized in dark-grown Physcomitrella. Degradation of PpHY5 in darkness, however, does not require PpSPAa and PpSPAb.The data suggest that COP1/SPA-mediated light signaling is only partially conserved between Arabidopsis and Physcomitrella. Whereas COP1/SPA interaction and HY5 degradation in darkness is conserved, the role of SPA proteins appears to have diverged. PpSPA genes, unlike their Arabidopsis counterparts, are only required to suppress a subset of light responses in darkness.

Shedding light on the evolution of light signalling

“…However, these studies also suggest that regulatory mechanisms partially diverged and that species‐specific rewiring of evolutionarily ancient components might have been an important mechanism in the evolution of light signalling networks (Han et al ., ). Artz et al . provide convincing evidence that this is also true for the COP1/SPA/HY5 module.…”

“…Phytochromes and cryptochromes have been studied in different green organisms, including mosses, ferns, and seed plants, but research on signalling networks acting downstream of the photoreceptors has focused almost exclusively on seed plants. In this issue of New Phytologist , Artz et al (; pp. 1613–1626) show that the two SPA genes in Physcomitrella patens , SPAa and SPAb , play a role in light signalling but that there are striking differences compared to the function of SPAs in Arabidopsis.…”

“…Both COP1 and SPA interact with HY5 and both are required for proteasomal degradation of HY5 in dark‐grown seedlings (Ang et al ., ; Osterlund et al ., ; Saijo et al ., ; Zhu et al ., ; Hoecker, ). In Physcomitrella, COP1 and SPA form a complex as well that binds HY5 through COP1 – yet, binding of HY5 to the COP1/SPA complex might not require SPAs (Artz et al .). The HY5 protein is stabilized when dark‐adapted Physcomitrella plants are exposed to light but degradation of HY5 in the dark does not depend on SPAs in Physcomitrella (Artz et al .).…”

“…In Physcomitrella, COP1 and SPA form a complex as well that binds HY5 through COP1 – yet, binding of HY5 to the COP1/SPA complex might not require SPAs (Artz et al .). The HY5 protein is stabilized when dark‐adapted Physcomitrella plants are exposed to light but degradation of HY5 in the dark does not depend on SPAs in Physcomitrella (Artz et al .). Since HY5 binds to COP1, it appears likely that COP1 is involved in HY5 degradation in dark‐adapted Physcomitrella plants; however, experimental testing of this hypothesis is required.…”

“…In Physcomitrella, the developmental programmes in the dark and light, skotomorphogenesis and photomorphogenesis, are much less well defined than in seed plants. Yet, Physcomitrella gametophores grown in the dark show an etiolation response and stem growth is enhanced compared to light‐grown gametophores, while leaflets remain small and underdeveloped in the dark (Artz et al .). This etiolation response still works in the spaAB double mutant, suggesting that the lack of SPAs is not sufficient to fully trigger photomorphogenesis in Physcomitrella, which is in stark contrast to Arabidopsis (Hoecker, ).…”