Phytochrome and retrograde signalling pathways converge to antagonistically regulate a light-induced transcriptional network.

Guiomar Martín,Pablo Leivar,James M Tepperman,Peter H Quail,Elena Monte,Dolores Ludevid

doi:10.1038/ncomms11431

Abstract

Plastid-to-nucleus retrograde signals emitted by dysfunctional chloroplasts impact photomorphogenic development, but the molecular link between retrograde- and photosensory-receptor signalling has remained unclear. Here, we show that the phytochrome and retrograde signalling (RS) pathways converge antagonistically to regulate the expression of the nuclear-encoded transcription factor GLK1, a key regulator of a light-induced transcriptional network central to photomorphogenesis. GLK1 gene transcription is directly repressed by PHYTOCHROME-INTERACTING FACTOR (PIF)-class bHLH transcription factors in darkness, but light-activated phytochrome reverses this activity, thereby inducing expression. Conversely, we show that retrograde signals repress this induction by a mechanism independent of PIF mediation. Collectively, our data indicate that light at moderate levels acts through the plant's nuclear-localized sensory-photoreceptor system to induce appropriate photomorphogenic development, but at excessive levels, sensed through the separate plastid-localized RS system, acts to suppress such development, thus providing a mechanism for protection against photo-oxidative damage by minimizing the tissue exposure to deleterious radiation.

Highlights

Plastid-to-nucleus retrograde signals emitted by dysfunctional chloroplasts impact photomorphogenic development, but the molecular link between retrograde- and photosensory-receptor signalling has remained unclear
While many of the components of the phytochrome pathway (PIFs) and the retrograde signalling (RS) pathway (GUN1, GLK1) examined in the present work have been reported in a number of publications[9,10,12,16,17,18], here we present data that connect the two in a comprehensive fashion, identifying the molecular framework that integrates the two pathways at a central node at the apex of a transcriptional network that regulates early seedling photomorphogenic development
We show that the phytochrome and the GUN1 RS pathways act antagonistically to control the expression of GLK1, a key transcriptional regulator of photomorphogenesis directly repressed by the PHYTOCHROME-INTERACTING FACTOR (PIF) in the dark

Summary

Introduction

Plastid-to-nucleus retrograde signals emitted by dysfunctional chloroplasts impact photomorphogenic development, but the molecular link between retrograde- and photosensory-receptor signalling has remained unclear. Our data indicate that light at moderate levels acts through the plant’s nuclear-localized sensory-photoreceptor system to induce appropriate photomorphogenic development, but at excessive levels, sensed through the separate plastid-localized RS system, acts to suppress such development, providing a mechanism for protection against photo-oxidative damage by minimizing the tissue exposure to deleterious radiation. Indicative of the central role of the PIFs in this process, a dark-grown quadruple pifq mutant, deficient in four PIFs (PIF1, PIF3, PIF4 and PIF5), largely phenocopies wild-type (WT) seedlings grown in the light at both the morphological and transcriptional levels These mutant seedlings display a constitutively photomorphogenic (cop-like) phenotype, which includes partially developed chloroplasts[10,11]. Whereas light at moderate levels acts through the phytochrome/ PIF sensory-photoreceptor system to induce GLK1 expression and photomorphogenic development, light at excessive levels is sensed by the plastid and represses GLK1 induction and photomorphogenesis through a GUN1-mediated RS mechanism independent of PIF mediation. Our data indicate that RS provides a mechanism for protection against photo-oxidative damage by minimizing the tissue exposure to deleterious radiation

Methods

Results

Conclusion