Learning the Languages of the Chloroplast: Retrograde Signaling and Beyond

Abstract

The chloroplast can act as an environmental sensor, communicating with the cell during biogenesis and operation to change the expression of thousands of proteins. This process, termed retrograde signaling, regulates expression in response to developmental cues and stresses that affect photosynthesis and yield. Recent advances have identified many signals and pathways-including carotenoid derivatives, isoprenes, phosphoadenosines, tetrapyrroles, and heme, together with reactive oxygen species and proteins-that build a communication network to regulate gene expression, RNA turnover, and splicing. However, retrograde signaling pathways have been viewed largely as a means of bilateral communication between organelles and nuclei, ignoring their potential to interact with hormone signaling and the cell as a whole to regulate plant form and function. Here, we discuss new findings on the processes by which organelle communication is initiated, transmitted, and perceived, not only to regulate chloroplastic processes but also to intersect with cellular signaling and alter physiological responses.

Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast

“…The regulation of translation in the context of retrograde signaling awaits scrutiny, but both the MAPK pathway (Bollig et al, 2003) and redox/ROS (Moore et al, 2016) likely affect the activity of components and, therefore, the different steps of initiation, elongation, and termination. Several regulatory factors have been identified that act downstream of chloroplastreleased ROS, as summarized recently (Chan et al, 2016). ROS appear to trigger the interaction of the regulatory protein RADICAL-INDUCED CELL DEATH1 with the transcription factor RAP2.4a, which in turn up-regulates the expression of chloroplast antioxidant genes such as 2-CYSTEINE PEROXIREDOXIN (Hiltscher et al, 2014).…”

A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments

“…Plants also have a robust repair system that replaces damaged PSII reaction center proteins (12,13), and a set of proteins facilitate this longer term repair process (14)(15)(16). Other long-term light responses include regulating expression of photosynthesisrelated genes (17)(18)(19)(20) and modulating the abundance of key photosynthetic proteins as well as the stoichiometry of photosystems to optimize light energy capture and conversion (21,22).…”

Phosphorylation of GENOMES UNCOUPLED 4 Alters Stimulation of Mg Chelatase Activity in Angiosperms

“…Five of the six known gun mutants encode mutant proteins involved in TBS (Susek et al, 1993;Mochizuki et al, 2001;Larkin et al, 2003;Koussevitzky et al, 2007;Woodson et al, 2011) so that tetrapyrrole metabolites and/or enzymes of the pathway were proposed to play a role in communicating the plastid status toward the nucleus for modulation of the nuclear gene expression (Woodson et al, 2011;Jarvis and López-Juez, 2013;Chan et al, 2016). Particularly for GUN4, a role in singlet oxygen specific signaling is discussed (Brzezowski et al, 2014;Tarahi Tabrizi et al, 2016).…”

“…Particularly for GUN4, a role in singlet oxygen specific signaling is discussed (Brzezowski et al, 2014;Tarahi Tabrizi et al, 2016). However, apart from the gun-mediated retrograde signaling, various stimuli and signals, which originate from different plastid localized processes like redox control during photosynthesis, plastid gene expression, and tetrapyrrole or carotenoid biosynthesis, were identified (Chan et al, 2016;Singh et al, 2015;Leister, 2016).…”