Reconsidering the nature and mode of action of metabolite retrograde signals from the chloroplast

Abstract

Plant organelles produce retrograde signals to alter nuclear gene expression in order to coordinate their biogenesis, maintain homeostasis, or optimize their performance under adverse conditions. Many signals of different chemical nature have been described in the past decades, including chlorophyll intermediates, reactive oxygen species (ROS), and adenosine derivatives. While the effects of retrograde signaling on gene expression are well understood, the initiation and transport of the signals and their mode of action have either not been resolved, or are a matter of speculation. Moreover, retrograde signaling should be considered as part of a broader cellular network, instead of as separate pathways, required to adjust to changing physiologically relevant conditions. Here we summarize current plastid retrograde signaling models in plants, with a focus on new signaling pathways, SAL1-PAP, methylerythritol cyclodiphosphate (MEcPP), and β-cyclocitral (β-CC), and outline missing links or future areas of research that we believe need to be addressed to have a better understanding of plant intracellular signaling networks.

Light-Induced Acclimation of the Arabidopsis chlorina1 Mutant to Singlet Oxygen

“…No cross-acclimation to other ROS generators could be observed; however, it was discovered that high light induces acclimation to 1 O 2 stress, demonstrating an overlap between 1 O 2 responses and high-light exposure (Ledford et al, 2007). Even if several plastid and cytosolic proteins or signaling molecules are involved in chloroplast-to-nucleus retrograde signaling (Estavillo et al, 2011(Estavillo et al, , 2012Inaba et al, 2011;Leister, 2012), the molecules transmitting the plastid 1 O 2 signal out of the chloroplast are still largely unknown. However, one of them seems to have been recently identified in Arabidopsis: b-Cyclocitral, a volatile derivative of b-carotene that accumulates in Arabidopsis leaves under high-light stress, was found to induce changes in the expression of a large set of 1 O 2 -specific genes (Ramel et al, 2012a).…”

12-oxo-phytodienoic acid interaction with cyclophilin CYP20-3 is a benchmark for understanding retrograde signaling in plants

“…A number of such signals acting through diverse pathways have been proposed, such as Mg protoporphyrin IX, haem, singlet oxygen, 3′-phosphoadenosine 5′-phosphate (PAP), methylerythritol cyclodiphosphate, or plant homeodomain-type transcription factors with transmembrane domain, which are normally present in plastid envelopes and upon stress migrate to the nucleus (reviewed in ref. 15). So, why is addition of OPDA on this list remarkable?…”

“…Although this seems to make sense for a receptor of a hormone synthesized in the chloroplast (13), it involves the inconvenience of transmitting the signal across the plastid envelope to the nucleus, the retrograde signaling (14,15). Retrograde signaling is essential to enable the cell to react to signals perceived in the plastids, such as high light, drought, or reactive oxygen species and readjust homeostasis (15).…”

“…Although this seems to make sense for a receptor of a hormone synthesized in the chloroplast (13), it involves the inconvenience of transmitting the signal across the plastid envelope to the nucleus, the retrograde signaling (14,15). Retrograde signaling is essential to enable the cell to react to signals perceived in the plastids, such as high light, drought, or reactive oxygen species and readjust homeostasis (15). A number of such signals acting through diverse pathways have been proposed, such as Mg protoporphyrin IX, haem, singlet oxygen, 3′-phosphoadenosine 5′-phosphate (PAP), methylerythritol cyclodiphosphate, or plant homeodomain-type transcription factors with transmembrane domain, which are normally present in plastid envelopes and upon stress migrate to the nucleus (reviewed in ref.…”

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

“…A wealth of literature evidence supports the concept that chloroplast redox processes play a pivotal role in the orchestration of gene expression, and also in post-transcriptional regulation including translation, protein folding and protein degradation [9,11,[72][73][74][75]. The thylakoid electron transport system is a key sensor of the environment, producing a range of redox signals that trigger both acclimation and immunity responses.…”