Chloroplasts compose about one-quarter of the mesophyll cell volume and contain about 60% of the cell protein. Photosynthetic carbon assimilation is the dominating metabolism in illuminated leaves. To optimize the resource expenditure in these costly organelles and to control and adjust chloroplast metabolism, an intensive transfer of information between nucleus–cytoplasm and chloroplasts occurs in both directions as anterograde and retrograde signalling. Recent research identified multiple retrograde pathways that use metabolite transfer and include reaction products of lipids and carotenoids with reactive oxygen species (ROS). Other pathways use metabolites of carbon, sulfur and nitrogen metabolism, low molecular weight antioxidants and hormone precursors to carry information between the cell compartments. This review focuses on redox- and ROS-related retrograde signalling pathways. In analogy to the microbe-associated molecular pattern, we propose the term ‘chloroplast-associated molecular pattern' which connects chloroplast performance to extrachloroplast processes such as nuclear gene transcription, posttranscriptional processing, including translation, and RNA and protein fate. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles'.

During land plant evolution, the number of genes encoding for components of the thiol redox regulatory network and the generator systems of reactive oxygen species (ROS) expanded, tentatively indicating a role in tailored environmental acclimatization. This hypothesis has been validated experimentally and theoretically during the last decades. Recent developments of dynamic roGFP-based in vivo sensors for H₂O₂ and the redox potential of the glutathione pool paved the way for dissecting the kinetics changes in these decisive parameters in response to environmental stressors. The versatile cellular redox sensory and response regulatory system monitors alterations in redox metabolism and controls the activity of redox target proteins, and thereby affects most, if not all, cellular processes ranging from transcription to translation and metabolism. This review exemplarily describes the role of the redox- and ROS-dependent regulatory network in realising the proper response to diverse environmental stresses. The selected case studies concern different environmental challenges, namely excess excitation energy, the heavy metal cadmium and the metalloid arsenic, nitrogen, or phosphate shortage as examples for nutrient deficiency, wounding, and nematode infestation. Each challenge affects the redox regulatory and ROS network, but the present state of knowledge also pinpoints to pressing open questions concerning the translation of redox regulation to environmental acclimatization.