Chloroplast-associated molecular patterns as concept for fine-tuned operational retrograde signalling

Abstract

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'.

Local and Systemic Changes in Photosynthetic Parameters and Antioxidant Activity in Cucumber Challenged with Pseudomonas syringae pv lachrymans

“…Moreover, chloroplasts are involved in the biosynthesis of salicylic (SA), abscisic and jasmonic acids, stress hormones tightly linked with defense against pathogens at the whole plant level [ 24 ]. Finally, considering their internal redox environment, chloroplasts significantly contribute to cellular redox status and generate multiple ROS/redox defensive signals regulating the intracellular and intercellular immune responses [ 25 , 26 , 27 , 28 ]. For example, changes in cellular redox status control the conformation of NPR1 (NON-EXPRESSOR OF PATHOGENESIS-RELATED GENE 1), a master protein regulator of SA-dependent defense genes which are relevant to both local defense against biotrophic/hemibiotrophic pathogens and systemic acquired resistance [ 29 ].…”

Supraoptimal Iron Nutrition of Brassica napus Plants Suppresses the Iron Uptake of Chloroplasts by Down-Regulating Chloroplast Ferric Chelate Reductase

“…Vaccinium corymbosum LON1 protease was reported to play a role in maintaining the Fe homeostasis in plastids increasing plastidial Fe content under insufficient Fe nutrition ( Zhong et al, 2019 ). ROS are important retrograde signalling compounds that are suggested to be involved in monitoring the chloroplast Fe status and involved in Fe status monitoring processes ( Vigani et al, 2013 ; Balparda et al, 2020 ; Unal et al, 2020 ). Nitric oxide (NO) has also been reported to regulate Fe homeostasis in chloroplasts ( Arnaud et al, 2006 ; Touraine et al, 2012 ).…”

A new take on organelle‐mediated stress sensing in plants

“…For example, plastid signaling involves carotenoid‐derived β‐cyclocitral and dihydroactiniolide as a consequence of increased singlet oxygen (Ramel et al ., 2012), derivatives of the isoprenoid precursor methylerythritol cyclodiphosphate (MEcPP) to influence salicylic acid (SA) and jasmonate pathways (Xiao et al ., 2012), or 3′‐phosphoadenosine 5′‐phosphate, a metabolite affecting 5′‐3′ exoribonuclease activity within the nucleus (Estavillo et al ., 2011). The spectrum of intermediates identified as components of retrograde signaling point to a vital function of plastid envelope transport systems in the evolution of this intracellular communication (Unal et al ., 2020). What remains unclear is how these transport systems partition to specialized plastid types.…”