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'.

Keywords: hormone; oxylipin; photosynthesis; reactive oxygen species; redox regulation; retrograde signalling.

Figure 1.

Principal mechanisms of retrograde signal transmission acting on the chloroplast-associated molecular pattern (ChAMP). This scheme shows four possible pathways of retrograde signaling, namely (i) diffusion through the membrane boundary, (ii) export by specific carriers (uni-, sym-, antiporters) through the inner envelope and through porins through the outer envelope membrane (cf. [2]), (iii) specific import as will be discussed for 3′phosphoadenosine 5′-phosphate below, and (iv) relay-type systems, where the signal from the chloroplast does not leave the chloroplast but rather is converted or transmitted at the envelope to another entity, as has been described for the release of the plant homeodomain transcription factor PTM from the outer envelope in response to chloroplast signals [3]. All these chloroplast-dependent retrograde processes define the ChAMP, which in turn determines the downstream adjustment of, e.g., transcription, RNA fate, translation and protein fate. (Online version in colour.)

Figure 2.

H₂O₂ in the peroxisome. Metabolite transport at the plastid envelope. This scheme distinguishes transporters that transport assimilation products at high rates and with high capacity (bulk metabolite transporters). Other transporters function with lower rate and capacity and play a more specific role in metabolism or signalling, e.g. in hormone, redox signalling and sulfur metabolism. The third category of specific transporters in the context of retrograde signalling of ROS or ROS-derived molecules (distinctive signal transporters) is least understood. Transporter proteins still need to be identified. See text for details. The MEX transporter carries maltose [10]. The first six bulk metabolite transporters are involved in adjustment of extrachloroplast phosphorylation potential (ATP), reduction potential (NAD(P)H) or production of ROS. Glycolate export as part of the photorespiratory cycle releases stoichiometric amounts of H₂O in the peroxisomes. 2-OG, 2-oxoglutarate; ABA, abscisic acid; ADP, adenosine diphosphate; AMP, adenosine monophosphate; ATP, adenosine triphosphate; AP, aquaporins; CLT, chloroquinone-like transporters; DCT, dicarboxylate transporter; DHA, dehydroascorbate; DHAP, dihydroxyacetonephosphate; FAX, fatty acid exporter; FRY1, phosphatase fiery 1; GG1, glycolate/glycerate translocator 1; Glu, glutamate; GPT, glucose-6-phosphate/phosphate translocator; G6P, glucose-6-phosphate; GSH, glutathione; H₂O₂, hydrogen peroxide; JA, jasmonic acid; MEcPP, methylerythritol cyclodiphosphate; MEX, maltose transporter; OAA, oxaloacetate; OAS, O-acetylserine; OPDA, oxophytodienoic acid; OMT, oxoglutarate–malate transporter; PAP, phosphoadenosine phosphate; PAPS, 3′-phosphoadenosine 5′-phosphosulfate; PEP, phosphoenolypyruvate; PHT, H⁺/phosphate co-transporter; Pi, inorganic phosphate; PPT, phosphoenolpyruvate/phosphate translocator; PRAT, amino acid transporter; TPT, triosephosphate/phosphate translocator. (Online version in colour.)

Figure 3.

Schematics of signalling pathways related to ¹O₂-mediated retrograde signalling and triggered by over-reduced PSII. The model summarizes signalling pathways involving carotenoid-derived retrograde signals such as β-cyclocitral and dihydroactiniolide, and addresses regulation of ¹O₂-responsive genes via EXECUTER proteins, EX1 and EX2, respectively. The pathways are described in detail in the text. Dashed lines indicate signalling connections that are suggested to exist based on circumstantial evidence like transcriptome data. Questions marks denote unknown mechanisms. ANAC102, Arabidopsis NAC domain-containing transcription factor; EDS1, enhanced disease susceptibility1; EX, EXECUTER; GST, glutathione-S-transferase; ICS1, isochorismate synthase 1; MBS, methylene blue sensitive; NPR1, non-expressor of pathogenesis-related protein; OEC, oxygen evolving complex; PSII, photosystem II; RES, reactive electrophilic species; SA, salicylic acid; SCL14, scarecrow-like 14. (Online version in colour.)

Figure 4.

Schematic of signalling pathways related to ROS-mediated retrograde signalling and triggered by over-reduced PSI. This scheme describes signal pathways that involve the MEcPP and PAP-SAL1 pathways. The pathways are described in detail in the text. Questions marks denote unknown mechanisms. Solid lines describe established pathways and dependencies, while dashed lines indicate postulated or unexplored signalling pathways. 3PGA: 3-phosphoglycerate; CaM, calmodulin; CAMTA3, calmodulin-binding transcriptional activator 3; G3P, glyceraldehyde-3-phosphate; GSR, general stress response genes; HL, high light; HLP, hydroperoxide lyase; MEP, methyl-d-erythritol 4-phosphate; MEcPP, methylerythritol cyclodiphosphate; PAP, phosphoadenosine phosphate; PEP, phosphoenolypyruvate; Pi, inorganic phosphate; PRANG, plastid redox-associated nuclear genes like Zat10 and APX2; PSI/II, photosystem I/II; ROS, reactive oxygen species; RuBP, ribulose-1,5-bisphosphate; SA, salicylic acid; SAL1, inositol polyphosphate 1-phosphatase; XRN, nuclear 5′–3′exoribonuclease. (Online version in colour.)

Figure 5.

Interference between signalling pathways and application of the control theory. (a) Depiction of the control strength exerted by signalling pathway 1 on the response of the system. The normalized slope of the response-versus-activity plot (δR/δA) defines the control coefficient c, which regularly ranges between c = 0 (no control) and c = 1 (full control). The summation theorem states that the sum of c-values of all involved components cannot exceed 1. A theoretical example could be the MEcPP pathway versus high light acclimation. Reducing the activity of the pathway 1 will not affect the response until more than 50% of the pathway activity is lost. However, impeding pathway 2 will increase the control coefficient of pathway 1. (b) Venn diagrams of overlapping transcriptomic changes (upregulation and downregulation) for multiple retrograde signalling pathways. Microarray-based expression data were taken from [,,–105]. Transcript amounts of mutants or treatments were compared with wild-type and filtered for fold change ≥2, ≤−2 and p ≤ 0.05. The filtered datasets were compared for possible overlaps using the online tool DRAW VENN DIAGRAM (bioinformatics.psb.ugent.be/webtools/Venn/).