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      The discovery of plastid-to-nucleus retrograde signaling—a personal perspective

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          Abstract

          DNA and machinery for gene expression have been discovered in chloroplasts during the 1960s. It was soon evident that the chloroplast genome is relatively small, that most genes for chloroplast-localized proteins reside in the nucleus and that chloroplast membranes, ribosomes, and protein complexes are composed of proteins encoded in both the chloroplast and the nuclear genome. This situation has made the existence of mechanisms highly probable that coordinate the gene expression in plastids and nucleus. In the 1970s, the first evidence for plastid signals controlling nuclear gene expression was provided by studies on plastid ribosome deficient mutants with reduced amounts and/or activities of nuclear-encoded chloroplast proteins including the small subunit of Rubisco, ferredoxin NADP+ reductase, and enzymes of the Calvin cycle. This review describes first models of plastid-to-nucleus signaling and their discovery. Today, many plastid signals are known. They do not only balance gene expression in chloroplasts and nucleus during developmental processes but are also generated in response to environmental changes sensed by the organelles.

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          Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants.

          (1)O(2) (singlet oxygen) is a reactive O(2) species produced from triplet excited chlorophylls in the chloroplasts, especially when plants are exposed to excess light energy. Similarly to other active O(2) species, (1)O(2) has a dual effect: It is toxic, causing oxidation of biomolecules, and it can act as a signal molecule that leads to cell death or to acclimation. Carotenoids are considered to be the main (1)O(2) quenchers in chloroplasts, and we show here that light stress induces the oxidation of the carotenoid β-carotene in Arabidopsis plants, leading to the accumulation of different volatile derivatives. One such compound, β-cyclocitral, was found to induce changes in the expression of a large set of genes that have been identified as (1)O(2) responsive genes. In contrast, β-cyclocitral had little effect on the expression of H(2)O(2) gene markers. β-Cyclocitral-induced reprogramming of gene expression was associated with an increased tolerance to photooxidative stress. The results indicate that β-cyclocitral is a stress signal produced in high light that is able to induce defense mechanisms and represents a likely messenger involved in the (1)O(2) signaling pathway in plants.
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            Learning the Languages of the Chloroplast: Retrograde Signaling and Beyond.

            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.
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              Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development.

              Chloroplast development requires coordinate nuclear and chloroplast gene expression. A putative signal from the chloroplast couples the transcription of certain nuclear genes encoding photosynthesis-related proteins with chloroplast function. We have identified at least three Arabidopsis nuclear genes (GUN1, GUN2, and GUN3) necessary for coupling the expression of some nuclear genes to the functional state of the chloroplast. Homozygous recessive gun mutations allow nuclear gene expression in the absence of chloroplast development and furthermore may interfere with the switch from dark-grown to light-grown development. Other reports suggest this intracellular cross-talk also involves mitochondrial interactions. The GUN genes thus define steps in one specific branch of a complex interorganellar regulatory network.
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                Author and article information

                Contributors
                +49 30 2093 49705 , thomas.boerner@rz.hu-berlin.de
                Journal
                Protoplasma
                Protoplasma
                Protoplasma
                Springer Vienna (Vienna )
                0033-183X
                1615-6102
                23 March 2017
                23 March 2017
                2017
                : 254
                : 5
                : 1845-1855
                Affiliations
                ISNI 0000 0001 2248 7639, GRID grid.7468.d, Institute of Biology, Molecular Genetics, , Humboldt University Berlin, ; Rhoda Erdmann Haus, Philippstr 13, 10115 Berlin, Germany
                Author notes

                Handling Editor: Peter Nick

                Author information
                http://orcid.org/0000-0001-9548-3348
                Article
                1104
                10.1007/s00709-017-1104-1
                5610210
                28337540
                db09dd35-43a2-46d2-89f3-d7d6f5376e32
                © The Author(s) 2017

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 13 February 2017
                : 10 March 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: SFB 429
                Award Recipient :
                Categories
                Review Article
                Custom metadata
                © Springer-Verlag GmbH Austria 2017

                Molecular biology
                chloroplast signal,plastid signal,retrograde signaling,chloroplast development,regulation of gene expression

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