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Spatial chloroplast-to-nucleus signalling involving plastid-nuclear complexes and stromules.

ABSTRACT: Communication between chloroplasts and the nucleus in response to various environmental cues may be mediated by various small molecules. Signalling specificity could be enhanced if the physical contact between these organelles facilitates direct transfer and prevents interference from other subcellular sources of the same molecules. Plant cells have plastid-nuclear complexes, which provide close physical contact between these organelles. Plastid-nuclear complexes have been proposed to facilitate transfer of photosynthesis-derived H2O2 to the nucleus in high light. Stromules (stroma filled tubular plastid extensions) may provide an additional conduit for transfer of a wider range of signalling molecules, including proteins. However, plastid-nuclear complexes and stromules have been hitherto treated as distinct phenomena. We suggest that plastid-nuclear complexes and stromules work in a coordinated manner so that, according to environmental conditions or developmental state, the two modes of connection contribute to varying extents. We hypothesize that this association is dynamic and that there may be a link between plastid-nuclear complexes and the development of stromules. Furthermore, the changes in contact could alter signalling specificity by allowing an extended or different range of signalling molecules to be delivered to the nucleus. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.

SUBMITTER: Mullineaux PM

PROVIDER: S-EPMC7209948 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Spatial chloroplast-to-nucleus signalling involving plastid-nuclear complexes and stromules.

Mullineaux Philip M PM Exposito-Rodriguez Marino M Laissue Pierre Philippe PP Smirnoff Nicholas N Park Eunsook E

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20200504 1801

Communication between chloroplasts and the nucleus in response to various environmental cues may be mediated by various small molecules. Signalling specificity could be enhanced if the physical contact between these organelles facilitates direct transfer and prevents interference from other subcellular sources of the same molecules. Plant cells have plastid-nuclear complexes, which provide close physical contact between these organelles. Plastid-nuclear complexes have been proposed to facilitate ...[more]

PMID: 32362250

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Project description:Plastids send "retrograde" signals to the nucleus to deliver information regarding their physiological status. One open question concerning this signal transfer is how the signal bridges the cytoplasm. Based on individual reports of plastid derived tubular membrane extensions connecting to nuclei, these so-called stromules have been suggested to function as communication routes between plastids and nuclei in response to biotic stress. However, based on the data currently available it is unclear whether interactions between stromules and nuclei are truly intentional or observed as a result of an inflated stromule frequency throughout the cell, and are thus a random event. The source of this uncertainty stems from missing information regarding the relative distribution of all plastids and stromules within a given cell. A comprehensive analysis of the upper epidermis of Arabidopsis thaliana rosette leaves was performed via a combination of still images and time-lapse movies of stromule formation in the context of the whole cell. This analysis could definitively confirm that stromule formation is not evenly distributed. Stromules are significantly more frequent within 8 ?m of the nucleus, and approximately 90% of said stromules formed facing the nucleus. Time-lapse movies revealed that this enrichment of stromules is achieved via a 10-fold higher frequency of stromule initiation events within this 8 ?m zone compared to the cell periphery. Following the movement of plastids and nuclei it became evident that movement and formation of stromules is correlated to nucleus movement. Observations suggest that stromules "connecting" to the nucleus are not necessarily the result of plastids sensing the nucleus and reaching out toward it, but are rather pulled out of the surface of nucleus associated plastids during opposing movement of these two organelles. This finding does not exclude the possibility that stromules could be transferring signals to the nucleus. However, this work provides support for an alternative hypothesis to explain stromule-nuclear interactions, suggesting that the main purpose of nucleus associated stromules may be to ensure a certain number of plastids maintain contact with the constantly moving nucleus.

Project description:Plastids in the viridiplantae sporadically form thin tubules called stromules that increase the interactive surface between the plastid and the surrounding cytoplasm. Several recent publications that report observations of certain proteins localizing to the extensions have then used the observations to suggest stromule-specific functions. The mechanisms by which specific localizations on these transient and sporadically formed extensions might occur remain unclear. Previous studies have yet to address the spatiotemporal relationship between a particular protein localization pattern and its distribution on an extended stromules and/or the plastid body. Here, we have used discrete protein patches found in several transgenic plants as fiducial markers to investigate this relationship. While we consider the inner plastid envelope-membrane localized protein patches of the GLUCOSE 6-PHOSPHATE/PHOSPHATE TRANSLOCATOR1 and the TRIOSE-PHOSPHATE/ PHOSPHATE TRANSLOCATOR 1 as artifacts of fluorescent fusion protein over-expression, stromule formation is not compromised in the respective stable transgenic lines that maintain normal growth and development. Our analysis of chloroplasts in the transgenic lines in the Arabidopsis Columbia background, and in the arc6 mutant, under stromule-inducing conditions shows that the possibility of finding a particular protein-enriched domain on an extended stromule or on a region of the main plastid body is stochastic. Our observations provide insights on the behavior of chloroplasts, the relationship between stromules and the plastid-body and strongly challenge claims of stromule-specific functions based solely upon protein localization to plastid extensions.One sentence summaryObservations of the spatiotemporal relationship between plastid envelope localized fluorescent protein fusions of two sugar-phosphate transporters and stromules suggest a stochastic rather than specific localization pattern that questions the idea of independent functions for stromules.

Project description:The initiation of chloroplast development in the light is dependent on nuclear encoded components. The nuclear genes encoding key components in the photosynthetic machinery are regulated by signals originating in the plastids. These plastid signals play an essential role in the regulation of photosynthesis associated nuclear genes (PhANGs) when proplastids develop into chloroplasts. One of the plastid signals is linked to the tetrapyrrole biosynthesis and accumulation of the intermediates the Mg-ProtoIX and its methyl ester Mg-ProtoIX-ME. Phytochrome-Associated Protein Phosphatase 5 (PAPP5) was isolated in a previous study as a putative Mg-ProtoIX interacting protein. In order to elucidate if there is a biological link between PAPP5 and the tetrapyrrole mediated signal we generated double mutants between the Arabidopsis papp5 and the crd mutants. The crd mutant over-accumulates Mg-ProtoIX and Mg-ProtoIX-ME and the tetrapyrrole accumulation triggers retrograde signalling. The crd mutant exhibits repression of PhANG expression, altered chloroplast morphology and a pale phenotype. However, in the papp5crd double mutant, the crd phenotype is restored and papp5crd accumulated wild type levels of chlorophyll, developed proper chloroplasts and showed normal induction of PhANG expression in response to light. Tetrapyrrole feeding experiments showed that PAPP5 is required to respond correctly to accumulation of tetrapyrroles in the cell and that PAPP5 is most likely a component in the plastid signalling pathway down stream of the tetrapyrrole Mg-ProtoIX/Mg-ProtoIX-ME. Inhibition of phosphatase activity phenocopied the papp5crd phenotype in the crd single mutant demonstrating that PAPP5 phosphatase activity is essential to mediate the retrograde signal and to suppress PhANG expression in the crd mutant. Thus, our results suggest that PAPP5 receives an inbalance in the tetrapyrrole biosynthesis through the accumulation of Mg-ProtoIX and acts as a negative regulator of PhANG expression during chloroplast biogenesis and development.

Dataset Information

Spatial chloroplast-to-nucleus signalling involving plastid-nuclear complexes and stromules.

Publications

Spatial chloroplast-to-nucleus signalling involving plastid-nuclear complexes and stromules.

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