Dataset Information

Plastid Envelope-Localized Proteins Exhibit a Stochastic Spatiotemporal Relationship to Stromules.

ABSTRACT: 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 summary:Observations 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.

SUBMITTER: Delfosse K

PROVIDER: S-EPMC5995270 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Plastid Envelope-Localized Proteins Exhibit a Stochastic Spatiotemporal Relationship to Stromules.

Delfosse Kathleen K Wozny Michael R MR Barton Kiah A KA Mathur Neeta N Griffiths Nigel N Mathur Jaideep J

Frontiers in plant science 20180604

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 a ...[more]

PMID: 29915611

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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:Tail-anchored (TA) proteins are a distinct class of membrane proteins that are sorted post-translationally to various organelles and function in a number of important cellular processes, including redox reactions, vesicular trafficking and protein translocation. While the molecular targeting signals and pathways responsible for sorting TA proteins to their correct intracellular destinations in yeasts and mammals have begun to be characterized, relatively little is known about TA protein biogenesis in plant cells, especially for those sorted to the plastid outer envelope.Here we investigated the biogenesis of three plastid TA proteins, including the 33-kDa and 34-kDa GTPases of the translocon at the outer envelope of chloroplasts (Toc33 and Toc34) and a novel 9-kDa protein of unknown function that we define here as an outer envelope TA protein (OEP9). Using a combination of in vivo and in vitro assays we show that OEP9 utilizes a different sorting pathway than that used by Toc33 and Toc34. For instance, while all three TA proteins interact with the cytosolic OEP chaperone/receptor, AKR2A, the plastid targeting information within OEP9 is distinct from that within Toc33 and Toc34. Toc33 and Toc34 also appear to differ from OEP9 in that their insertion is dependent on themselves and the unique lipid composition of the plastid outer envelope. By contrast, the insertion of OEP9 into the plastid outer envelope occurs in a proteinaceous-dependent, but Toc33/34-independent manner and membrane lipids appear to serve primarily to facilitate normal thermodynamic integration of this TA protein.Collectively, the results provide evidence in support of at least two sorting pathways for plastid TA outer envelope proteins and shed light on not only the complex diversity of pathways involved in the targeting and insertion of proteins into plastids, but also the molecular mechanisms that underlie the delivery of TA proteins to their proper intracellular locations in general.

Dataset Information

Plastid Envelope-Localized Proteins Exhibit a Stochastic Spatiotemporal Relationship to Stromules.

Publications

Plastid Envelope-Localized Proteins Exhibit a Stochastic Spatiotemporal Relationship to Stromules.

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