The Plasmodesmal Localization Signal of TMV MP Is Recognized by Plant Synaptotagmin SYTA

ABSTRACT Plant viruses cross the barrier of the plant cell wall by moving through intercellular channels, termed plasmodesmata, to invade their hosts. They accomplish this by encoding movement proteins (MPs), which act to alter plasmodesmal gating. How MPs target to plasmodesmata is not well underst...

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Autores principales: Cheng Yuan, Sondra G. Lazarowitz, Vitaly Citovsky
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:2cddeb59be0b4b338c6e12b228b4b5722021-11-15T16:00:14ZThe Plasmodesmal Localization Signal of TMV MP Is Recognized by Plant Synaptotagmin SYTA10.1128/mBio.01314-182150-7511https://doaj.org/article/2cddeb59be0b4b338c6e12b228b4b5722018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01314-18https://doaj.org/toc/2150-7511ABSTRACT Plant viruses cross the barrier of the plant cell wall by moving through intercellular channels, termed plasmodesmata, to invade their hosts. They accomplish this by encoding movement proteins (MPs), which act to alter plasmodesmal gating. How MPs target to plasmodesmata is not well understood. Our recent characterization of the first plasmodesmal localization signal (PLS) identified in a viral MP, namely, the MP encoded by the Tobamovirus Tobacco mosaic virus (TMV), now provides the opportunity to identify host proteins that recognize this PLS and may be important for its plasmodesmal targeting. One such candidate protein is Arabidopsis synaptotagmin A (SYTA), which is required to form endoplasmic reticulum (ER)-plasma membrane contact sites and regulates the MP-mediated trafficking of begomoviruses, tobamoviruses, and potyviruses. In particular, SYTA interacts with, and regulates the cell-to-cell transport of, both TMV MP and the MP encoded by the Tobamovirus Turnip vein clearing virus (TVCV). Using in planta bimolecular fluorescence complementation (BiFC) and yeast two-hybrid assays, we show here that the TMV PLS interacted with SYTA. This PLS sequence was both necessary and sufficient for interaction with SYTA, and the plasmodesmal targeting activity of the TMV PLS was substantially reduced in an Arabidopsis syta knockdown line. Our findings show that SYTA is one host factor that can recognize the TMV PLS and suggest that this interaction may stabilize the association of TMV MP with plasmodesmata. IMPORTANCE Plant viruses use their movement proteins (MPs) to move through host intercellular connections, plasmodesmata. Perhaps one of the most intriguing, yet least studied, aspects of this transport is the MP signal sequences and their host recognition factors. Recently, we have described the plasmodesmal localization signal (PLS) of the Tobacco mosaic virus (TMV) MP. Here, we identified the Arabidopsis synaptotagmin A (SYTA) as a host factor that recognizes TMV MP PLS and promotes its association with the plasmodesmal membrane. The significance of these findings is two-fold: (i) we identified the TMV MP association with the cell membrane at plasmodesmata as an important PLS-dependent step in plasmodesmal targeting, and (ii) we identified the plant SYTA protein that specifically recognizes PLS as a host factor involved in this step.Cheng YuanSondra G. LazarowitzVitaly CitovskyAmerican Society for Microbiologyarticleplasmodesmatamovement proteintargetingTobacco mosaic virusMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution DOAJ
collection DOAJ
language EN
topic plasmodesmata
movement protein
targeting
Tobacco mosaic virus
Microbiology
QR1-502
spellingShingle plasmodesmata
movement protein
targeting
Tobacco mosaic virus
Microbiology
QR1-502
Cheng Yuan
Sondra G. Lazarowitz
Vitaly Citovsky
The Plasmodesmal Localization Signal of TMV MP Is Recognized by Plant Synaptotagmin SYTA
description ABSTRACT Plant viruses cross the barrier of the plant cell wall by moving through intercellular channels, termed plasmodesmata, to invade their hosts. They accomplish this by encoding movement proteins (MPs), which act to alter plasmodesmal gating. How MPs target to plasmodesmata is not well understood. Our recent characterization of the first plasmodesmal localization signal (PLS) identified in a viral MP, namely, the MP encoded by the Tobamovirus Tobacco mosaic virus (TMV), now provides the opportunity to identify host proteins that recognize this PLS and may be important for its plasmodesmal targeting. One such candidate protein is Arabidopsis synaptotagmin A (SYTA), which is required to form endoplasmic reticulum (ER)-plasma membrane contact sites and regulates the MP-mediated trafficking of begomoviruses, tobamoviruses, and potyviruses. In particular, SYTA interacts with, and regulates the cell-to-cell transport of, both TMV MP and the MP encoded by the Tobamovirus Turnip vein clearing virus (TVCV). Using in planta bimolecular fluorescence complementation (BiFC) and yeast two-hybrid assays, we show here that the TMV PLS interacted with SYTA. This PLS sequence was both necessary and sufficient for interaction with SYTA, and the plasmodesmal targeting activity of the TMV PLS was substantially reduced in an Arabidopsis syta knockdown line. Our findings show that SYTA is one host factor that can recognize the TMV PLS and suggest that this interaction may stabilize the association of TMV MP with plasmodesmata. IMPORTANCE Plant viruses use their movement proteins (MPs) to move through host intercellular connections, plasmodesmata. Perhaps one of the most intriguing, yet least studied, aspects of this transport is the MP signal sequences and their host recognition factors. Recently, we have described the plasmodesmal localization signal (PLS) of the Tobacco mosaic virus (TMV) MP. Here, we identified the Arabidopsis synaptotagmin A (SYTA) as a host factor that recognizes TMV MP PLS and promotes its association with the plasmodesmal membrane. The significance of these findings is two-fold: (i) we identified the TMV MP association with the cell membrane at plasmodesmata as an important PLS-dependent step in plasmodesmal targeting, and (ii) we identified the plant SYTA protein that specifically recognizes PLS as a host factor involved in this step.
format article
author Cheng Yuan
Sondra G. Lazarowitz
Vitaly Citovsky
author_facet Cheng Yuan
Sondra G. Lazarowitz
Vitaly Citovsky
author_sort Cheng Yuan
title The Plasmodesmal Localization Signal of TMV MP Is Recognized by Plant Synaptotagmin SYTA
title_short The Plasmodesmal Localization Signal of TMV MP Is Recognized by Plant Synaptotagmin SYTA
title_full The Plasmodesmal Localization Signal of TMV MP Is Recognized by Plant Synaptotagmin SYTA
title_fullStr The Plasmodesmal Localization Signal of TMV MP Is Recognized by Plant Synaptotagmin SYTA
title_full_unstemmed The Plasmodesmal Localization Signal of TMV MP Is Recognized by Plant Synaptotagmin SYTA
title_sort plasmodesmal localization signal of tmv mp is recognized by plant synaptotagmin syta
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/2cddeb59be0b4b338c6e12b228b4b572
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