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A comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species

BACKGROUND: A major route for cell-to-cell signalling in plants is mediated by cell wall-embedded pores termed plasmodesmata forming the symplasm. Plasmodesmata regulate the plant development and responses to the environment; however, our understanding of what factors or regulatory cues affect their...

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Autores principales: Kirk, Philip, Amsbury, Sam, German, Liam, Gaudioso-Pedraza, Rocio, Benitez-Alfonso, Yoselin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9164936/
https://www.ncbi.nlm.nih.gov/pubmed/35655273
http://dx.doi.org/10.1186/s12915-022-01331-1
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author Kirk, Philip
Amsbury, Sam
German, Liam
Gaudioso-Pedraza, Rocio
Benitez-Alfonso, Yoselin
author_facet Kirk, Philip
Amsbury, Sam
German, Liam
Gaudioso-Pedraza, Rocio
Benitez-Alfonso, Yoselin
author_sort Kirk, Philip
collection PubMed
description BACKGROUND: A major route for cell-to-cell signalling in plants is mediated by cell wall-embedded pores termed plasmodesmata forming the symplasm. Plasmodesmata regulate the plant development and responses to the environment; however, our understanding of what factors or regulatory cues affect their structure and permeability is still limited. In this paper, a meta-analysis was carried out for the identification of conditions affecting plasmodesmata transport and for the in silico prediction of plasmodesmata proteins in species for which the plasmodesmata proteome has not been experimentally determined. RESULTS: Using the information obtained from experimental proteomes, an analysis pipeline (named plasmodesmata in silico proteome 1 or PIP1) was developed to rapidly generate candidate plasmodesmata proteomes for 22 plant species. Using the in silico proteomes to interrogate published transcriptomes, gene interaction networks were identified pointing to conditions likely affecting plasmodesmata transport capacity. High salinity, drought and osmotic stress regulate the expression of clusters enriched in genes encoding plasmodesmata proteins, including those involved in the metabolism of the cell wall polysaccharide callose. Experimental determinations showed restriction in the intercellular transport of the symplasmic reporter GFP and enhanced callose deposition in Arabidopsis roots exposed to 75-mM NaCl and 3% PEG (polyethylene glycol). Using PIP1 and transcriptome meta-analyses, candidate plasmodesmata proteins for the legume Medicago truncatula were generated, leading to the identification of Medtr1g073320, a novel receptor-like protein that localises at plasmodesmata. Expression of Medtr1g073320 affects callose deposition and the root response to infection with the soil-borne bacteria rhizobia in the presence of nitrate. CONCLUSIONS: Our study shows that combining proteomic meta-analysis and transcriptomic data can be a valuable tool for the identification of new proteins and regulatory mechanisms affecting plasmodesmata function. We have created the freely accessible pipeline PIP1 as a resource for the screening of experimental proteomes and for the in silico prediction of PD proteins in diverse plant species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01331-1.
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spelling pubmed-91649362022-06-05 A comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species Kirk, Philip Amsbury, Sam German, Liam Gaudioso-Pedraza, Rocio Benitez-Alfonso, Yoselin BMC Biol Research Article BACKGROUND: A major route for cell-to-cell signalling in plants is mediated by cell wall-embedded pores termed plasmodesmata forming the symplasm. Plasmodesmata regulate the plant development and responses to the environment; however, our understanding of what factors or regulatory cues affect their structure and permeability is still limited. In this paper, a meta-analysis was carried out for the identification of conditions affecting plasmodesmata transport and for the in silico prediction of plasmodesmata proteins in species for which the plasmodesmata proteome has not been experimentally determined. RESULTS: Using the information obtained from experimental proteomes, an analysis pipeline (named plasmodesmata in silico proteome 1 or PIP1) was developed to rapidly generate candidate plasmodesmata proteomes for 22 plant species. Using the in silico proteomes to interrogate published transcriptomes, gene interaction networks were identified pointing to conditions likely affecting plasmodesmata transport capacity. High salinity, drought and osmotic stress regulate the expression of clusters enriched in genes encoding plasmodesmata proteins, including those involved in the metabolism of the cell wall polysaccharide callose. Experimental determinations showed restriction in the intercellular transport of the symplasmic reporter GFP and enhanced callose deposition in Arabidopsis roots exposed to 75-mM NaCl and 3% PEG (polyethylene glycol). Using PIP1 and transcriptome meta-analyses, candidate plasmodesmata proteins for the legume Medicago truncatula were generated, leading to the identification of Medtr1g073320, a novel receptor-like protein that localises at plasmodesmata. Expression of Medtr1g073320 affects callose deposition and the root response to infection with the soil-borne bacteria rhizobia in the presence of nitrate. CONCLUSIONS: Our study shows that combining proteomic meta-analysis and transcriptomic data can be a valuable tool for the identification of new proteins and regulatory mechanisms affecting plasmodesmata function. We have created the freely accessible pipeline PIP1 as a resource for the screening of experimental proteomes and for the in silico prediction of PD proteins in diverse plant species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01331-1. BioMed Central 2022-06-02 /pmc/articles/PMC9164936/ /pubmed/35655273 http://dx.doi.org/10.1186/s12915-022-01331-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Kirk, Philip
Amsbury, Sam
German, Liam
Gaudioso-Pedraza, Rocio
Benitez-Alfonso, Yoselin
A comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species
title A comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species
title_full A comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species
title_fullStr A comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species
title_full_unstemmed A comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species
title_short A comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species
title_sort comparative meta-proteomic pipeline for the identification of plasmodesmata proteins and regulatory conditions in diverse plant species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9164936/
https://www.ncbi.nlm.nih.gov/pubmed/35655273
http://dx.doi.org/10.1186/s12915-022-01331-1
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