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A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees

BACKGROUND: Secretory Carrier-Associated Membrane Proteins (SCAMPs) are highly conserved 32–38 kDa proteins that are involved in membrane trafficking. A systems approach was taken to elucidate function of SCAMPs in wood formation of Populus trees. Phenotypic and multi-omics analyses were performed i...

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Autores principales: Obudulu, Ogonna, Mähler, Niklas, Skotare, Tomas, Bygdell, Joakim, Abreu, Ilka N., Ahnlund, Maria, Latha Gandla, Madhavi, Petterle, Anna, Moritz, Thomas, Hvidsten, Torgeir R., Jönsson, Leif J., Wingsle, Gunnar, Trygg, Johan, Tuominen, Hannele
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5753437/
https://www.ncbi.nlm.nih.gov/pubmed/29298676
http://dx.doi.org/10.1186/s12864-017-4411-1
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author Obudulu, Ogonna
Mähler, Niklas
Skotare, Tomas
Bygdell, Joakim
Abreu, Ilka N.
Ahnlund, Maria
Latha Gandla, Madhavi
Petterle, Anna
Moritz, Thomas
Hvidsten, Torgeir R.
Jönsson, Leif J.
Wingsle, Gunnar
Trygg, Johan
Tuominen, Hannele
author_facet Obudulu, Ogonna
Mähler, Niklas
Skotare, Tomas
Bygdell, Joakim
Abreu, Ilka N.
Ahnlund, Maria
Latha Gandla, Madhavi
Petterle, Anna
Moritz, Thomas
Hvidsten, Torgeir R.
Jönsson, Leif J.
Wingsle, Gunnar
Trygg, Johan
Tuominen, Hannele
author_sort Obudulu, Ogonna
collection PubMed
description BACKGROUND: Secretory Carrier-Associated Membrane Proteins (SCAMPs) are highly conserved 32–38 kDa proteins that are involved in membrane trafficking. A systems approach was taken to elucidate function of SCAMPs in wood formation of Populus trees. Phenotypic and multi-omics analyses were performed in woody tissues of transgenic Populus trees carrying an RNAi construct for Populus tremula x tremuloides SCAMP3 (PttSCAMP3; Potri.019G104000). RESULTS: The woody tissues of the transgenic trees displayed increased amounts of both polysaccharides and lignin oligomers, indicating increased deposition of both the carbohydrate and lignin components of the secondary cell walls. This coincided with a tendency towards increased wood density as well as significantly increased thickness of the suberized cork in the transgenic lines. Multivariate OnPLS (orthogonal projections to latent structures) modeling of five different omics datasets (the transcriptome, proteome, GC-MS metabolome, LC-MS metabolome and pyrolysis-GC/MS metabolome) collected from the secondary xylem tissues of the stem revealed systemic variation in the different variables in the transgenic lines, including changes that correlated with the changes in the secondary cell wall composition. The OnPLS model also identified a rather large number of proteins that were more abundant in the transgenic lines than in the wild type. Several of these were related to secretion and/or endocytosis as well as both primary and secondary cell wall biosynthesis. CONCLUSIONS: Populus SCAMP proteins were shown to influence accumulation of secondary cell wall components, including polysaccharides and phenolic compounds, in the woody tissues of Populus tree stems. Our multi-omics analyses combined with the OnPLS modelling suggest that this function is mediated by changes in membrane trafficking to fine-tune the abundance of cell wall precursors and/or proteins involved in cell wall biosynthesis and transport. The data provides a multi-level source of information for future studies on the function of the SCAMP proteins in plant stem tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4411-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-57534372018-01-05 A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees Obudulu, Ogonna Mähler, Niklas Skotare, Tomas Bygdell, Joakim Abreu, Ilka N. Ahnlund, Maria Latha Gandla, Madhavi Petterle, Anna Moritz, Thomas Hvidsten, Torgeir R. Jönsson, Leif J. Wingsle, Gunnar Trygg, Johan Tuominen, Hannele BMC Genomics Research Article BACKGROUND: Secretory Carrier-Associated Membrane Proteins (SCAMPs) are highly conserved 32–38 kDa proteins that are involved in membrane trafficking. A systems approach was taken to elucidate function of SCAMPs in wood formation of Populus trees. Phenotypic and multi-omics analyses were performed in woody tissues of transgenic Populus trees carrying an RNAi construct for Populus tremula x tremuloides SCAMP3 (PttSCAMP3; Potri.019G104000). RESULTS: The woody tissues of the transgenic trees displayed increased amounts of both polysaccharides and lignin oligomers, indicating increased deposition of both the carbohydrate and lignin components of the secondary cell walls. This coincided with a tendency towards increased wood density as well as significantly increased thickness of the suberized cork in the transgenic lines. Multivariate OnPLS (orthogonal projections to latent structures) modeling of five different omics datasets (the transcriptome, proteome, GC-MS metabolome, LC-MS metabolome and pyrolysis-GC/MS metabolome) collected from the secondary xylem tissues of the stem revealed systemic variation in the different variables in the transgenic lines, including changes that correlated with the changes in the secondary cell wall composition. The OnPLS model also identified a rather large number of proteins that were more abundant in the transgenic lines than in the wild type. Several of these were related to secretion and/or endocytosis as well as both primary and secondary cell wall biosynthesis. CONCLUSIONS: Populus SCAMP proteins were shown to influence accumulation of secondary cell wall components, including polysaccharides and phenolic compounds, in the woody tissues of Populus tree stems. Our multi-omics analyses combined with the OnPLS modelling suggest that this function is mediated by changes in membrane trafficking to fine-tune the abundance of cell wall precursors and/or proteins involved in cell wall biosynthesis and transport. The data provides a multi-level source of information for future studies on the function of the SCAMP proteins in plant stem tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4411-1) contains supplementary material, which is available to authorized users. BioMed Central 2018-01-03 /pmc/articles/PMC5753437/ /pubmed/29298676 http://dx.doi.org/10.1186/s12864-017-4411-1 Text en © The Author(s). 2018 Open AccessThis 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. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Obudulu, Ogonna
Mähler, Niklas
Skotare, Tomas
Bygdell, Joakim
Abreu, Ilka N.
Ahnlund, Maria
Latha Gandla, Madhavi
Petterle, Anna
Moritz, Thomas
Hvidsten, Torgeir R.
Jönsson, Leif J.
Wingsle, Gunnar
Trygg, Johan
Tuominen, Hannele
A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees
title A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees
title_full A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees
title_fullStr A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees
title_full_unstemmed A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees
title_short A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees
title_sort multi-omics approach reveals function of secretory carrier-associated membrane proteins in wood formation of​ ​​populus​​ ​trees
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5753437/
https://www.ncbi.nlm.nih.gov/pubmed/29298676
http://dx.doi.org/10.1186/s12864-017-4411-1
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