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A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans

BACKGROUND: Pectins are a group of structurally complex plant cell wall polysaccharides whose biosynthesis and function remain poorly understood. The pectic polysaccharide rhamnogalacturonan-I (RG-I) has two types of arabinogalactan side chains, type-I and type-II arabinogalactans. To date few enzym...

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Autores principales: Stonebloom, Solomon, Ebert, Berit, Xiong, Guangyan, Pattathil, Sivakumar, Birdseye, Devon, Lao, Jeemeng, Pauly, Markus, Hahn, Michael G., Heazlewood, Joshua L., Scheller, Henrik Vibe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4836069/
https://www.ncbi.nlm.nih.gov/pubmed/27091363
http://dx.doi.org/10.1186/s12870-016-0780-x
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author Stonebloom, Solomon
Ebert, Berit
Xiong, Guangyan
Pattathil, Sivakumar
Birdseye, Devon
Lao, Jeemeng
Pauly, Markus
Hahn, Michael G.
Heazlewood, Joshua L.
Scheller, Henrik Vibe
author_facet Stonebloom, Solomon
Ebert, Berit
Xiong, Guangyan
Pattathil, Sivakumar
Birdseye, Devon
Lao, Jeemeng
Pauly, Markus
Hahn, Michael G.
Heazlewood, Joshua L.
Scheller, Henrik Vibe
author_sort Stonebloom, Solomon
collection PubMed
description BACKGROUND: Pectins are a group of structurally complex plant cell wall polysaccharides whose biosynthesis and function remain poorly understood. The pectic polysaccharide rhamnogalacturonan-I (RG-I) has two types of arabinogalactan side chains, type-I and type-II arabinogalactans. To date few enzymes involved in the biosynthesis of pectin have been described. Here we report the identification of a highly conserved putative glycosyltransferase encoding gene, Pectic ArabinoGalactan synthesis-Related (PAGR), affecting the biosynthesis of RG-I arabinogalactans and critical for pollen tube growth. RESULTS: T-DNA insertions in PAGR were identified in Arabidopsis thaliana and were found to segregate at a 1:1 ratio of heterozygotes to wild type. We were unable to isolate homozygous pagr mutants as pagr mutant alleles were not transmitted via pollen. In vitro pollen germination assays revealed reduced rates of pollen tube formation in pollen from pagr heterozygotes. To characterize a loss-of-function phenotype for PAGR, the Nicotiana benthamiana orthologs, NbPAGR-A and B, were transiently silenced using Virus Induced Gene Silencing. NbPAGR-silenced plants exhibited reduced internode and petiole expansion. Cell wall materials from NbPAGR-silenced plants had reduced galactose content compared to the control. Immunological and linkage analyses support that RG-I has reduced type-I arabinogalactan content and reduced branching of the RG-I backbone in NbPAGR-silenced plants. Arabidopsis lines overexpressing PAGR exhibit pleiotropic developmental phenotypes and the loss of apical dominance as well as an increase in RG-I type-II arabinogalactan content. CONCLUSIONS: Together, results support a function for PAGR in the biosynthesis of RG-I arabinogalactans and illustrate the essential roles of these polysaccharides in vegetative and reproductive plant growth. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0780-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-48360692016-04-20 A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans Stonebloom, Solomon Ebert, Berit Xiong, Guangyan Pattathil, Sivakumar Birdseye, Devon Lao, Jeemeng Pauly, Markus Hahn, Michael G. Heazlewood, Joshua L. Scheller, Henrik Vibe BMC Plant Biol Research Article BACKGROUND: Pectins are a group of structurally complex plant cell wall polysaccharides whose biosynthesis and function remain poorly understood. The pectic polysaccharide rhamnogalacturonan-I (RG-I) has two types of arabinogalactan side chains, type-I and type-II arabinogalactans. To date few enzymes involved in the biosynthesis of pectin have been described. Here we report the identification of a highly conserved putative glycosyltransferase encoding gene, Pectic ArabinoGalactan synthesis-Related (PAGR), affecting the biosynthesis of RG-I arabinogalactans and critical for pollen tube growth. RESULTS: T-DNA insertions in PAGR were identified in Arabidopsis thaliana and were found to segregate at a 1:1 ratio of heterozygotes to wild type. We were unable to isolate homozygous pagr mutants as pagr mutant alleles were not transmitted via pollen. In vitro pollen germination assays revealed reduced rates of pollen tube formation in pollen from pagr heterozygotes. To characterize a loss-of-function phenotype for PAGR, the Nicotiana benthamiana orthologs, NbPAGR-A and B, were transiently silenced using Virus Induced Gene Silencing. NbPAGR-silenced plants exhibited reduced internode and petiole expansion. Cell wall materials from NbPAGR-silenced plants had reduced galactose content compared to the control. Immunological and linkage analyses support that RG-I has reduced type-I arabinogalactan content and reduced branching of the RG-I backbone in NbPAGR-silenced plants. Arabidopsis lines overexpressing PAGR exhibit pleiotropic developmental phenotypes and the loss of apical dominance as well as an increase in RG-I type-II arabinogalactan content. CONCLUSIONS: Together, results support a function for PAGR in the biosynthesis of RG-I arabinogalactans and illustrate the essential roles of these polysaccharides in vegetative and reproductive plant growth. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0780-x) contains supplementary material, which is available to authorized users. BioMed Central 2016-04-18 /pmc/articles/PMC4836069/ /pubmed/27091363 http://dx.doi.org/10.1186/s12870-016-0780-x Text en © Stonebloom et al. 2016 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
Stonebloom, Solomon
Ebert, Berit
Xiong, Guangyan
Pattathil, Sivakumar
Birdseye, Devon
Lao, Jeemeng
Pauly, Markus
Hahn, Michael G.
Heazlewood, Joshua L.
Scheller, Henrik Vibe
A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans
title A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans
title_full A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans
title_fullStr A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans
title_full_unstemmed A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans
title_short A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans
title_sort duf-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4836069/
https://www.ncbi.nlm.nih.gov/pubmed/27091363
http://dx.doi.org/10.1186/s12870-016-0780-x
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