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Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization

BACKGROUND: As in animals, cell–cell communication plays a pivotal role in male–female recognition during plant sexual reproduction. Prelaid peptides secreted from the female reproductive tissues guide pollen tubes towards ovules for fertilization. However, the elaborate mechanisms for this dialogue...

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Autores principales: Hafidh, Said, Potěšil, David, Fíla, Jan, Čapková, Věra, Zdráhal, Zbyněk, Honys, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4853860/
https://www.ncbi.nlm.nih.gov/pubmed/27139692
http://dx.doi.org/10.1186/s13059-016-0928-x
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author Hafidh, Said
Potěšil, David
Fíla, Jan
Čapková, Věra
Zdráhal, Zbyněk
Honys, David
author_facet Hafidh, Said
Potěšil, David
Fíla, Jan
Čapková, Věra
Zdráhal, Zbyněk
Honys, David
author_sort Hafidh, Said
collection PubMed
description BACKGROUND: As in animals, cell–cell communication plays a pivotal role in male–female recognition during plant sexual reproduction. Prelaid peptides secreted from the female reproductive tissues guide pollen tubes towards ovules for fertilization. However, the elaborate mechanisms for this dialogue have remained elusive, particularly from the male perspective. RESULTS: We performed genome-wide quantitative liquid chromatography–tandem mass spectrometry analysis of a pistil-stimulated pollen tube secretome and identified 801 pollen tube-secreted proteins. Interestingly, in silico analysis reveals that the pollen tube secretome is dominated by proteins that are secreted unconventionally, representing 57 % of the total secretome. In support, we show that an unconventionally secreted protein, translationally controlled tumor protein, is secreted to the apoplast. Remarkably, we discovered that this protein could be secreted by infiltrating through the initial phases of the conventional secretory pathway and could reach the apoplast via exosomes, as demonstrated by co-localization with Oleisin1 exosome marker. We demonstrate that translationally controlled tumor protein-knockdown Arabidopsis thaliana plants produce pollen tubes that navigate poorly to the target ovule and that the mutant allele is poorly transmitted through the male. Further, we show that regulators of the endoplasmic reticulum–trans-Golgi network protein secretory pathway control secretion of Nicotiana tabacum Pollen tube-secreted cysteine-rich protein 2 and Lorelei-like GPI-anchor protein 3 and that a regulator of endoplasmic reticulum–trans-Golgi protein translocation is essential for pollen tube growth, pollen tube guidance and ovule-targeting competence. CONCLUSIONS: This work, the first study on the pollen tube secretome, identifies novel genome-wide pollen tube-secreted proteins with potential functions in pollen tube guidance towards ovules for sexual reproduction. Functional analysis highlights a potential mechanism for unconventional secretion of pollen tube proteins and reveals likely regulators of conventional pollen tube protein secretion. The association of pollen tube-secreted proteins with marker proteins shown to be secreted via exosomes in other species suggests exosome secretion is a possible mechanism for cell–cell communication between the pollen tube and female reproductive cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-016-0928-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-48538602016-05-04 Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization Hafidh, Said Potěšil, David Fíla, Jan Čapková, Věra Zdráhal, Zbyněk Honys, David Genome Biol Research BACKGROUND: As in animals, cell–cell communication plays a pivotal role in male–female recognition during plant sexual reproduction. Prelaid peptides secreted from the female reproductive tissues guide pollen tubes towards ovules for fertilization. However, the elaborate mechanisms for this dialogue have remained elusive, particularly from the male perspective. RESULTS: We performed genome-wide quantitative liquid chromatography–tandem mass spectrometry analysis of a pistil-stimulated pollen tube secretome and identified 801 pollen tube-secreted proteins. Interestingly, in silico analysis reveals that the pollen tube secretome is dominated by proteins that are secreted unconventionally, representing 57 % of the total secretome. In support, we show that an unconventionally secreted protein, translationally controlled tumor protein, is secreted to the apoplast. Remarkably, we discovered that this protein could be secreted by infiltrating through the initial phases of the conventional secretory pathway and could reach the apoplast via exosomes, as demonstrated by co-localization with Oleisin1 exosome marker. We demonstrate that translationally controlled tumor protein-knockdown Arabidopsis thaliana plants produce pollen tubes that navigate poorly to the target ovule and that the mutant allele is poorly transmitted through the male. Further, we show that regulators of the endoplasmic reticulum–trans-Golgi network protein secretory pathway control secretion of Nicotiana tabacum Pollen tube-secreted cysteine-rich protein 2 and Lorelei-like GPI-anchor protein 3 and that a regulator of endoplasmic reticulum–trans-Golgi protein translocation is essential for pollen tube growth, pollen tube guidance and ovule-targeting competence. CONCLUSIONS: This work, the first study on the pollen tube secretome, identifies novel genome-wide pollen tube-secreted proteins with potential functions in pollen tube guidance towards ovules for sexual reproduction. Functional analysis highlights a potential mechanism for unconventional secretion of pollen tube proteins and reveals likely regulators of conventional pollen tube protein secretion. The association of pollen tube-secreted proteins with marker proteins shown to be secreted via exosomes in other species suggests exosome secretion is a possible mechanism for cell–cell communication between the pollen tube and female reproductive cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-016-0928-x) contains supplementary material, which is available to authorized users. BioMed Central 2016-05-03 /pmc/articles/PMC4853860/ /pubmed/27139692 http://dx.doi.org/10.1186/s13059-016-0928-x Text en © Hafidh 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
Hafidh, Said
Potěšil, David
Fíla, Jan
Čapková, Věra
Zdráhal, Zbyněk
Honys, David
Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization
title Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization
title_full Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization
title_fullStr Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization
title_full_unstemmed Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization
title_short Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization
title_sort quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4853860/
https://www.ncbi.nlm.nih.gov/pubmed/27139692
http://dx.doi.org/10.1186/s13059-016-0928-x
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