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Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species

BACKGROUND: Cellular membranes are dynamic structures, continuously adjusting their composition, allowing plants to respond to developmental signals, stresses, and changing environments. To facilitate transmembrane transport of substrates, plant membranes are embedded with both active and passive tr...

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Autores principales: De Rosa, Annamaria, Watson-Lazowski, Alexander, Evans, John R., Groszmann, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7285608/
https://www.ncbi.nlm.nih.gov/pubmed/32517797
http://dx.doi.org/10.1186/s12870-020-02412-5
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author De Rosa, Annamaria
Watson-Lazowski, Alexander
Evans, John R.
Groszmann, Michael
author_facet De Rosa, Annamaria
Watson-Lazowski, Alexander
Evans, John R.
Groszmann, Michael
author_sort De Rosa, Annamaria
collection PubMed
description BACKGROUND: Cellular membranes are dynamic structures, continuously adjusting their composition, allowing plants to respond to developmental signals, stresses, and changing environments. To facilitate transmembrane transport of substrates, plant membranes are embedded with both active and passive transporters. Aquaporins (AQPs) constitute a major family of membrane spanning channel proteins that selectively facilitate the passive bidirectional passage of substrates across biological membranes at an astonishing 10(8) molecules per second. AQPs are the most diversified in the plant kingdom, comprising of five major subfamilies that differ in temporal and spatial gene expression, subcellular protein localisation, substrate specificity, and post-translational regulatory mechanisms; collectively providing a dynamic transportation network spanning the entire plant. Plant AQPs can transport a range of solutes essential for numerous plant processes including, water relations, growth and development, stress responses, root nutrient uptake, and photosynthesis. The ability to manipulate AQPs towards improving plant productivity, is reliant on expanding our insight into the diversity and functional roles of AQPs. RESULTS: We characterised the AQP family from Nicotiana tabacum (NtAQPs; tobacco), a popular model system capable of scaling from the laboratory to the field. Tobacco is closely related to major economic crops (e.g. tomato, potato, eggplant and peppers) and itself has new commercial applications. Tobacco harbours 76 AQPs making it the second largest characterised AQP family. These fall into five distinct subfamilies, for which we characterised phylogenetic relationships, gene structures, protein sequences, selectivity filter compositions, sub-cellular localisation, and tissue-specific expression. We also identified the AQPs from tobacco’s parental genomes (N. sylvestris and N. tomentosiformis), allowing us to characterise the evolutionary history of the NtAQP family. Assigning orthology to tomato and potato AQPs allowed for cross-species comparisons of conservation in protein structures, gene expression, and potential physiological roles. CONCLUSIONS: This study provides a comprehensive characterisation of the tobacco AQP family, and strengthens the current knowledge of AQP biology. The refined gene/protein models, tissue-specific expression analysis, and cross-species comparisons, provide valuable insight into the evolutionary history and likely physiological roles of NtAQPs and their Solanaceae orthologs. Collectively, these results will support future functional studies and help transfer basic research to applied agriculture.
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spelling pubmed-72856082020-06-10 Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species De Rosa, Annamaria Watson-Lazowski, Alexander Evans, John R. Groszmann, Michael BMC Plant Biol Research Article BACKGROUND: Cellular membranes are dynamic structures, continuously adjusting their composition, allowing plants to respond to developmental signals, stresses, and changing environments. To facilitate transmembrane transport of substrates, plant membranes are embedded with both active and passive transporters. Aquaporins (AQPs) constitute a major family of membrane spanning channel proteins that selectively facilitate the passive bidirectional passage of substrates across biological membranes at an astonishing 10(8) molecules per second. AQPs are the most diversified in the plant kingdom, comprising of five major subfamilies that differ in temporal and spatial gene expression, subcellular protein localisation, substrate specificity, and post-translational regulatory mechanisms; collectively providing a dynamic transportation network spanning the entire plant. Plant AQPs can transport a range of solutes essential for numerous plant processes including, water relations, growth and development, stress responses, root nutrient uptake, and photosynthesis. The ability to manipulate AQPs towards improving plant productivity, is reliant on expanding our insight into the diversity and functional roles of AQPs. RESULTS: We characterised the AQP family from Nicotiana tabacum (NtAQPs; tobacco), a popular model system capable of scaling from the laboratory to the field. Tobacco is closely related to major economic crops (e.g. tomato, potato, eggplant and peppers) and itself has new commercial applications. Tobacco harbours 76 AQPs making it the second largest characterised AQP family. These fall into five distinct subfamilies, for which we characterised phylogenetic relationships, gene structures, protein sequences, selectivity filter compositions, sub-cellular localisation, and tissue-specific expression. We also identified the AQPs from tobacco’s parental genomes (N. sylvestris and N. tomentosiformis), allowing us to characterise the evolutionary history of the NtAQP family. Assigning orthology to tomato and potato AQPs allowed for cross-species comparisons of conservation in protein structures, gene expression, and potential physiological roles. CONCLUSIONS: This study provides a comprehensive characterisation of the tobacco AQP family, and strengthens the current knowledge of AQP biology. The refined gene/protein models, tissue-specific expression analysis, and cross-species comparisons, provide valuable insight into the evolutionary history and likely physiological roles of NtAQPs and their Solanaceae orthologs. Collectively, these results will support future functional studies and help transfer basic research to applied agriculture. BioMed Central 2020-06-09 /pmc/articles/PMC7285608/ /pubmed/32517797 http://dx.doi.org/10.1186/s12870-020-02412-5 Text en © The Author(s) 2020 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/. 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 in a credit line to the data.
spellingShingle Research Article
De Rosa, Annamaria
Watson-Lazowski, Alexander
Evans, John R.
Groszmann, Michael
Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species
title Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species
title_full Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species
title_fullStr Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species
title_full_unstemmed Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species
title_short Genome-wide identification and characterisation of Aquaporins in Nicotiana tabacum and their relationships with other Solanaceae species
title_sort genome-wide identification and characterisation of aquaporins in nicotiana tabacum and their relationships with other solanaceae species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7285608/
https://www.ncbi.nlm.nih.gov/pubmed/32517797
http://dx.doi.org/10.1186/s12870-020-02412-5
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