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A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants

Multidrug and toxic compound extrusion (MATE) transporters comprise a multigene family that mediates multiple functions in plants through the efflux of diverse substrates including organic molecules, specialized metabolites, hormones, and xenobiotics. MATE classification based on genome-wide studies...

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Autores principales: Nimmy, Manduparambil Subramanian, Kumar, Vinod, Suthanthiram, Backiyarani, Subbaraya, Uma, Nagar, Ramawatar, Bharadwaj, Chellapilla, Jain, Pradeep Kumar, Krishnamurthy, Panneerselvam
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8970042/
https://www.ncbi.nlm.nih.gov/pubmed/35371145
http://dx.doi.org/10.3389/fpls.2022.774885
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author Nimmy, Manduparambil Subramanian
Kumar, Vinod
Suthanthiram, Backiyarani
Subbaraya, Uma
Nagar, Ramawatar
Bharadwaj, Chellapilla
Jain, Pradeep Kumar
Krishnamurthy, Panneerselvam
author_facet Nimmy, Manduparambil Subramanian
Kumar, Vinod
Suthanthiram, Backiyarani
Subbaraya, Uma
Nagar, Ramawatar
Bharadwaj, Chellapilla
Jain, Pradeep Kumar
Krishnamurthy, Panneerselvam
author_sort Nimmy, Manduparambil Subramanian
collection PubMed
description Multidrug and toxic compound extrusion (MATE) transporters comprise a multigene family that mediates multiple functions in plants through the efflux of diverse substrates including organic molecules, specialized metabolites, hormones, and xenobiotics. MATE classification based on genome-wide studies remains ambiguous, likely due to a lack of large-scale phylogenomic studies and/or reference sequence datasets. To resolve this, we established a phylogeny of the plant MATE gene family using a comprehensive kingdom-wide phylogenomic analysis of 74 diverse plant species. We identified more than 4,000 MATEs, which were classified into 14 subgroups based on a systematic bioinformatics pipeline using USEARCH, blast+ and synteny network tools. Our classification was performed using a four-step process, whereby MATEs sharing ≥ 60% protein sequence identity with a ≤ 1E-05 threshold at different sequence lengths (either full-length, ≥ 60% length, or ≥ 150 amino acids) or retaining in the similar synteny blocks were assigned to the same subgroup. In this way, we assigned subgroups to 95.8% of the identified MATEs, which we substantiated using synteny network clustering analysis. The subgroups were clustered under four major phylogenetic groups and named according to their clockwise appearance within each group. We then generated a reference sequence dataset, the usefulness of which was demonstrated in the classification of MATEs in additional species not included in the original analysis. Approximately 74% of the plant MATEs exhibited synteny relationships with angiosperm-wide or lineage-, order/family-, and species-specific conservation. Most subgroups evolved independently, and their distinct evolutionary trends were likely associated with the development of functional novelties or the maintenance of conserved functions. Together with the systematic classification and synteny network profiling analyses, we identified all the major evolutionary events experienced by the MATE gene family in plants. We believe that our findings and the reference dataset provide a valuable resource to guide future functional studies aiming to explore the key roles of MATEs in different aspects of plant physiology. Our classification framework can also be readily extendable to other (super) families.
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spelling pubmed-89700422022-04-01 A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants Nimmy, Manduparambil Subramanian Kumar, Vinod Suthanthiram, Backiyarani Subbaraya, Uma Nagar, Ramawatar Bharadwaj, Chellapilla Jain, Pradeep Kumar Krishnamurthy, Panneerselvam Front Plant Sci Plant Science Multidrug and toxic compound extrusion (MATE) transporters comprise a multigene family that mediates multiple functions in plants through the efflux of diverse substrates including organic molecules, specialized metabolites, hormones, and xenobiotics. MATE classification based on genome-wide studies remains ambiguous, likely due to a lack of large-scale phylogenomic studies and/or reference sequence datasets. To resolve this, we established a phylogeny of the plant MATE gene family using a comprehensive kingdom-wide phylogenomic analysis of 74 diverse plant species. We identified more than 4,000 MATEs, which were classified into 14 subgroups based on a systematic bioinformatics pipeline using USEARCH, blast+ and synteny network tools. Our classification was performed using a four-step process, whereby MATEs sharing ≥ 60% protein sequence identity with a ≤ 1E-05 threshold at different sequence lengths (either full-length, ≥ 60% length, or ≥ 150 amino acids) or retaining in the similar synteny blocks were assigned to the same subgroup. In this way, we assigned subgroups to 95.8% of the identified MATEs, which we substantiated using synteny network clustering analysis. The subgroups were clustered under four major phylogenetic groups and named according to their clockwise appearance within each group. We then generated a reference sequence dataset, the usefulness of which was demonstrated in the classification of MATEs in additional species not included in the original analysis. Approximately 74% of the plant MATEs exhibited synteny relationships with angiosperm-wide or lineage-, order/family-, and species-specific conservation. Most subgroups evolved independently, and their distinct evolutionary trends were likely associated with the development of functional novelties or the maintenance of conserved functions. Together with the systematic classification and synteny network profiling analyses, we identified all the major evolutionary events experienced by the MATE gene family in plants. We believe that our findings and the reference dataset provide a valuable resource to guide future functional studies aiming to explore the key roles of MATEs in different aspects of plant physiology. Our classification framework can also be readily extendable to other (super) families. Frontiers Media S.A. 2022-03-15 /pmc/articles/PMC8970042/ /pubmed/35371145 http://dx.doi.org/10.3389/fpls.2022.774885 Text en Copyright © 2022 Nimmy, Kumar, Suthanthiram, Subbaraya, Nagar, Bharadwaj, Jain and Krishnamurthy. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Nimmy, Manduparambil Subramanian
Kumar, Vinod
Suthanthiram, Backiyarani
Subbaraya, Uma
Nagar, Ramawatar
Bharadwaj, Chellapilla
Jain, Pradeep Kumar
Krishnamurthy, Panneerselvam
A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants
title A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants
title_full A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants
title_fullStr A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants
title_full_unstemmed A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants
title_short A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants
title_sort systematic phylogenomic classification of the multidrug and toxic compound extrusion transporter gene family in plants
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8970042/
https://www.ncbi.nlm.nih.gov/pubmed/35371145
http://dx.doi.org/10.3389/fpls.2022.774885
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