Global analysis of the MATE gene family of metabolite transporters in tomato

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Abstract

Background

Species in the Solanaceae family are known for producing plethora of specialized metabolites. In addition to biosynthesis pathways, a full comprehension of secondary metabolism must also take into account the transport and subcellular compartmentalization of substances. Here, we examined the MATE (Multidrug and Toxic Compound Extrusion, or Multi-Antimicrobial Extrusion) gene family in the tomato ( Solanum lycopersicum) genome with the objective of better understanding the transport of secondary metabolites in this model species. MATE membrane effluxers encompass an ancient gene family of secondary transporters present in all kingdoms of life, but with a remarkable expansion in plants. They mediate the transport of primary and secondary metabolites using the proton motive force through several membrane systems of the cell.

Results

We identified 67 genes coding for MATE transporters in the tomato genome, 33 of which are expressed constitutively whereas 34 are expressed in specific cell types or environmental conditions. Synteny analyses revealed bona fide paralogs and Arabidopsis orthologs. Co-expression analysis between MATE and regulatory genes revealed 78 positive and 8 negative strong associations (ρ≥|0.8|). We found no evidence of MATE transporters belonging to known metabolic gene clusters in tomato.

Conclusions

Altogether, our expression data, phylogenetic analyses, and synteny study provide strong evidence of functional homologies between MATE genes of tomato and Arabidopsis thaliana. Our co-expression study revealed potential transcriptional regulators of MATE genes that warrant further investigation. This work sets the stage for genome-wide functional analyses of MATE transporters in tomato and other Solanaceae species of economic relevance.

Electronic supplementary material

The online version of this article (10.1186/s12870-017-1115-2) contains supplementary material, which is available to authorized users.

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Most cited references 82

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A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum.

Jurandir Magalhaes, Jiping Liu, Claudia T Guimaraes … (2007)

Crop yields are significantly reduced by aluminum toxicity on highly acidic soils, which comprise up to 50% of the world's arable land. Candidate aluminum tolerance proteins include organic acid efflux transporters, with the organic acids forming non-toxic complexes with rhizosphere aluminum. In this study, we used positional cloning to identify the gene encoding a member of the multidrug and toxic compound extrusion (MATE) family, an aluminum-activated citrate transporter, as responsible for the major sorghum (Sorghum bicolor) aluminum tolerance locus, Alt(SB). Polymorphisms in regulatory regions of Alt(SB) are likely to contribute to large allelic effects, acting to increase Alt(SB) expression in the root apex of tolerant genotypes. Furthermore, aluminum-inducible Alt(SB) expression is associated with induction of aluminum tolerance via enhanced root citrate exudation. These findings will allow us to identify superior Alt(SB) haplotypes that can be incorporated via molecular breeding and biotechnology into acid soil breeding programs, thus helping to increase crop yields in developing countries where acidic soils predominate.

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Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids.

Eric Lyons, Brent Pedersen, Josh Kane … (2008)

In addition to the genomes of Arabidopsis (Arabidopsis thaliana) and poplar (Populus trichocarpa), two near-complete rosid genome sequences, grape (Vitis vinifera) and papaya (Carica papaya), have been recently released. The phylogenetic relationship among these four genomes and the placement of their three independent, fractionated tetraploidies sum to a powerful comparative genomic system. CoGe, a platform of multiple whole or near-complete genome sequences, provides an integrative Web-based system to find and align syntenic chromosomal regions and visualize the output in an intuitive and interactive manner. CoGe has been customized to specifically support comparisons among the rosids. Crucial facts and definitions are presented to clearly describe the sorts of biological questions that might be answered in part using CoGe, including patterns of DNA conservation, accuracy of annotation, transposability of individual genes, subfunctionalization and/or fractionation of syntenic gene sets, and conserved noncoding sequence content. This précis of an online tutorial, CoGe with Rosids (http://tinyurl.com/4a23pk), presents sample results graphically.

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Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance.

Jiping Liu, Jurandir Magalhaes, Jon Shaff … (2009)

Aluminum-activated root malate and citrate exudation play an important role in plant Al tolerance. This paper characterizes AtMATE, a homolog of the recently discovered sorghum and barley Al-tolerance genes, shown here to encode an Al-activated citrate transporter in Arabidopsis. Together with the previously characterized Al-activated malate transporter, AtALMT1, this discovery allowed us to examine the relationship in the same species between members of the two gene families for which Al-tolerance genes have been identified. AtMATE is expressed primarily in roots and is induced by Al. An AtMATE T-DNA knockdown line exhibited very low AtMATE expression and Al-activated root citrate exudation was abolished. The AtALMT1 AtMATE double mutant lacked both Al-activated root malate and citrate exudation and showed greater Al sensitivity than the AtALMT1 mutant. Therefore, although AtALMT1 is a major contributor to Arabidopsis Al tolerance, AtMATE also makes a significant but smaller contribution. The expression patterns of AtALMT1 and AtMATE and the profiles of Al-activated root citrate and malate exudation are not affected by the presence or absence of the other gene. These results suggest that AtALMT1-mediated malate exudation and AtMATE-mediated citrate exudation evolved independently to confer Al tolerance in Arabidopsis. However, a link between regulation of expression of the two transporters in response to Al was identified through work on STOP1, a transcription factor that was previously shown to be necessary for AtALMT1 expression. Here we show that STOP1 is also required for AtMATE expression and Al-activated citrate exudation.

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Author and article information

Contributors

Vagner Augusto Benedito: +1-304-293-5434 , vagner.benedito@mail.wvu.edu

Journal

Journal ID (nlm-ta): BMC Plant Biol

Journal ID (iso-abbrev): BMC Plant Biol

Title: BMC Plant Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2229

Publication date (Electronic): 30 October 2017

Publication date PMC-release: 30 October 2017

Publication date Collection: 2017

Volume: 17

Electronic Location Identifier: 185

Affiliations

[1 ]ISNI 0000 0001 2156 6140, GRID grid.268154.c, Division of Plant and Soil Sciences, , West Virginia University, ; 3425 New Agricultural Sciences Building, Morgantown, WV 26506-6108 USA

[2 ]ISNI 0000 0000 8816 9513, GRID grid.411269.9, Plant Molecular Physiology Laboratory, Biology Department, , Federal University of Lavras (UFLA), ; Lavras, MG Brazil

[3 ]ISNI 0000 0001 0664 9773, GRID grid.59056.3f, Department of Biotechnology, , University of Calcutta, ; Kolkata, India

[4 ]ISNI 0000 0004 1760 4804, GRID grid.411389.6, State Key Laboratory of Tea Plant Biology and Utilization, College of Tea and Food Sciences, , Anhui Agricultural University, ; Hefei, 230036 China

Article

Publisher ID: 1115

DOI: 10.1186/s12870-017-1115-2

PMC ID: 5663081

PubMed ID: 29084510

SO-VID: 39a562d8-da58-4786-844b-ec39d81a3f43

License:

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.

History

Date received : 5 April 2017

Date accepted : 9 October 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;

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ScienceOpen disciplines: Plant science & Botany

Keywords: antiporter,efflux,genome evolution,metabolic gene cluster,regulatory gene network

Data availability:

ScienceOpen disciplines: Plant science & Botany

Keywords: antiporter, efflux, genome evolution, metabolic gene cluster, regulatory gene network

Global analysis of the MATE gene family of metabolite transporters in tomato

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Plant MYBs

Most cited references 82

A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum.

Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids.

Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance.

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