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Comprehensive characterization of the ALMT and MATE families on Populus trichocarpa and gene co-expression network analysis of its members during aluminium toxicity and phosphate starvation stresses

Abstract

Aluminium (Al) toxicity and phosphate deficit on soils are some of the main problems of modern agriculture and are usually associated. Some plants are able to overcome these stresses through exuding organic acids on the rhizosphere, such as citrate and malate, which are exported by MATE (Multi drug and toxin extrusion) and ALMT (Aluminium-activated malate transporter) transporters, respectively. Despite its co-action on acidic soils, few studies explore these two families' correlation, especially on tree crops, therefore we performed a comprehensive description of MATE and ALMT families on Populus trichocarpa as a model species for arboreal plants. We found 20 and 56 putative members of ALMT and MATE families, respectively. Then, a gene co-expression network analysis was performed using broad transcriptomic data to analyze which members of each family were transcriptionally associated. Four independent networks were generated, one of which is composed of members putatively related to phosphate starvation and aluminum toxicity stresses. The PoptrALMT10 and PoptrMATE54 genes were selected from this network for a deeper analysis, which revealed that in roots under phosphate starvation stress the two genes have independent transcriptional profiles, however, on the aluminum toxicity stress they share some common correlations with other genes. The data presented here help on the description of these gene families, of which some members are potentially involved in plant responses to acid soil-related stresses and its exploration is an important step towards using this knowledge on breeding programs for P. trichocarpa and other tree crops.

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Acknowledgements

We would like to thank the National Council for Scientific and Technological Development (CNPq) from Ministry of Science and Technology, Brazil, and the Foundation of Support Research of the State of Minas Gerais (FAPEMIG) for the financial support provided to this study. The Coordination for the Improvement of Higher Education Personnel (CAPES) from Ministry of Education, for the grants awarded to the authors. We also thank the Federal University of Lavras (UFLA) for providing the infrastructure and equipment to accomplish this research, including real-time PCR machine, computers and servers for bioinformatics analyses, which is supported by Ministry of Science and Technology and Ministry of Education.

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Thiago Bergamo Cardoso. The first draft of the manuscript was written by Thiago Bergamo Cardoso e Renan Terassi Pinto and review & editing by Luciano Vilela Paiva, all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Thiago Bergamo Cardoso or Luciano Vilela Paiva.

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The authors declare that they have no conflict of interest.

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This article does not contain any original research involving human participants or animals.

Electronic supplementary material

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File S1

Amino acid sequence of the characterized genes of the ALTM family, with the full name of the species and NCBI code, and the sequences of the members in Populus trichocarpa (TXT 17 KB)

File S2

Amino acid sequence of the characterized genes of the MATE family, with the full name of the species and NCBI code, and the sequences of the members in Populus trichocarpa (TXT 52 KB)

Figure S1

Description of the aluminium and phosphorus stress libraries. A Describes the distribution of treatments for aluminium and phosphorus stress, as well as the tissues used and the culture methodology. B Demonstrates the distribution pattern of the libraries for both stresses according to the Biological Coefficient of Variation (BCV) (EPS 1700 KB)

Figure S2

GO distribution in level 5 (top 20) for Biological Process, Molecular Function and Component Cellular (PDF 806 KB)

Table S1

Description of the genes used in this work. Description of the genes of the MATE and ALMT families that have been functionally characterized in other species. Description of members of the MATE and ALMT genetic families in Populus trichocarpa. Characteristics such as name, gene, conserved domain, number of transmembrane domains, number of amino acids and which subgroup of the phylogenetic (XLSX 174 KB)

Table S2

Co-expression network in root and leaf tissues under phosphorus and aluminium stresses (XLSX 172 KB)

Table S3

Result of the enrichment of the transcripts related to members of the ALMT and MATE families. A BLAST homology search against the NCBI non-redundant protein database. Gene ontologies (GO) were assigned using Blast2GO, mapped to existing gene categories. Finally, InterProScan was run through Blast2GO, and that were merged with the mapped gene ontologies (XLSX 699 KB)

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Cardoso, T.B., Pinto, R.T. & Paiva, L.V. Comprehensive characterization of the ALMT and MATE families on Populus trichocarpa and gene co-expression network analysis of its members during aluminium toxicity and phosphate starvation stresses. 3 Biotech 10, 525 (2020). https://doi.org/10.1007/s13205-020-02528-3

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  • DOI: https://doi.org/10.1007/s13205-020-02528-3

Keywords

  • Acid soil
  • Phosphorus starvation
  • Aluminum toxicity
  • Phylogenetic analyses
  • Synteny
  • Gene regulation