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.

Keywords: Acid soil; Aluminum toxicity; Gene regulation; Phosphorus starvation; Phylogenetic analyses; Synteny.

Fig. 1

Phylogeny of the ALMT transporter family in the Populus trichocarpa genome. The phylogenetic tree was constructed by MEGA 7.0 using Neighbour-Joining method. Bootstrap values in percentage (1000 replicates) are indicated on the nodes. The phylogenetic tree shows the distribution of the ALMT sequences from Populus (colored according to the subgroup), divided into three subgroups (A in red, B in green and C in blue), along with other members that are functionally characterized in other plant species (black)

Fig. 2

Synteny analysis of ALMT genes in the Populus genome. a Identification of eight pairs of paralogs within the Populus genome using microsynteny. b Synteny analysis between the ALMT family in Populus and the Arabidopsis thaliana genome, with five syntenic paralogs. C Tandem duplications of the ALMT genes in the Populus genome

Fig. 3

Expression profile of ALMT transporters. The heat map with hierarchical clustering of 15 PoptrALMT genes was constructed using PopGenIE platform by average linkage with Euclidean distance. Colour key represents the relative transcript abundance of the PoptrALMT genes in 24 Populus tissues according to the variation of the standard score (VST). Genes are sorted according to their expression profile and coloured according to the phylogenetic tree subgroups

Fig. 4

The phylogenetic tree of MATE proteins from P. trichocarpa. The tree uses the same units for the distance of the branches and the evolutionary distances used to infer the phylogenetic tree. Evolutionary distances were calculated using the p-distance method. The evolutionary history was inferred using the Neighbour-Joining method with 1000 bootstraps. The phylogenetic tree shows the distribution of MATE sequences in Populus (colored according to the subgroup) along with other sequences of MATE transporters functionally characterized in other plant species (black). The tree was divided into five groups (I in green, II in yellow, III in blue, IV in purple and V in red), some groups have subgroups, being indicated by the numbers 1, 2, 3 and 4

Fig. 5

Expression of the MATE transporter family in Populus trichocarpa. The heat map with hierarchical clustering of 56 PoptrMATE genes was constructed using PopGenIE platform by average linkage with Euclidean distance. Colour key represents the relative transcript abundance of the PoptrMATE genes in 24 Populus tissues according to the variation of the standard score (VST). The colour of the genes corresponds to their location in the phylogenetic tree

Fig. 6

A gene coexpression network between the MATE and ALMT family’s members and an illustration of the expression in different tissues. a Correlation network between members of the ALMT and MATE families constructed using Pearson’s correlation with a minimum correlation of |0.7|. The colors of the circles are according to the groups of the phylogenetic trees. The thickness of the connection is proportional to the value of the correlation, the closer to |1| the thicker. b Illustration of the expression of the genes of the MATE and ALMT family in six plant tissues, the colour of the tissues corresponds to the number of transcripts

Fig. 7

Correlation network between the PoptrALMT10 and PoptrMATE54 genes under phosphorus and aluminium stresses. For the phosphorus stress, two tissues were analysed: leaf and root. For the aluminium stress, only the root was analysed. The correlation network was constructed using Spearman’s correlation with a minimum correlation of |0.8|