Genetic variability and evolutionary diversification of membrane ABC transporters in plants

Abstract

Background: ATP-binding cassette proteins have been recognized as playing a crucial role in the regulation of growth and resistance processes in all kingdoms of life. They have been deeply studied in vertebrates because of their role in drug resistance, but much less is known about ABC superfamily functions in plants.

Results: Recently released plant genome sequences allowed us to identify 803 ABC transporters in four vascular plants (Oryza. sativa, Solanum lycopersicum, Solanum tuberosum and Vitis vinifera) and 76 transporters in the green alga Volvox carteri, by comparing them with those reannotated in Arabidopsis thaliana and the yeast Saccharomyces cerevisiae. Retrieved proteins have been phylogenetically analysed to infer orthologous relationships. Most orthologous relationships in the A, D, E and F subfamilies were found, and interesting expansions within the ABCG subfamily were observed and discussed. A high level of purifying selection is acting in the five ABC subfamilies A, B, C, D and E. However, evolutionary rates of recent duplicate genes could influence vascular plant genome diversification. The transcription profiles of ABC genes within tomato organs revealed a broad functional role for some transporters and a more specific activity for others, suggesting the presence of key ABC regulators in tomato.

Conclusions: The findings achieved in this work could contribute to address several biological questions concerning the evolution of the relationship between genomes of different species. Plant ABC protein inventories obtained could be a valuable tool both for basic and applied studies. Indeed, interpolation of the putative role of gene functions can accelerate the discovering of new ABC superfamily members.

Figure 1

ABC protein subfamilies profile normalized on proteome size of each analysed species. k value: ratio between number of ABC protein for each subfamilies (ABCA; ABCB; ABCD; ABCE; ABCF; ABCG and ABCI) and total number of protein sequences for each species.

Figure 2

Phylogenetic tree of ATP-binding cassette subfamily A (ABCA) phylogenetic tree. The ABCA evolutionary history was inferred using the Maximum Likelihood method based on the Whelan and Goldman model and conducted in MEGA5. Bootstrap values > 70% are indicated above branches. The tree is drawn to scale, with branch lengths proportional to the number of substitutions per site. Identified clades are indicated by numbers and delineated by vertical lines. To facilitate the tree description, the clades were split in “clusters” (subgroups described in more detail).

Figure 3

Phylogenetic tree of ATP-binding cassette subfamily D (ABCD). A, Evolutionary analyses were performed as reported for ABCA transporter subfamily. B, Reconstruction of domain structure of ABCD proteins, refer to PFAM database.

Figure 4

Phylogenetic tree of ATP-binding cassette subfamily E (ABCE). Evolutionary analyses were performed as reported for ABCA transporter subfamily.

Figure 5

Phylogenetic tree of ATP-binding cassette subfamily F (ABCF). Evolutionary analyses were performed as reported for ABCA transporter subfamily.

Figure 6

Phylogenetic tree of PDR group of ATP-binding cassette subfamily G (ABCG _PDR ). Evolutionary analyses were performed as reported for ABCA transporter subfamily.

Figure 7

Distribution of ABC transporter genes across chromosomes for each plant species analysed.

Figure 8

Locus microsyntenic comparison between S. lycopersicum and S. tuberosum . A) The evolutionary history was inferred using the maximum likelihood method based on the general time reversible model in MEGA5. Bootstrap values >60% are indicated above branches. The tree is drawn to scale, with branch lengths measured in terms of the number of substitutions per site. B) MAUVE alignments of two genomic fragments of about 50 Kb of S. lycopersicum and S. tuberosum chromosome 5. Similar locally collinear blocks are labelled with the same colour and connected by fine lines. The boundaries of coloured blocks indicate the breakpoints of genome rearrangements.

Figure 9

Venn diagram of tomato expressed ABC genes annotated in root, leaf, bud, flower and 3cm_fruit tissues.