Vesicle Transport in Plants: A Revised Phylogeny of SNARE Proteins

Abstract

Communication systems within and between plant cells involve the transfer of ions and molecules between compartments, and are essential for development and responses to biotic and abiotic stresses. This in turn requires the regulated movement and fusion of membrane systems with their associated cargo. Recent advances in genomics has provided new resources with which to investigate the evolutionary relationships between membrane proteins across plant species. Members of the soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) are known to play important roles in vesicle trafficking across plant, animal and microbial species. Using recent public expression and transcriptomic data from 9 representative green plants, we investigated the evolution of the SNARE classes and linked protein changes to functional specialization (expression patterns). We identified an additional 3 putative SNARE genes in the model plant Arabidopsis. We found that all SNARE classes have expanded in number to a greater or lesser degree alongside the evolution of multicellularity, and that within-species expansions are also common. These gene expansions appear to be associated with the accumulation of amino acid changes and with sub-functionalization of SNARE family members to different tissues. These results provide an insight into SNARE protein evolution and functional specialization. The work provides a platform for hypothesis-building and future research into the precise functions of these proteins in plant development and responses to the environment.

Keywords: Arabidopsis thaliana; SNAREs; Viridiplantae; membrane fusion; phylogenetics; vesicle trafficking.

Figure 1.

The vesicle trafficking pathway. Adapted from Cai et al.

Figure 2.

Maximum likelihood trees of all 5 classes of SNARE genes in 9 different species representing all green plants. Branch tips have been labelled according to UniProt gene name and 5 letter species abbreviation, except for Arabidopsis where the gene name has been provided instead. Branches and tip labels have been coloured according to species: Arabidopsis thaliana (ARATH); Brachypodium distachyon (BRADI); Chlamydomonas reinhardtii (CHLRE); Oryza sativa (ORYSJ); Physcomitrella patens (PHYPA); Populus trichocarpa (POPTR); Sorghum bicolor (SORBI); Glycine max (SOYBN); Vitis vinifera (VITVI). Clades representing a predominance of 1 Arabidopsis gene type have been highlighted with different colours. The rings of bands correspond to protein domains identified in each gene. Black domains correspond to domains annotated as SNAREs and grey bands correspond to other domains. Domains are ordered from the centre to the edge of the circle approximating their N to C terminal order.

Figure 3.

Expression heat map of SNARE genes in different organs and developmental stages of Arabidopsis. Expression levels of each gene across samples were scaled linearly to have a mean of 0 and a standard deviation of 1. Samples were numbered as in Supplemental Table 5.

Figure 4.

Relationships between (A, left) genetic distance versus expression distances, and (B, right) Dn/Ds ratios versus expression distances across SNARE gene classes in Arabidopsis. Filled diamonds show mean values for SNARE gene classes. Dotted bars show standard deviations. Gene class names and the number of values assessed are plotted to the left and right of each point, respectively.