Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants

Abstract

The green plant lineage is the second major multicellular expansion among the eukaryotes, arising from unicellular ancestors to produce the incredible diversity of morphologies and habitats observed today. In the unicellular ancestors, secretion of material through the endomembrane system was the major mechanism for interacting and shaping the external environment. In a multicellular organism, the external environment can be made of other cells, some of which may have vastly different developmental fates, or be part of different tissues or organs. In this context, a given cell must find ways to organize its secretory pathway at a level beyond that of the unicellular ancestor. Recently, sequence information from many green plants have become available, allowing an examination of the genomes for the machinery involved in the secretory pathway. In this work, the SNARE proteins of several green plants have been identified. While little increase in gene number was seen in the SNAREs of the early secretory system, many new SNARE genes and gene families have appeared in the multicellular green plants with respect to the unicellular plants, suggesting that this increase in the number of SNARE genes may have some relation to the rise of multicellularity in green plants.

Figure 1.

SNARE genes in several eukaryotic genomes. SNAREs are divided into three basic modules based upon the site of action: ER/Golgi, TGN/endosomal (including vacuole), and secretory/PM. Among the unicellular eukaryotes, this division is based upon homology to SNAREs with known functions and does not exclude multiple roles for some proteins (especially in Cyanidioschyzon where the Qb, Qc, and R roles in secretion must be played by proteins from other modules). SNARE genes are indicated by individual boxes with the type of SNARE labeled with a color (Qa, orange; Qb, purple; Qb + Qc, violet; Qc, red; R, blue). Each box indicates a single genomic locus and does not include alternatively spliced isoforms of SNARE genes that are common in some lineages (especially vertebrates). Lineages are specified to the left with arrows indicating relationships among the major groups (Adl et al., 2005): Green, Green plants; embryo., embryophytes (land plants); chloro., chlorophytes (green algae); red, red algae; hetero., heterokonts (brown algae, diatoms, oomycetes); amoeba, amoebozoa (slime molds); fungi; animals. Species abbreviations: Arath, Arabidopsis; Poptr, P. trichocarpa; Orysa, O. sativa; Phypa, P. patens; Chlre, C. reinhardtii; Volca, V. carteri; Ostta, O. tauri; Ostlu, O. lucimarinus; Cyame, Cyanidioschyzon merolae; Thaps, Thalassiosira pseudonana; Phatr, Phaeodactylum tricornutum; Physo, Phytophthora sojae; Phyra, Phytophthora ramorum; Dicdi, Dictyostelium discoideum; Sacce, S. cerevisiae; Schpo, Schizosaccharomyces pombe; Caeel, Caenorhabditis elegans; Drome, Drosophila melanogaster; Homsa, Homo sapiens.

Figure 2.

Clustering of SNARE gene families among eukaryotic groups. SNARE-encoding genes from several fully sequenced eukaryotes are indicated by boxes as described in Figure 1. Hatched boxes in the row for pine (Pinta, Pinus taeda) indicate that these genes are derived from searches of the EST database only and likely represent an underestimate of the number of SNARE genes in this organism. Each vertical stack of boxes indicates a particular related group of SNARE proteins (see Supplemental Figs. S1–S6) with the names given to the plant groups across the top and to the vertebrate groups across the bottom. See Figure 1 for abbreviations and notations. See Supplemental Table S1 for a list of individual genes for each organism.

Figure 3.

Qa-SNAREs of the PM have greatly expanded in the land plants. Full-length protein sequences of the Qa-PM orthologs from various organisms were aligned by ClustalW, distances were estimated with a neighbor-joining algorithm and visualized in a phylogram. The tree was rooted using the Qa-PM SNAREs of heterokonts. Bootstrap support is indicated to the left of branches. The clades and subclades of land plant syntaxins are also indicated as described in the text (also see Supplemental Fig. S7). See Figure 1 for species abbreviations.

Figure 4.

R-SNAREs of the VAMP7 group have greatly expanded in the land plants. Full-length protein sequences of the R-VAMP7 orthologs from various organisms were aligned by ClustalW, distances were estimated with a neighbor-joining algorithm and visualized in a phylogram (top). The tree was rooted using the VAMP7 SNAREs from heterokonts. Bootstrap support is indicated to the left of branches. The ubiquitous VAMP71 and the green-plant-specific VAMP72 clades are indicated at right, along with the subclades of the land plants (see text and Supplemental Fig. S8). See Figure 1 for species abbreviations.

Figure 5.

Hypothetical expansion of secretory SNARE gene families in the green plants. Relevant taxa of green plants are indicated with boxes representing the hypothesized state of the Qa-SYP1 and R-VAMP7 gene families at the point in green plant evolution indicated by the arrow. New gene families are indicated by indented names with arrows indicating the hypothetical descent of that gene from a related gene family (see text and Supplemental Figs. S7 and S8 for more details).