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Front Plant Sci
2012 Nov 29;3:263. doi: 10.3389/fpls.2012.00263.
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Molecular Evolution of Slow and Quick Anion Channels (SLACs and QUACs/ALMTs).
Dreyer I
,
Gomez-Porras JL
,
Riaño-Pachón DM
,
Hedrich R
,
Geiger D
.
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Electrophysiological analyses conducted about 25 years ago detected two types of anion channels in the plasma membrane of guard cells. One type of channel responds slowly to changes in membrane voltage while the other responds quickly. Consequently, they were named SLAC, for SLow Anion Channel, and QUAC, for QUick Anion Channel. Recently, genes SLAC1 and QUAC1/ALMT12, underlying the two different anion current components, could be identified in the model plant Arabidopsis thaliana. Expression of the gene products in Xenopus oocytes confirmed the quick and slow current kinetics. In this study we provide an overview on our current knowledge on slow and quick anion channels in plants and analyze the molecular evolution of ALMT/QUAC-like and SLAC-like channels. We discovered fingerprints that allow screening databases for these channel types and were able to identify 192 (177 non-redundant) SLAC-like and 422 (402 non-redundant) ALMT/QUAC-like proteins in the fully sequenced genomes of 32 plant species. Phylogenetic analyses provided new insights into the molecular evolution of these channel types. We also combined sequence alignment and clustering with predictions of protein features, leading to the identification of known conserved phosphorylation sites in SLAC1-like channels along with potential sites that have not been yet experimentally confirmed. Using a similar strategy to analyze the hydropathicity of ALMT/QUAC-like channels, we propose a modified topology with additional transmembrane regions that integrates structure and function of these membrane proteins. Our results suggest that cross-referencing phylogenetic analyses with position-specific protein properties and functional data could be a very powerful tool for genome research approaches in general.
Figure 1. Topology of SLAC-like channels. (A) SLAC-like channels show a topology of ten transmembrane regions and cytosolic N- and C-termini. (B) Three channel modules assemble into a trimeric structure. The pore-forming transmembrane regions (yellow, blue, orange, green, red) were used to generate Hidden Markov Models (HMMs) to screen for SLAC-like channels in plant genomes. (C) Sequence logos of the HMMs of the regions shown in (A) and (B). The crucial phenylalanine residue in the motif 5 (corresponding to Aratha-SLAC1-F450) is displayed in gray.
Figure 2. Topology of ALMT/QUAC-like channels. (A) Topology model developed by Motoda et al. (2007) for the channel TaALMT1. The red and the yellow regions were used to generate Hidden Markov Models (HMMs) to screen for ALMT/QUAC-like channels in plant genomes. Dotted ellipses indicate regions that differ most between the different clades of the ALMT/QUAC protein family. A detailed analysis of the C-terminal half is shown in Presentation S1 in Supplementary Material. (B) Sequence logos of the HMMs of the regions shown in (A). (C) Proposed modified topology for ALMT/QUAC-like channels. In addition to the model of Motoda et al. (2007), the C-terminal half is spanning twice the membrane resulting in extracellular and intracellular C-terminal regions. Furthermore, the larger N-terminal extension may contain another membrane spanning region (dotted). The positions of the highly conserved WEP-motif as well as the position of the phosphorylation site TaALMT1-S384 (yellow circle) are indicated.
Figure 3. Evolutionary relationships among ALMT/QUAC-like channels in land plants. There are seven clearly distinguished clades of ALMT/QUAC-like channels in extant land plants, i.e., clades 1, 2, 3, 4, 5, clade S.m. (S. moellendorffii specific) and clade P.p. (P. patens-specific). Each clade represents an independent group of orthologs. To elaborate the evolutionary relationship, reconciliation analyses have been carried out. The last recent common ancestor of all embryophytes had a single ALMT/QUAC-like channel. Several duplications resulted in the diversity observed today in angiosperms. A P. patens-specific group separated relatively early. Right after, gene duplication separated clades 2/5 from the others. A second duplication separated clade 3 (comprising QUAC1/ALMT12) from clades 1/4 followed by a third duplication that then separated clade 1 from clade 4. In comparison quite recently, another duplication event led to the separation of clades 2 and 5. Red “D”s at branching points indicate predicted gene duplications, numbers designate bootstrap values. For clarity, predicted events of gene losses are not shown.
Figure 4. Averaged Kyte and Doolittle plot of ALMT/QUAC-like channels. The hydropathicity score was determined separately for each channel and then assigned to the respective position in the global sequence alignment. Subsequently, for each clade and for all channels the average values at each position were determined. The plot identified clearly the known six transmembrane domains TM1-TM6 and, additionally, two further potential transmembrane domains in the C-terminal halves of the proteins (TM7 and TM8). For clarity, negative values were only displayed for the average over all clades.
Figure 5. Evolutionary relationships among SLAC-like channels in land plants. (A) Phylogenetic tree resulting from UPGMA analyses of 135 SLAC-like channels that did not show apparent deletions or wrong predictions of splicing sites. SLAC-like channels of angiosperms could be grouped into three-groups: SLAC1-group (blue), SLAH2/3-group (red) and SLAH1/4-group (green). (B) Summary of pairwise identities of proteins within the three different groups and between the groups. Data are mean ± SD. In brackets the value range is specified. (C) Reconciliation analysis of early duplication events in SLAC-like proteins. SLAC-like channels diversified into the three groups by two duplication events (red “D”s and circles). For clarity, predicted events of gene losses are not shown. (D) Phylogenetic analysis of representative SLAC-like and algae-Mae-like channels. Aratha-SLAH1 represents the SLAH1/4-group, Aratha-SLAH2 the SLAH2/3-group and Aratha-SLAC1 the SLAC1-group. For comparison the tellurite-resistance/C(4)-dicarboxylate transporter Haeinf-TehA from Haemophilus influenzae and the malic acid transport protein Mae1 from Schizosaccharomyces pombe were included in the analysis. (E) Reconciliation analysis of the tree in (D) confirmed the results already obtained with the UPGMA data set. For clarity, predicted events of gene losses are not shown.
Figure 6. Prediction of group-specifically conserved phosphorylation sites in SLAC-like channels. The Netphos 2.0 score for S, T, and Y residues was determined separately for each channel and then assigned to the respective position in the global sequence alignment. Subsequently, the average values at each position were determined for each clade. Conserved positions were identified using the following criteria: (i) conservation of >90% of the potential phosphorylation site within one group, (ii) minimum score of 0.6 for at least one of these residues, and (iii) minimum average score of 0.2 within one channel group. (A) Illustration of the localization of the identified conserved phosphorylation sites. Letters refer to detailed information in (B–G). (B–G) Sequence logos of the closer environment of the conserved putative phosphorylation sites (yellow). The positional information of the model channels Aratha-SLAC1, Aratha-SLAH3, and Aratha-SLAH1 is displayed explicitly. Values indicate mean ± SD of the score values. In case the mean score value was below 0.9, also the maximal value obtained for a single sequence is indicated. The displayed information is color coded (blue: SLAC1-group, red: SLAH2/3-group, green: SLAH1/4-group).
Figure 7. Bottleneck model for the evolution of SLAC-like channels. In the aquatic environment Tellurite-resistance/Dicarboxylate Transporters (TDTs) evolved into a huge variability. In algae transporters were identified that share features with malic acid transport proteins (MAEs). Closer relatives of the common ancestor of SLAC-like channels still need to be identified in Chlorophyta (algae C, algae D). Only one of these protein classes survived the transition from the aquatic to the land environment setting the starting point for the further evolution of SLAC-like channels.
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