Linking the evolution of plant transporters to their functions

In the past decade, an increasing number of plant genomes ranging from unicellular alga to trees have been completely sequenced. As the transport of water, nutrients, hormones, and metabolites in aquatic plants could differ from that of non-vascular, vascular or flowering plants, this rich resource has the potential to answer many of our most urgent questions: How did specific transporters evolve as early plants adapted to dry land? Does the evolution of transporters in monocot plants differ from that in dicots? What are the orthologs in food and energy crops of critical transporters characterized in model plants? Can we infer functions or membrane localization from phylogeny? Phylogenetic analyses of transport proteins will shed light on these questions and potentially reveal novel insights for future studies to understand the contribution of transporters in plant nutrition, stress tolerance, biomass production, as well as in signaling and development. We invited the plant biology community to participate in this effort as ∼5% of Arabidopsis thaliana (and probably other plant) genome encodes proteins with predicted transport roles. The Arabidopsis thaliana genome with 27 thousand protein-coding genes has over a 1000 genes classified as transporters, whereas the genomes of other flowering plants can be 2–7 times larger. In this topic issue, several authors have examined the evolutionary history and diversification of a range of transporters and these initial results are yielding surprising insights. Some transporter families can be traced to the simplest green plants, including unicellular Chlamydomonas reinhardtii (Chlorophyta). Thus H+-coupled antiporters like NHX (Chanroj et al., 2012), CAX, MHX, CCX (Emery et al., 2012), Sultr (Takahashi et al., 2012) and primary H+ and Ca2+ pumps, such as AHA, ACA, ECA (Pedersen et al., 2012) are highly conserved in all green plants. In some cases, the gene family has diversified, for example, from 2 AHA genes in early land plant Physcomitrella patens to 11 genes in the flowering plant A. thaliana, indicating a need to regulate the proton motive force in specialized organs or cell types. In contrast, homologs of other transporter families in flowering plants were traced to a Charophyte, but not found in Chlorophyta. This history suggests that CHX co-transporters of K+ (Chanroj et al.), LHT amino acid transporters (Tegeder and Ward, 2012) and SUT sucrose transporter (Reinders et al., 2012) had origins in an aquatic Charophyte, and further supports Charaphytes as basal to land plants. The increase in sibling genes within each family through gene duplication and diversification, can be attributed in part to innovations in vascular tissue development (LHT in phloem) and in sexual reproduction (LHT in pollen) on land. Strikingly, CHX genes have diversified in pollen especially in dicots, suggesting roles in the delivery of sperms in pollen tubes to distant ovules. Curiously, the purine uptake permease, PUP family exists in a vascular early land plant, Selaginella moellendorfii, but not in a non-vascular moss (Physcomitrella patens) (Jelesko, 2012). It is possible that PUP genes have a role in the transport of secondary metabolites for defense and/or reproductive success in vascular plants. Early land plants, such as moss and Selaginella, possess MIP homologs similar to PIP and TIP water channels (Anderberg et al., 2012), though it is not yet clear whether aquatic Charophytes need such proteins to transport water. Chlorophytes possess MIP-like homologs though their substrate(s) may be small uncharged molecules other than water. A striking feature is that three branches of the AtNHX family correspond to Na+(K+)/H+ antiporters associated with three distinct subcellular locations (plasma membrane, trans Golgi network and vacuolar membrane) in Arabidopsis (Chanroj et al., 2012). Though not all subclades of families are separated according to location, it does illustrate that finding orthologs from another species could aid in predicting function as well as membrane association (e.g., Reinders et al., 2012; Takahashi et al., 2012). Facchinelli and Weber (2011) reviewed the evolutionary history of select metabolite transporters localized at the inner envelope of plastids. Phylogenetic studies are showing that Arabidopsis thaliana contributes 58% of the metabolite transporters vs. 12% from the endosymbiont cyanobacterium. The study illustrates that connecting plastid metabolism with that of the host cell is driving the evolution of metabolite transporters at the inner envelope. Authors also examine differences in phosphate transporters of photosynthetically-active plastids vs. heterotrophic plastids in non-green tissues. ATP/ADP exchangers localized to the inner envelope membrane of plastids are thought to provide ATP for reactions in heterotrophic plastids, or photosynthetic plastids during the night. However recent evidence for ATP/ADP antiporters on thylakoid membranes of Arabidopsis was surprising. Spetea et al. (2012) have traced the history of thylakoid ATP/ADP antiporters (TAAC) in plants and phylogenetic evidence suggests they arose once before the divergence of Chlorophyta and Streptophyta. These transporters are thought to supply ATP into the lumen for the biosynthesis and turnover of photosynthetic complexes. Haferkamp and Schmitz-Esser (2012) re-analyzed the evolution of the Arabidopsis mitochondrial carrier family (MCF) catalyzing the transport of various substrates in mitochondria and other organelles. They found that various MCFs from Arabidopsis,