Host origin of plastid solute transporters in the first photosynthetic eukaryotes
- Heather M Tyra†1,
- Marc Linka†2,
- Andreas PM Weber2, 3Email author and
- Debashish Bhattacharya1Email author
© Tyra et al.; licensee BioMed Central Ltd. 2007
Received: 22 June 2007
Accepted: 5 October 2007
Published: 05 October 2007
It is generally accepted that a single primary endosymbiosis in the Plantae (red, green (including land plants), and glaucophyte algae) common ancestor gave rise to the ancestral photosynthetic organelle (plastid). Plastid establishment necessitated many steps, including the transfer and activation of endosymbiont genes that were relocated to the nuclear genome of the 'host' followed by import of the encoded proteins into the organelle. These innovations are, however, highly complex and could not have driven the initial formation of the endosymbiosis. We postulate that the re-targeting of existing host solute transporters to the plastid fore-runner was critical for the early success of the primary endosymbiosis, allowing the host to harvest endosymbiont primary production.
We tested this model of transporter evolution by conducting a comprehensive analysis of the plastid permeome in Arabidopsis thaliana. Of 137 well-annotated transporter proteins that were initially considered, 83 that are broadly distributed in Plantae were submitted to phylogenetic analysis. Consistent with our hypothesis, we find that 58% of Arabidopsis transporters, including all carbohydrate transporters, are of host origin, whereas only 12% arose from the cyanobacterial endosymbiont. Four transporter genes are derived from a Chlamydia-like source, suggesting that establishment of the primary plastid likely involved contributions from at least two prokaryotic sources.
Our results indicate that the existing plastid solute transport system shared by Plantae is derived primarily from host genes. Important contributions also came from the cyanobacterial endosymbiont and Chlamydia-like bacteria likely co-resident in the first algae.
Plastids in eukaryotes that contain chlorophyll are capable of carrying out photosynthesis, a process that converts light energy, carbon dioxide, and water into organic compounds. The evolutionary history of this organelle unfolded over a billion years ago when a previously non-photosynthetic protist engulfed and maintained a free-living cyanobacterium in its cytoplasm . It is hard to over-state the importance of this ancient and extraordinarily rare primary endosymbiosis because plastids allowed the evolution of algae and the plants that form the base of the food chain for many ecosystems on Earth. Current data suggest that the primary endosymbiosis occurred once in the common ancestor of the red, green (including land plants), and glaucophyte algae, the Plantae [2–4], with the original plastid and the nuclear-encoded machinery for running the organelle spreading in subsequent cell captures to other branches of the eukaryotic tree [5–7]. The only other known case of a potential bona fide cyanobacterial primary endosymbiosis occurred relatively recently in the thecate amoeba Paulinella chromatophora [8, 9].
The gradualist view of evolution through mutation-selection suggests that it would have taken millions of years for the captured prokaryote to become fully integrated into the 'host' eukaryote, ultimately becoming the site not only for carbon fixation but also for other complex functions, such as lipid, isoprenoid, and amino acid biosynthesis . These processes were associated with the migration of much of the cyanobacterial genome to the host nucleus and development of the complex protein import system that are key shared features among all canonical plastids [3, 11, 12]. A remarkable exception to the view that endosymbiosis was a gradual process of integration is offered by the katablepharid protist 'Hatena', which undergoes large-scale morphological changes following the engulfment of a green alga .
Regardless of whether the ancient primary endosymbiosis fostered an accelerated rate of morphological evolution in the Plantae ancestor or whether general cell morphology was unchanged as in the Paulinella example , one thing is clear - in the absence of rapid benefits to the host it is unlikely that the endosymbiosis would long have been sustained. Given the need for short-term survival, a key feature of early success for the endosymbiosis must have been the integration of the metabolism of the two cells. The key to this process would have been solute transporters that regulate the flux of metabolites (for example, ATP, phosphate, sugars and sugar phosphates, metal ions, and other important ions) across the organelle membranes. Controlled exchange in response to environmental factors such as changes in light intensity and trace metal availability [15–17] is decisive because the unregulated flux of metabolites would have had detrimental effects and, thereby, lowered the evolutionary fitness of the endosymbiosis. A complex system of solute transporters is in place today in extant plastids that provides the link between this organelle and the surrounding cytosol [18–20]. Here we focus on the evolutionary history of these plastid metabolite transporters to infer early events in plastid evolution.
We make two assumptions in this study. First, a system of metabolite transporters was a critical and early development in plastid evolution to supply the endosymbiont with essential nutrients and to enable the host to reap immediate benefit from photosynthetic primary production. It is unclear why the cyanobacterium that was destined to become the plastid escaped digestion in the host but this scenario has also played out in 'Hatena' and in Paulinella. Second, whereas the genome of the previously free-living cyanobacterium encoded all the transport systems required for the uptake of essential inorganic nutrients, it most likely did not harbor genes encoding transporters for the export of organic solutes to the host - this would have served no obvious pre-existing purpose in the prokaryote. Precisely how the plastid solute transport system was established is unknown. One possible model involves a primarily cyanobacterial origin, in which the plastid continued to utilize its own original cyanobacterial solute transporters with their evolution over time into proteins that perform most or all currently known plastid permeome functions. An alternative model involves a host-driven solute transport system, likely derived from the vacuolar envelope that initially surrounded the endosymbiont after its engulfment . And finally, both of the new partners could have contributed proteins equally to this machinery, resulting in a chimeric system composed of the most beneficial combination possible of prokaryotic and eukaryotic transporters. To determine which of these competing hypotheses best explains plastid transporter evolution, we undertook an initial bioinformatics analysis of 137 Arabidopsis thaliana solute transporters and then a detailed phylogenetic analysis of a subset of 83 conserved proteins that included available data from other Plantae. The Arabidopsis transporters are either predicted or have been shown to be chloroplast targeted and are ideal for tracking plastid permeome evolution. Using these data we demonstrate that over one-half of Plantae plastid targeted transporters are putatively of host origin whereas less than a quarter arose from the cyanobacterial endosymbiont. This suggests that the lasting contribution to the Plantae host-endosymbiont relationship with regard to the plastid solute transport system was made primarily by host genes. We also find evidence for the origin of four transporter genes or gene families from a Chlamydia-like source. This latter result raises the possibility that establishment of the ancient primary plastid may have involved contributions from at least two prokaryotic sources, perhaps explaining its singular nature. This hypothesis received substantial support from the recent finding of at least 21 genes of Chlamydia-like origin in the nuclear genome of the extremophilic red alga Cyanidioschyzon merolae .
Results and discussions
Distribution of transporters within Plantae
Arabidopsis solute transporters
Ligand-effect modulator 3 (LEM3) family
Glucose-6-phosphate/phosphate translocator 2 (GPT2)
Transporter associated with antigen processing protein 1 (AtTAP1)
Ligand-effect modulator 3 (LEM3) family
Cation efflux family protein
Na+-dependent inorganic phosphate cotransporter
Na+-dependent inorganic phosphate cotransporter
Multi antimicrobial extrusion (MATE Efflux) protein
Amino acid transporter
Phosphoenolpyruvate/phosphate translocator 2 (PPT2)
Ligand-effect modulator 3 LEM3 family
Cyclic nucleotide-binding transporter 2
Cyclic nucleotide-binding transporter 1
Anion transporter 2 (ANTR2)
Major intrinsic family protein
Adenine nucleotide uniporter
Arabidopsis thaliana K+ rectifying channel 1 (ATKC1)
Multi antimicrobial extrusion (MATE Efflux) protein
S-adenosylmethionine carrier 2 (SAMT)
Amino acid permease
Amino acid permease
Mitochondrial phosphate transporter
Glucose-6-phosphate transporter 1 (XPT)
ABC transporter (White)
CorA-like magnesium transporter
Phosphoenolpyruvate/phosphate translocator (PPT1)
Mitochondrial substrate carrier family
Triose phosphate translocator (TPT)
ABC transporter (White)
Glucose-6-phosphate/phosphate transporter 1(GPT1)
Integral membrane family protein
Trigalactosyldiacylglycerol 1, TGD1
Integral membrane family protein
Folate monoglutamate transporter, FT
Metal-transporting P-type ATPase (PAA1)
Adenine nucleotide translocase 2 (AtNTT2)
Adenine nucleotide translocase 1 (AtNTT1)
Low affinity phosphate transporter (PHT2;1)
Heavy metal ATPase HMA1
Dicarboxylate translocator 1 (DiT1)
Dicarboxylate translocator 2.2 (DiT2.2)
Dicarboxylate translocator 2.1 (DiT2.1)
Bile acid:sodium symporter
Expressed protein | (Putative small multi-drug export)
Enhanced disease susceptibility protein
Bile acid:sodium symporter
Bile acid:sodium symporter
1-Acylglycerol-3-phosphate O-acyltransferase (ATS2)
Cytosine/purines, uracil, thiamine, allantoin family permease
Integral membrane HPP family protein
Maltose transporter (MEX1)
Most proteins of the plastid envelope permeome are host-derived
The cyanobacterial contribution
In summary, it is surprising that bacteria not putatively involved in the endosymbiosis contributed 8% of the transporters that we have identified. When one considers the functions of these transporters, the chlamydial contribution becomes more important. HMA1 increases copper and/or zinc transport into the plastid under conditions of high light, facilitating the production of copper/zinc superoxide dismutase (CuZnSOD), which protects the plant from superoxide radicals produced under high light conditions [42, 43]. PHT2;1, a phosphate transporter, controls phosphate allocation under conditions of phosphate-starvation . The DiT transporters are involved in assimilating nitrogen and recovering carbon lost to photorespiration, a process that is initiated by the oxygenation reaction of Rubisco that primarily occurs under conditions when a high O2:CO2 ratio is present in the vicinity of Rubisco. Mutants lacking these transporters are unable to survive in ambient CO2 concentrations [17, 45, 46]. Finally, the AtNTT1 and AtNTT2 transporters are required for ATP import into the plastid during the dark (that is, in the absence of photosynthetic ATP production), particularly during lipid and chlorophyll biosynthesis. Although AtNTT2 mutants are still capable of producing lipids, indicating that the plastid has an alternative method for generating the ATP required for lipid biosynthesis, the production is significantly reduced and mutant plants have a sharply reduced growth rate . Arabidopsis mutants deficient in both AtNTT1 and AtNTT2 develop necrotic lesions when grown under short days, accumulate H2O2, and, strikingly, show constitutive expression of CuZnSOD2 and ascorbate peroxidase . The phenotype of the mutant was linked to reduced magnesium chelatase activity and it was concluded that ATP import into plastids in the dark is required for chlorophyll biosynthesis and for preventing photooxidative damage . The import of ATP into plastids in the dark is thus clearly a case in which the endosymbiont benefits from host metabolism. The ancient origin of these transporters in the tree of photosynthetic eukaryotes (Figure 4a) is indicative of an essential role of this uptake system in the formation of the endosymbiosis. With the exception of the DiT translocators, each of these transporters appear to perform somewhat redundant functions (that is, copper and phosphate transport) but in a way that permits the plant to adapt to stresses involved in life on the land (that is, high light and O2 levels or low phosphate availability). This may explain why the genes encoding these four plastid transporters have been retained in the Arabidopsis genome.
How the 'Chlamydia-like' genes entered into the Plantae ancestor is unclear but it is possible that both the cyanobacterial endosymbiont and chlamydial parasites may have co-existed in the cell. Many environmental Chlamydia are known today that are broadly distributed in animals and protists . The co-existence of these two distinct prokaryotes may have provided the genetic 'toolkit' to make permanent the endosymbiosis with gene transfer from each cell providing essential functions for endosymbiont utilization. An alternative explanation is that the cyanobacterial endosymbiont was itself highly chimeric (that is, the 'fluid chromosome model')  and contained genes of chlamydial origin that had been gathered through HGT. Although possible, this scenario seems less plausible because it invokes, for example, the presence of an ADP/ATP translocator (a gene typical for 'energy parasites' such as Rickettsiae) in the genome of an oxygenic photosynthetic cell that is unlikely to encounter high concentrations of ATP in the surrounding environment; that is, it is absent from all studied cyanobacteria. Additional discussion of these issues can be found in Huang and Gogarten .
'Other' and 'Plantae-specific' transporters
Of the remaining transporters, four fell in the 'Plantae-specific' category because they lacked identifiable homologs outside of this supergroup and may simply be too divergent to determine their origin. This includes At5g24690 (Figure 5b, a hypothetical expressed protein) and the plastidic maltose exporter MEX1. The latter is required for export of maltose resulting from starch breakdown from plastids at night in green plants (Figure S5 in Additional data file 1). Storage of starch inside the chloroplast is exclusively found in the green linage. Therefore, MEX1 has likely co-evolved with plastid-based starch biosynthesis and breakdown since it can be detected only in members of the Viridiplantae with one gene found in the dinoflagellate Karlodinium micrum, which, as described above for Dit2, likely has resulted from a HGT.
Here we determined the phylogeny of 83 Arabidopsis plastid solute transporters to determine whether they are of endosymbiotic origin from the captured cyanobacterium, of host origin, or of a 'mixed' origin from both of these sources. Our analysis has afforded a rare look at early, critical events in primary plastid evolution and support the notion that integration of plastid-host metabolism was primarily driven by host-derived transporters with important contributions coming from the cyanobacterial endosymbiont and Chlamydia-like bacteria. Another class of proteins of currently unknown origin included plant specific transporters such as MEX1. Despite the power of our comparative approach, our work has some important limitations. One is that because we used the Arabidopsis transporter set, we most certainly have missed a number of Plantae transporters that are specific to red or green algae and have been lost from the Arabidopsis genome. In addition, we lack significant data from glaucophytes, but the upcoming Cyanophora paradoxa (glaucophyte) nuclear genome sequence  will allow us to incorporate this lineage into future inferences about transporter evolution. It is reasonable to assume, however, given the wealth of data supporting Plantae monophyly [2–4, 7], that our inferences regarding the red and green lineages also apply to their glaucophyte sisters. Despite these limitations and the fact that phylogenetic signal is imperfectly maintained over a billion years of evolution, our comprehensive analysis of the chloroplast solute transport system will likely hold up and can be further tested as other genome sequences become available.
Materials and methods
Initial transporter analyses
As a starting point for the compilation of a conservative set of predicted or confirmed plastid envelope membrane transporters, we used a previously published list of 137 plastid-targeted membrane proteins that was based on predicted plastid localization and classification by the transporter classification system . This list was manually curated to remove proteins from the list if published evidence indicated that they were localized to a cellular location other than chloroplasts, if they represented membrane-bound enzymes, or if they were annotated as components of the TIC/TOC protein import apparatus, the photosynthetic machinery of the thylakoid membrane, or the Sec or Tat protein targeting pathways. This curated list of candidate genes was updated and amended with recently published chloroplast envelope membrane transporters, such as AtFOLT1, a plastid localized transporter belonging to the mitochondrial carrier family that does not contain a plastid targeting signal  and was thus not included in previous lists. The final list contained 83 A. thaliana predicted or confirmed chloroplast solute transporters.
The sequence for each protein was obtained from The Arabidopsis Information Resource website . These protein sequences were used as queries in blastp and tblastn searches of the NCBI Database , the plant and algal genomes available through the Joint Genome Institute , the Cyanidioschyzon merolae Genome Project website , the Galdieria sulphuraria Genome Project website , and Dragonblast V2.1 (SE Ruemmele, unpublished data), a web based database in the DB lab that contains EST datasets for several chromalveolates, Plantae, excavates, Rhizaria, and Amoebozoa. We used the predicted protein sequences for the following species for our analysis whenever available: Arabidopsis thaliana, Oryza sativa, Physcomitrella patens, Chlamydomonas reinhardtii, Ostreococcus tauri, Ostreococcus lucimarinus, Cyanidioschyzon merolae, Galdieria sulphuraria, Cyanophora paradoxa, Dictyostelium discoideum, Strongylocentrotus purpuratus, Xenopus laevis, Danio rerio, Mus musculus, Canis familiaris, and Homo sapiens. In addition, we included at least one insect, three fungal species, and a broad range of Bacteria and Archaea in our analysis. The BLAST searches used an e-value cut-off < 10-5. If a translated EST sequence was not available, the nucleotide sequence was translated over six frames using the ExPASy translate tool . The resulting protein sequences were used in a BLAST search against the NCBI protein database to ensure the correct translation was obtained.
We used the ClustalW feature included with BioEdit V18.104.22.168 to generate protein alignments . Alignments were visually inspected and manually corrected if necessary. Trees were generated under maximum likelihood using PHYML V2.4.4 utilizing the WAG model of amino acid substitution and estimating both the proportion of invariable sites and the alpha parameter (that is, WAG + I + Γ). We performed non-parametric bootstrap analysis with 100 replicates for each PHYML analysis. The resulting trees were analyzed to determine the origin of the transporter in Arabidopsis and other Plantae.
The designation of gene origin was done as follows. When the Plantae solute transporter formed a well-supported (usually > 70% bootstrap support) monophyletic group with homologs in opisthokonts (that is, animals and fungi) and secondarily with other eukaryotes such as excavates and chromalveolates (if present), then it was classified as having a 'Host' origin. Under this scheme, no bacterial sequences interrupted the eukaryotic domain. 'Cyanobacterial' or 'Chlamydia-like' origin was inferred if the Plantae sequence formed a monophyletic group with protein sequences from either of these lineages with strong bootstrap support. Other bacterial or eukaryotic sequences could (not necessarily) be in these trees but there had to be a robust separation of the Plantae + cyanobacteria or Chlamydia-like clade from all other homologs. We had two other categories of gene origin that likely reflected a lack of phylogenetic resolution or pervasive HGT among taxa that defied a clear inference of origin. The first was the 'Other' category in which the Plantae transporter formed a well-supported monophyletic clade but its position relative to available bacterial data was unresolved, thereby not allowing us to identify the donor taxon. The second, 'Plantae-specific', was for transporters that had no significant hits to sequences in GenBank or other databases and appeared to be limited to the Plantae. All of the transporter PHYML bootstrap trees are available in Additional data file 1. The protein alignments are available in the download section of the Bhattacharya Lab website .
Detailed phylogenetic analyses
For eight representative transporters from the five categories described above we inferred a maximum likelihood phylogeny using RAxML (RAxML-VI-HPC, v2.2.1)  and the WAG + Γ evolutionary model. The specific transporters were: 'Host' - At4g39460 (SAMT, S-adenosylmethionine carrier 1 protein, 236 amino acids), At5g66380 (AtFOLT1, Arabidopsis thaliana folate transporter 1, 268 amino acids); 'Cyanobacterial' - At1g19800 (TGD1, trigalactosyldiacylglycerol 1, lipid transporter, 234 amino acids), At5g64940 (ABC transporter protein, 487 amino acids); 'Chlamydia-like' - At1g15500 (chloroplast ADP, ATP carrier protein 2, 436 amino acids), At4g37270 (HMA1, copper exporting ATPase, 444 amino acids); 'Other' - At1g32080 (putative membrane protein, 211 amino acids); 'Plantae-specific' - At5g24690 (hypothetical expressed protein, 274 amino acids). These detailed analyses used a random starting tree (one round of taxon addition) and the rapid hill-climbing algorithm (that is, option -f d in RAxML). To generate bootstrap values for these phylogenies, we used RAxML with the same settings and 100 replications. In addition, we used Bayesian inference (MrBayes V3.0b4)  with each of the eight data sets using the WAG + I + Γ model to calculate posterior probabilities for nodes in the RAxML trees. Metropolis-coupled Markov chain Monte Carlo from a random starting tree was used in this analysis with two independent runs (that is, nrun = 2 command) and 1 cold and 3 heated chains. The Bayesian analyses were run for two million generations each with trees sampled every 100th generation. To increase the probability of chain convergence, we sampled trees after the standard deviation values of the two runs were < 0.01 to calculate the posterior probabilities. We also ran the Bayesian analysis for the remaining two putative 'Chlamydia-like' genes in Plantae (dicarboxylate translocators DiT1, DiT2.1, and DiT2.2, and the phosphate transporter PHT2;1) to assess the topologies. We incorporated a representative diversity of available sequences in all of these trees.
Additional data files
The following additional data are available with the online version of this paper. Additional data file 1 shows trees of all remaining plastid transporters analyzed in this study
A. thaliana folate transporter
A. thaliana ADP/ATP translocase
expressed sequence tag
horizontal gene transfer
heavy metal ATPase
This work was supported by NSF Award EF-0332882 to APMW and NIH Award R01 ES013679-01 and NSF Award EF-0431117 to DB.
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