Host origin of plastid solute transporters in the first photosynthetic eukaryotes

Abstract

Background: 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.

Results: 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.

Conclusion: 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.

Figure 1

Origin of plastid targeted solute transporters in Plantae. (a) Gene distribution among Plantae and gene origin for 63 distinct transporters considered in this study. (b) Summary pie-charts showing the origin of all the 83 transporters (top chart) and the 63 distinct genes (lower chart) considered in this study.

Figure 2

Plastid targeted solute transporters of putative 'Host' origin in Plantae. These are RAxML trees with the numbers above the branches inferred from a RAxML bootstrap analysis and the thick branches showing significant (P > 0.95) support from a Bayesian phylogenetic inference. Only bootstrap values ≥ 60% are shown. Branch lengths are proportional to the number of substitutions per site (see scale bars). The filled magenta circle shows the node that unites the Plantae taxa within the eukaryotic domain. The different algal groups are shown in different text colors: red for red algae, green for green algae and land plants, and brown for chromalveolates. The inclusion of chromalveolates within the Plantae is believed to reflect horizontal or endosymbiotic gene transfer events (for example, [50]). The two transporters are: (a) SAMT, S-adenosylmethionine carrier 1 protein; and (b) AtFOLT1, Arabidopsis thaliana folate transporter 1. The name of the A. thaliana solute transporter used for the query is indicated for both trees shown in this figure.

Figure 3

Plastid targeted solute transporters of putative 'Cyanobacterial' (that is, plastid endosymbiont) origin in Plantae. For details of tree building see Figure 2. The filled magenta circle shows the node that unites the Plantae taxa as sister to cyanobacteria. The different photosynthetic groups are shown in different text colors: blue for cyanobacteria, red for red algae, green for green algae and land plants, and brown for chromalveolates. The inclusion of chromalveolates or Euglenozoa (Eugl.) within the Plantae is believed to reflect horizontal or endosymbiotic gene transfer events (for example, [50]). The two transporters are: (a) TGD1, trigalactosyldiacylglycerol 1, lipid transporter; and (b) ABC1-family transporter protein. The name of the A. thaliana solute transporter used for the query is indicated for both trees shown in this figure.

Figure 4

Plastid targeted solute transporters of putative 'Chlamydia-like' origin in Plantae. For details of tree building see Figure 2. The filled magenta circle shows the node that unites chlamydial taxa with plastid targeted Plantae transporters. The different photosynthetic groups are shown in different text colors: blue for cyanobacteria, red for red algae, green for green algae and land plants, magenta for glaucophytes, and brown for chromalveolates. The inclusion of chromalveolates within the Plantae is believed to reflect horizontal or endosymbiotic gene transfer events (for example, [50]). The two transporters are: (a) ADP/ATP translocater; and (b) heavy metal ATPase (HMA1) copper transporter. The name of the A. thaliana solute transporter used for the query is indicated for both trees shown in this figure.

Figure 5

Plastid targeted solute transporters of 'Other' or 'Plantae-specific' origin in Plantae. For details of tree building see Figure 2. The filled magenta circle shows the node that unites the Plantae taxa. The different algal groups are shown in different text colors: red for red algae, green for green algae and land plants, magenta for glaucophytes, and brown for chromalveolates. The inclusion of chromalveolates within the Plantae is believed to reflect horizontal or endosymbiotic gene transfer events (for example, [50]). The different transporters are: (a) transporter in the 'Other' category: putative membrane protein; and (b) transporter in the 'Plantae-specific' category: hypothetical expressed protein. The name of the A. thaliana solute transporter used for the query is indicated for both trees shown in this figure.