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Function and evolution of channels and transporters in photosynthetic membranes.

Pfeil BE, Schoefs B, Spetea C - Cell. Mol. Life Sci. (2013)

Bottom Line: PCC 6803.Additionally, the shift from a non-thylakoid to a thylakoid location appears to have occurred at different times for different transport proteins.Some of the proteins recruited to serve in the thylakoid may have been the result of the increased specialization of its pigment-protein composition and organization in green plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological and Environmental Sciences, University of Gothenburg, 40530, Gothenburg, Sweden.

ABSTRACT
Chloroplasts from land plants and algae originated from an endosymbiotic event, most likely involving an ancestral photoautotrophic prokaryote related to cyanobacteria. Both chloroplasts and cyanobacteria have thylakoid membranes, harboring pigment-protein complexes that perform the light-dependent reactions of oxygenic photosynthesis. The composition, function and regulation of these complexes have thus far been the major topics in thylakoid membrane research. For many decades, we have also accumulated biochemical and electrophysiological evidence for the existence of solute transthylakoid transport activities that affect photosynthesis. However, research dedicated to molecular identification of the responsible proteins has only recently emerged with the explosion of genomic information. Here we review the current knowledge about channels and transporters from the thylakoid membrane of Arabidopsis thaliana and of the cyanobacterium Synechocystis sp. PCC 6803. No homologues of these proteins have been characterized in algae, although similar sequences could be recognized in many of the available sequenced genomes. Based on phylogenetic analyses, we hypothesize a host origin for most of the so far identified Arabidopsis thylakoid channels and transporters. Additionally, the shift from a non-thylakoid to a thylakoid location appears to have occurred at different times for different transport proteins. We propose that closer control of and provision for the thylakoid by products of the host genome has been an ongoing process, rather than a one-step event. Some of the proteins recruited to serve in the thylakoid may have been the result of the increased specialization of its pigment-protein composition and organization in green plants.

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Hypothesis for the evolutionary pathways of thylakoid transporters. (Left panel) Symbiont origin proteins in Archaeplastida (green plants, red algae and lineages that have derived their chloroplasts from red algae) are expected to be more closely related to cyanobacterial lineages than to non-Archaeplastida, such as animals and fungi. (Right panel) If the proteins have a host origin, then a closer relationship between Archaeplastida lineages and other eukaryotes, such as animals and fungi, is expected. In a symbiont origin phylogeny, brown algae derive these proteins via red algae, and are expected to be more closely related to that lineage
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Fig5: Hypothesis for the evolutionary pathways of thylakoid transporters. (Left panel) Symbiont origin proteins in Archaeplastida (green plants, red algae and lineages that have derived their chloroplasts from red algae) are expected to be more closely related to cyanobacterial lineages than to non-Archaeplastida, such as animals and fungi. (Right panel) If the proteins have a host origin, then a closer relationship between Archaeplastida lineages and other eukaryotes, such as animals and fungi, is expected. In a symbiont origin phylogeny, brown algae derive these proteins via red algae, and are expected to be more closely related to that lineage

Mentions: No homologues of the thylakoid transporters thus far described in Arabidopsis and Synechosystis have been described in algae, although similar sequences can be recognized in many of the sequenced genomes. Phylogenetic analyses show that the Arabidopsis channels and transporters can be divided into two groups. In the first group are those proteins whose origins appear to be derived from cyanobacterial lineages (Fig. 5: left panel), and would, therefore, have been present in the common ancestor of Archaeplastida (which includes glaucophytes, red algae and green plants) at the time of the cyanobiont acquisition. These proteins include two members of the HMA family (PAA1 and PAA2; Supplemental Fig. S1), and three members of the KEA family (KEA1-3; Supplemental Fig. S2). In the second group are those transport proteins whose closest relatives are instead found among eukaryotes other than Archaeplastida. They would, therefore, appear to have been co-opted from existing gene families present in the common ancestor of most or all eukaryotes (Fig. 5: right panel). In Arabidopsis, this group includes five members of the PHT4 gene family (PHT4;1 to PHT4;5: Supplemental Fig. S3), both members of the TAAC family (TAAC and the protein encoded by the At3g51870 gene [3]), the TPK family (TPK1 to TPK5; Supplemental Fig. S4) and the TIP family [114]. For the remaining family of thylakoid proteins reviewed here (CLC), the phylogenetic results do not decisively show their evolutionary origins (Supplemental Fig. S5). The 28-member CHX family in Arabidopsis does not include any known thylakoid-located members (only a chloroplast envelope one [91]), but is also mentioned below with respect to its relationship to the KEAs.Fig. 5


Function and evolution of channels and transporters in photosynthetic membranes.

Pfeil BE, Schoefs B, Spetea C - Cell. Mol. Life Sci. (2013)

Hypothesis for the evolutionary pathways of thylakoid transporters. (Left panel) Symbiont origin proteins in Archaeplastida (green plants, red algae and lineages that have derived their chloroplasts from red algae) are expected to be more closely related to cyanobacterial lineages than to non-Archaeplastida, such as animals and fungi. (Right panel) If the proteins have a host origin, then a closer relationship between Archaeplastida lineages and other eukaryotes, such as animals and fungi, is expected. In a symbiont origin phylogeny, brown algae derive these proteins via red algae, and are expected to be more closely related to that lineage
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3928508&req=5

Fig5: Hypothesis for the evolutionary pathways of thylakoid transporters. (Left panel) Symbiont origin proteins in Archaeplastida (green plants, red algae and lineages that have derived their chloroplasts from red algae) are expected to be more closely related to cyanobacterial lineages than to non-Archaeplastida, such as animals and fungi. (Right panel) If the proteins have a host origin, then a closer relationship between Archaeplastida lineages and other eukaryotes, such as animals and fungi, is expected. In a symbiont origin phylogeny, brown algae derive these proteins via red algae, and are expected to be more closely related to that lineage
Mentions: No homologues of the thylakoid transporters thus far described in Arabidopsis and Synechosystis have been described in algae, although similar sequences can be recognized in many of the sequenced genomes. Phylogenetic analyses show that the Arabidopsis channels and transporters can be divided into two groups. In the first group are those proteins whose origins appear to be derived from cyanobacterial lineages (Fig. 5: left panel), and would, therefore, have been present in the common ancestor of Archaeplastida (which includes glaucophytes, red algae and green plants) at the time of the cyanobiont acquisition. These proteins include two members of the HMA family (PAA1 and PAA2; Supplemental Fig. S1), and three members of the KEA family (KEA1-3; Supplemental Fig. S2). In the second group are those transport proteins whose closest relatives are instead found among eukaryotes other than Archaeplastida. They would, therefore, appear to have been co-opted from existing gene families present in the common ancestor of most or all eukaryotes (Fig. 5: right panel). In Arabidopsis, this group includes five members of the PHT4 gene family (PHT4;1 to PHT4;5: Supplemental Fig. S3), both members of the TAAC family (TAAC and the protein encoded by the At3g51870 gene [3]), the TPK family (TPK1 to TPK5; Supplemental Fig. S4) and the TIP family [114]. For the remaining family of thylakoid proteins reviewed here (CLC), the phylogenetic results do not decisively show their evolutionary origins (Supplemental Fig. S5). The 28-member CHX family in Arabidopsis does not include any known thylakoid-located members (only a chloroplast envelope one [91]), but is also mentioned below with respect to its relationship to the KEAs.Fig. 5

Bottom Line: PCC 6803.Additionally, the shift from a non-thylakoid to a thylakoid location appears to have occurred at different times for different transport proteins.Some of the proteins recruited to serve in the thylakoid may have been the result of the increased specialization of its pigment-protein composition and organization in green plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological and Environmental Sciences, University of Gothenburg, 40530, Gothenburg, Sweden.

ABSTRACT
Chloroplasts from land plants and algae originated from an endosymbiotic event, most likely involving an ancestral photoautotrophic prokaryote related to cyanobacteria. Both chloroplasts and cyanobacteria have thylakoid membranes, harboring pigment-protein complexes that perform the light-dependent reactions of oxygenic photosynthesis. The composition, function and regulation of these complexes have thus far been the major topics in thylakoid membrane research. For many decades, we have also accumulated biochemical and electrophysiological evidence for the existence of solute transthylakoid transport activities that affect photosynthesis. However, research dedicated to molecular identification of the responsible proteins has only recently emerged with the explosion of genomic information. Here we review the current knowledge about channels and transporters from the thylakoid membrane of Arabidopsis thaliana and of the cyanobacterium Synechocystis sp. PCC 6803. No homologues of these proteins have been characterized in algae, although similar sequences could be recognized in many of the available sequenced genomes. Based on phylogenetic analyses, we hypothesize a host origin for most of the so far identified Arabidopsis thylakoid channels and transporters. Additionally, the shift from a non-thylakoid to a thylakoid location appears to have occurred at different times for different transport proteins. We propose that closer control of and provision for the thylakoid by products of the host genome has been an ongoing process, rather than a one-step event. Some of the proteins recruited to serve in the thylakoid may have been the result of the increased specialization of its pigment-protein composition and organization in green plants.

Show MeSH