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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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Thylakoid membrane organization and composition in cyanobacteria and plants. Cyanobacterial thylakoid membranes are located directly in the cytosol, are arranged in layers, make contact with the plasma membrane, and have attached phycobilisomes. Thylakoid membranes in green algae and land plants are located inside the chloroplast, are organized in grana stacks interconnected by stroma-exposed lamellae and contain chlorophyll-protein complexes for harvesting light. Four photosynthetic complexes are present in the thylakoid membrane, namely photosystem II (PSII), cytochrome b6f (cytbf), photosystem I (PSI) and H+-translocating ATP synthase (F0F1, cF0F1). These complexes are uniformly distributed in cyanobacteria, whereas in green algae and land plants they display a lateral distribution
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Fig1: Thylakoid membrane organization and composition in cyanobacteria and plants. Cyanobacterial thylakoid membranes are located directly in the cytosol, are arranged in layers, make contact with the plasma membrane, and have attached phycobilisomes. Thylakoid membranes in green algae and land plants are located inside the chloroplast, are organized in grana stacks interconnected by stroma-exposed lamellae and contain chlorophyll-protein complexes for harvesting light. Four photosynthetic complexes are present in the thylakoid membrane, namely photosystem II (PSII), cytochrome b6f (cytbf), photosystem I (PSI) and H+-translocating ATP synthase (F0F1, cF0F1). These complexes are uniformly distributed in cyanobacteria, whereas in green algae and land plants they display a lateral distribution

Mentions: Oxygenic photosynthesis is a biophysicochemical process that converts carbon dioxide into organic compounds using light as a source of energy. It occurs in plants, algae and cyanobacteria, but not in archaea, and uses water as a source of electrons, releasing oxygen as a waste product. Photosynthesis confers autotrophy to organisms and is the only natural process allowing for creation of food from simple and abundant compounds. This process is vital for all aerobic life on Earth because, in addition to maintaining normal levels of oxygen in the atmosphere, photosynthetic products directly or indirectly constitute the ultimate source of energy in food. Regardless of the type of photosynthetic organism, this process takes place according to the same scheme [1]. It always requires the collection of photons by pigment molecules within light-harvesting complexes. The harvested energy is transferred to the reaction center and is used to drive an electron flow within the membrane hosting the photosynthetic apparatus, the so-called thylakoid membrane. In prokaryotic photosynthetic organisms, such as cyanobacteria, thylakoid membranes are in direct contact with the cytosol, whereas in eukaryotic photosynthetic organisms, i.e., red algae, brown algae, diatoms, green algae and land plants, thylakoids are separated from the cytosol by envelopes, together forming a unique cell compartment, the chloroplast. Glaucophytes occupy an intermediate position between cyanobacteria and chloroplasts, because their photosynthetic apparatus, the so-called cyanelle, is surrounded by a peptidoglycan layer that is believed to be a relic of the endosymbiotic origin of chloroplasts from cyanobacteria. Thus, the chloroplast has evolved via primary symbiosis from an ancestor shared with cyanobacteria. As a result of secondary symbiosis, a four-layer envelope surrounds the chloroplast in brown algae and diatoms, in contrast to a double envelope around the chloroplast in red algae, green algae and land plants [2, 3]. The organization of the photosynthetic machinery in cyanobacteria, green algae and land plants is presented in Fig. 1.Fig. 1


Function and evolution of channels and transporters in photosynthetic membranes.

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

Thylakoid membrane organization and composition in cyanobacteria and plants. Cyanobacterial thylakoid membranes are located directly in the cytosol, are arranged in layers, make contact with the plasma membrane, and have attached phycobilisomes. Thylakoid membranes in green algae and land plants are located inside the chloroplast, are organized in grana stacks interconnected by stroma-exposed lamellae and contain chlorophyll-protein complexes for harvesting light. Four photosynthetic complexes are present in the thylakoid membrane, namely photosystem II (PSII), cytochrome b6f (cytbf), photosystem I (PSI) and H+-translocating ATP synthase (F0F1, cF0F1). These complexes are uniformly distributed in cyanobacteria, whereas in green algae and land plants they display a lateral distribution
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: Thylakoid membrane organization and composition in cyanobacteria and plants. Cyanobacterial thylakoid membranes are located directly in the cytosol, are arranged in layers, make contact with the plasma membrane, and have attached phycobilisomes. Thylakoid membranes in green algae and land plants are located inside the chloroplast, are organized in grana stacks interconnected by stroma-exposed lamellae and contain chlorophyll-protein complexes for harvesting light. Four photosynthetic complexes are present in the thylakoid membrane, namely photosystem II (PSII), cytochrome b6f (cytbf), photosystem I (PSI) and H+-translocating ATP synthase (F0F1, cF0F1). These complexes are uniformly distributed in cyanobacteria, whereas in green algae and land plants they display a lateral distribution
Mentions: Oxygenic photosynthesis is a biophysicochemical process that converts carbon dioxide into organic compounds using light as a source of energy. It occurs in plants, algae and cyanobacteria, but not in archaea, and uses water as a source of electrons, releasing oxygen as a waste product. Photosynthesis confers autotrophy to organisms and is the only natural process allowing for creation of food from simple and abundant compounds. This process is vital for all aerobic life on Earth because, in addition to maintaining normal levels of oxygen in the atmosphere, photosynthetic products directly or indirectly constitute the ultimate source of energy in food. Regardless of the type of photosynthetic organism, this process takes place according to the same scheme [1]. It always requires the collection of photons by pigment molecules within light-harvesting complexes. The harvested energy is transferred to the reaction center and is used to drive an electron flow within the membrane hosting the photosynthetic apparatus, the so-called thylakoid membrane. In prokaryotic photosynthetic organisms, such as cyanobacteria, thylakoid membranes are in direct contact with the cytosol, whereas in eukaryotic photosynthetic organisms, i.e., red algae, brown algae, diatoms, green algae and land plants, thylakoids are separated from the cytosol by envelopes, together forming a unique cell compartment, the chloroplast. Glaucophytes occupy an intermediate position between cyanobacteria and chloroplasts, because their photosynthetic apparatus, the so-called cyanelle, is surrounded by a peptidoglycan layer that is believed to be a relic of the endosymbiotic origin of chloroplasts from cyanobacteria. Thus, the chloroplast has evolved via primary symbiosis from an ancestor shared with cyanobacteria. As a result of secondary symbiosis, a four-layer envelope surrounds the chloroplast in brown algae and diatoms, in contrast to a double envelope around the chloroplast in red algae, green algae and land plants [2, 3]. The organization of the photosynthetic machinery in cyanobacteria, green algae and land plants is presented in Fig. 1.Fig. 1

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