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A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids.

Sturm S, Engelken J, Gruber A, Vugrinec S, Kroth PG, Adamska I, Lavaud J - BMC Evol. Biol. (2013)

Bottom Line: Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection and are found in the red and green plant lineages, with a complex distribution pattern of subfamilies in the different algal lineages.The occurrence of RedCAPs was found to be restricted to the red algal lineage, including red algae (with primary plastids) as well as cryptophytes, haptophytes and heterokontophytes (with secondary plastids of red algal origin).In their proposed function, the RedCAP protein family may thus have played a role in the evolutionary structural remodelling of light-harvesting antennae in the red lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Ökophysiologie der Pflanzen, Fach 611, Universität Konstanz, 78457 Konstanz, Germany.

ABSTRACT

Background: Light, the driving force of photosynthesis, can be harmful when present in excess; therefore, any light harvesting system requires photoprotection. Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection and are found in the red and green plant lineages, with a complex distribution pattern of subfamilies in the different algal lineages.

Results: Here, we demonstrate that the recently discovered "red lineage chlorophyll a/b-binding-like proteins" (RedCAPs) form a monophyletic family within this protein superfamily. The occurrence of RedCAPs was found to be restricted to the red algal lineage, including red algae (with primary plastids) as well as cryptophytes, haptophytes and heterokontophytes (with secondary plastids of red algal origin). Expression of a full-length RedCAP:GFP fusion construct in the diatom Phaeodactylum tricornutum confirmed the predicted plastid localisation of RedCAPs. Furthermore, we observed that similarly to the fucoxanthin chlorophyll a/c-binding light-harvesting antenna proteins also RedCAP transcripts in diatoms were regulated in a diurnal way at standard light conditions and strongly repressed at high light intensities.

Conclusions: The absence of RedCAPs from the green lineage implies that RedCAPs evolved in the red lineage after separation from the the green lineage. During the evolution of secondary plastids, RedCAP genes therefore must have been transferred from the nucleus of the endocytobiotic alga to the nucleus of the host cell, a process that involved complementation with pre-sequences allowing import of the gene product into the secondary plastid bound by four membranes. Based on light-dependent transcription and on localisation data, we propose that RedCAPs might participate in the light (intensity and quality)-dependent structural or functional reorganisation of the light-harvesting antennae of the photosystems upon dark to light shifts as regularly experienced by diatoms in nature. Remarkably, in plastids of the red lineage as well as in green lineage plastids, the phycobilisome based cyanobacterial light harvesting system has been replaced by light harvesting systems that are based on members of the extended LHC protein superfamily, either for one of the photosystems (PS I of red algae) or for both (diatoms). In their proposed function, the RedCAP protein family may thus have played a role in the evolutionary structural remodelling of light-harvesting antennae in the red lineage.

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Phylogenetic relationships of RedCAPs. Thirteen available full-length sequences from red algae and algae with secondary plastids of red algal origin, with an aligned 146 amino acid positions, thereof 99 phylogenetically informative, were analysed. A Maximum likelihood tree was inferred under the CpRev + G model. Bootstrap values for Neighbor-joining (10,000 replicates) and Maximum likelihood analysis (100 replicates) as well as posterior probabilities (one million generation, 25% burn-in) are given. Accession numbers of analysed sequences are listed in Table S1, see Additional file 1, for sequence alignment see Additional file 6.
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Figure 1: Phylogenetic relationships of RedCAPs. Thirteen available full-length sequences from red algae and algae with secondary plastids of red algal origin, with an aligned 146 amino acid positions, thereof 99 phylogenetically informative, were analysed. A Maximum likelihood tree was inferred under the CpRev + G model. Bootstrap values for Neighbor-joining (10,000 replicates) and Maximum likelihood analysis (100 replicates) as well as posterior probabilities (one million generation, 25% burn-in) are given. Accession numbers of analysed sequences are listed in Table S1, see Additional file 1, for sequence alignment see Additional file 6.

Mentions: In a phylogenetic analysis of all currently available RedCAP sequences (RedCAPs from 13 taxa, alignment of 146 positions, see Additional file 6), the expected species tree with red algae and algae with complex plastids as sister groups was recovered to some detail (Figure 1). This implies that the evolution of RedCAPs apparently did not involve the emergence of paralogous gene copies (as it is commonly observed in LHCs) and that no horizontal gene transfer events could be detected within algae with secondary plastids of the red lineage.


A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids.

Sturm S, Engelken J, Gruber A, Vugrinec S, Kroth PG, Adamska I, Lavaud J - BMC Evol. Biol. (2013)

Phylogenetic relationships of RedCAPs. Thirteen available full-length sequences from red algae and algae with secondary plastids of red algal origin, with an aligned 146 amino acid positions, thereof 99 phylogenetically informative, were analysed. A Maximum likelihood tree was inferred under the CpRev + G model. Bootstrap values for Neighbor-joining (10,000 replicates) and Maximum likelihood analysis (100 replicates) as well as posterior probabilities (one million generation, 25% burn-in) are given. Accession numbers of analysed sequences are listed in Table S1, see Additional file 1, for sequence alignment see Additional file 6.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750529&req=5

Figure 1: Phylogenetic relationships of RedCAPs. Thirteen available full-length sequences from red algae and algae with secondary plastids of red algal origin, with an aligned 146 amino acid positions, thereof 99 phylogenetically informative, were analysed. A Maximum likelihood tree was inferred under the CpRev + G model. Bootstrap values for Neighbor-joining (10,000 replicates) and Maximum likelihood analysis (100 replicates) as well as posterior probabilities (one million generation, 25% burn-in) are given. Accession numbers of analysed sequences are listed in Table S1, see Additional file 1, for sequence alignment see Additional file 6.
Mentions: In a phylogenetic analysis of all currently available RedCAP sequences (RedCAPs from 13 taxa, alignment of 146 positions, see Additional file 6), the expected species tree with red algae and algae with complex plastids as sister groups was recovered to some detail (Figure 1). This implies that the evolution of RedCAPs apparently did not involve the emergence of paralogous gene copies (as it is commonly observed in LHCs) and that no horizontal gene transfer events could be detected within algae with secondary plastids of the red lineage.

Bottom Line: Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection and are found in the red and green plant lineages, with a complex distribution pattern of subfamilies in the different algal lineages.The occurrence of RedCAPs was found to be restricted to the red algal lineage, including red algae (with primary plastids) as well as cryptophytes, haptophytes and heterokontophytes (with secondary plastids of red algal origin).In their proposed function, the RedCAP protein family may thus have played a role in the evolutionary structural remodelling of light-harvesting antennae in the red lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Ökophysiologie der Pflanzen, Fach 611, Universität Konstanz, 78457 Konstanz, Germany.

ABSTRACT

Background: Light, the driving force of photosynthesis, can be harmful when present in excess; therefore, any light harvesting system requires photoprotection. Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection and are found in the red and green plant lineages, with a complex distribution pattern of subfamilies in the different algal lineages.

Results: Here, we demonstrate that the recently discovered "red lineage chlorophyll a/b-binding-like proteins" (RedCAPs) form a monophyletic family within this protein superfamily. The occurrence of RedCAPs was found to be restricted to the red algal lineage, including red algae (with primary plastids) as well as cryptophytes, haptophytes and heterokontophytes (with secondary plastids of red algal origin). Expression of a full-length RedCAP:GFP fusion construct in the diatom Phaeodactylum tricornutum confirmed the predicted plastid localisation of RedCAPs. Furthermore, we observed that similarly to the fucoxanthin chlorophyll a/c-binding light-harvesting antenna proteins also RedCAP transcripts in diatoms were regulated in a diurnal way at standard light conditions and strongly repressed at high light intensities.

Conclusions: The absence of RedCAPs from the green lineage implies that RedCAPs evolved in the red lineage after separation from the the green lineage. During the evolution of secondary plastids, RedCAP genes therefore must have been transferred from the nucleus of the endocytobiotic alga to the nucleus of the host cell, a process that involved complementation with pre-sequences allowing import of the gene product into the secondary plastid bound by four membranes. Based on light-dependent transcription and on localisation data, we propose that RedCAPs might participate in the light (intensity and quality)-dependent structural or functional reorganisation of the light-harvesting antennae of the photosystems upon dark to light shifts as regularly experienced by diatoms in nature. Remarkably, in plastids of the red lineage as well as in green lineage plastids, the phycobilisome based cyanobacterial light harvesting system has been replaced by light harvesting systems that are based on members of the extended LHC protein superfamily, either for one of the photosystems (PS I of red algae) or for both (diatoms). In their proposed function, the RedCAP protein family may thus have played a role in the evolutionary structural remodelling of light-harvesting antennae in the red lineage.

Show MeSH
Related in: MedlinePlus