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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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Proposed evolutionary history of RedCAP, LHC and LHC-like genes. RedCAPs evolved in red algae after primary endocytobiosis and their genes can be found in the nuclear genome of almost all red algae investigated so far. During secondary endocytobiosis, when a red alga was taken up by another eukaryotic host, the RedCAP gene was transferred to the nucleus of the host cell and was lost from the nuclear genome of the former endosymbiont. Similarly, different nuclear encoded LHC variants evolved in organisms with primary plastids and were transferred to the nucleus of the secondary host during the evolution of secondary plastids. Interestingly, in diatoms, HLIP/OHP1-like genes (plastid encoded in red algae) as well as OHP2 genes (nucleus encoded in red algae) have been transferred to the nucleus of the secondary host cell. This is in contrast to the situation in the cryptophyte Guillardia theta, in which HLIP/OHP1-like is plastid encoded, and OHP2 is nucleomorph encoded. Table S2 (see Additional file 7) contains detailed genome/gene information.
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Figure 2: Proposed evolutionary history of RedCAP, LHC and LHC-like genes. RedCAPs evolved in red algae after primary endocytobiosis and their genes can be found in the nuclear genome of almost all red algae investigated so far. During secondary endocytobiosis, when a red alga was taken up by another eukaryotic host, the RedCAP gene was transferred to the nucleus of the host cell and was lost from the nuclear genome of the former endosymbiont. Similarly, different nuclear encoded LHC variants evolved in organisms with primary plastids and were transferred to the nucleus of the secondary host during the evolution of secondary plastids. Interestingly, in diatoms, HLIP/OHP1-like genes (plastid encoded in red algae) as well as OHP2 genes (nucleus encoded in red algae) have been transferred to the nucleus of the secondary host cell. This is in contrast to the situation in the cryptophyte Guillardia theta, in which HLIP/OHP1-like is plastid encoded, and OHP2 is nucleomorph encoded. Table S2 (see Additional file 7) contains detailed genome/gene information.

Mentions: Evolutionary studies indicate that all LHC superfamily members have a common origin and arose from an cyanobacterial one-helix HLIP-like protein ancestor [4-6,8-11,15]. The HLIP/OHP1-like sequences were likely at the origin of the nuclear-encoded OHP1, OHP2 and SEP in the green or OHP2 and SEP in the red algal lineage (the monophyletic group of OHP2 sequences might also originate from degenerated SEP sequences) [11]. In the green lineage, the ancestral HLIP/OHP1-like sequences were lost, whereas in the red lineage HLIP/OHP1-like sequences can be found, encoded either on the plastid or the nuclear genomes (Figure 2, Table S2, see Additional file 7).


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)

Proposed evolutionary history of RedCAP, LHC and LHC-like genes. RedCAPs evolved in red algae after primary endocytobiosis and their genes can be found in the nuclear genome of almost all red algae investigated so far. During secondary endocytobiosis, when a red alga was taken up by another eukaryotic host, the RedCAP gene was transferred to the nucleus of the host cell and was lost from the nuclear genome of the former endosymbiont. Similarly, different nuclear encoded LHC variants evolved in organisms with primary plastids and were transferred to the nucleus of the secondary host during the evolution of secondary plastids. Interestingly, in diatoms, HLIP/OHP1-like genes (plastid encoded in red algae) as well as OHP2 genes (nucleus encoded in red algae) have been transferred to the nucleus of the secondary host cell. This is in contrast to the situation in the cryptophyte Guillardia theta, in which HLIP/OHP1-like is plastid encoded, and OHP2 is nucleomorph encoded. Table S2 (see Additional file 7) contains detailed genome/gene information.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Proposed evolutionary history of RedCAP, LHC and LHC-like genes. RedCAPs evolved in red algae after primary endocytobiosis and their genes can be found in the nuclear genome of almost all red algae investigated so far. During secondary endocytobiosis, when a red alga was taken up by another eukaryotic host, the RedCAP gene was transferred to the nucleus of the host cell and was lost from the nuclear genome of the former endosymbiont. Similarly, different nuclear encoded LHC variants evolved in organisms with primary plastids and were transferred to the nucleus of the secondary host during the evolution of secondary plastids. Interestingly, in diatoms, HLIP/OHP1-like genes (plastid encoded in red algae) as well as OHP2 genes (nucleus encoded in red algae) have been transferred to the nucleus of the secondary host cell. This is in contrast to the situation in the cryptophyte Guillardia theta, in which HLIP/OHP1-like is plastid encoded, and OHP2 is nucleomorph encoded. Table S2 (see Additional file 7) contains detailed genome/gene information.
Mentions: Evolutionary studies indicate that all LHC superfamily members have a common origin and arose from an cyanobacterial one-helix HLIP-like protein ancestor [4-6,8-11,15]. The HLIP/OHP1-like sequences were likely at the origin of the nuclear-encoded OHP1, OHP2 and SEP in the green or OHP2 and SEP in the red algal lineage (the monophyletic group of OHP2 sequences might also originate from degenerated SEP sequences) [11]. In the green lineage, the ancestral HLIP/OHP1-like sequences were lost, whereas in the red lineage HLIP/OHP1-like sequences can be found, encoded either on the plastid or the nuclear genomes (Figure 2, Table S2, see Additional file 7).

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