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Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms.

Coesel S, Oborník M, Varela J, Falciatore A, Bowler C - PLoS ONE (2008)

Bottom Line: Consistent with the supplemental xanthophyll cycle in diatoms, we found more copies of the genes encoding violaxanthin de-epoxidase (VDE) and zeaxanthin epoxidase (ZEP) enzymes compared with other photosynthetic eukaryotes.Protein domain structures and expression analyses in the pennate diatom Phaeodactylum tricornutum indicate diverse roles for the different ZEP and VDE isoforms and demonstrate that they are differentially regulated by light.These studies therefore reveal the ancient origins of several components of the carotenoid biosynthesis pathway in photosynthetic eukaryotes and provide information about how they have diversified and acquired new functions in the diatoms.

View Article: PubMed Central - PubMed

Affiliation: Cell Signalling Laboratory, Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy.

ABSTRACT
Carotenoids are produced by all photosynthetic organisms, where they play essential roles in light harvesting and photoprotection. The carotenoid biosynthetic pathway of diatoms is largely unstudied, but is of particular interest because these organisms have a very different evolutionary history with respect to the Plantae and are thought to be derived from an ancient secondary endosymbiosis between heterotrophic and autotrophic eukaryotes. Furthermore, diatoms have an additional xanthophyll-based cycle for dissipating excess light energy with respect to green algae and higher plants. To explore the origins and functions of the carotenoid pathway in diatoms we searched for genes encoding pathway components in the recently completed genome sequences of two marine diatoms. Consistent with the supplemental xanthophyll cycle in diatoms, we found more copies of the genes encoding violaxanthin de-epoxidase (VDE) and zeaxanthin epoxidase (ZEP) enzymes compared with other photosynthetic eukaryotes. However, the similarity of these enzymes with those of higher plants indicates that they had very probably diversified before the secondary endosymbiosis had occurred, implying that VDE and ZEP represent early eukaryotic innovations in the Plantae. Consequently, the diatom chromist lineage likely obtained all paralogues of ZEP and VDE genes during the process of secondary endosymbiosis by gene transfer from the nucleus of the algal endosymbiont to the host nucleus. Furthermore, the presence of a ZEP gene in Tetrahymena thermophila provides the first evidence for a secondary plastid gene encoded in a heterotrophic ciliate, providing support for the chromalveolate hypothesis. Protein domain structures and expression analyses in the pennate diatom Phaeodactylum tricornutum indicate diverse roles for the different ZEP and VDE isoforms and demonstrate that they are differentially regulated by light. These studies therefore reveal the ancient origins of several components of the carotenoid biosynthesis pathway in photosynthetic eukaryotes and provide information about how they have diversified and acquired new functions in the diatoms.

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Maximum likelihood phylogenetic tree of violaxanthin de-epoxidases and related proteins.A maximum likelihood phylogenetic tree (loglk = −13981.66253) as inferred from amino acid sequences (141 amino acid characters) of violaxanthin de-epoxidases and related proteins was computed using WAG model for amino acid substitution (selected by PROTTEST) with discrete gamma distribution in four categories. All parameters (gamma shape = 2.158; proportion of invariants = 0.000) were estimated from the dataset. Numbers above branches indicate ML/NJ bootstrap supports. ML bootstraps were computed using the above mentioned model in 300 replicates. An NJ tree was inferred using AsaturA program with cutoff value 0.906 and 1000 replicates. Black stars indicate both bootstraps over 90%. Nodes that display different NJ topology than the one obtained by ML are indicated by “dt”.
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pone-0002896-g003: Maximum likelihood phylogenetic tree of violaxanthin de-epoxidases and related proteins.A maximum likelihood phylogenetic tree (loglk = −13981.66253) as inferred from amino acid sequences (141 amino acid characters) of violaxanthin de-epoxidases and related proteins was computed using WAG model for amino acid substitution (selected by PROTTEST) with discrete gamma distribution in four categories. All parameters (gamma shape = 2.158; proportion of invariants = 0.000) were estimated from the dataset. Numbers above branches indicate ML/NJ bootstrap supports. ML bootstraps were computed using the above mentioned model in 300 replicates. An NJ tree was inferred using AsaturA program with cutoff value 0.906 and 1000 replicates. Black stars indicate both bootstraps over 90%. Nodes that display different NJ topology than the one obtained by ML are indicated by “dt”.

Mentions: A phylogenetic tree of the diatom and plant VDEs and related genes was generated and rooted by related lipocalin family proteins from both prokaryotes and eukaryotes. As can be seen in the tree (Fig. 3), there is a considerable difference between the ancient lipocalins and VDEs, such that the ancestor of VDE proteins within these lipocalin proteins cannot be specified. The VDE proteins constituted three distinct clusters: VDE, VDL (VDE-like) and VDR (VDE-related) proteins. Two of these clusters (VDE and VDR) are composed of plant and diatom sequences with diatom sequences appearing on the root of each cluster (Fig. 3). Plant sequences are absent from the VDL cluster, which contains, in addition to diatom proteins, sequences from other chromalveolates, such as heterokonts and dinoflagellates (Fig. 3). A single metazoan VDL sequence from the eastern oyster Crassostrea virginica, which has been obtained from ESTs at NCBI, appeared within the VDL proteins; however, the position of this oyster sequence is not supported by bootstraps. Its position is also questioned by the fact that the NJ tree showed a different topology than the ML tree, placing C. virginica at the root of all VDE and related proteins (data not shown). The sequence from C. virginica is the only VDE sequence known from non-photosynthetic eukaryotes and, moreover, when Blast searched in NCBI it yields hits only from photosynthetic eukaryotes. We therefore have serious reservations about the identity of this sequence and speculate that it may be derived from contamination of C. virginica cDNA with material from eukaryotic algae.


Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms.

Coesel S, Oborník M, Varela J, Falciatore A, Bowler C - PLoS ONE (2008)

Maximum likelihood phylogenetic tree of violaxanthin de-epoxidases and related proteins.A maximum likelihood phylogenetic tree (loglk = −13981.66253) as inferred from amino acid sequences (141 amino acid characters) of violaxanthin de-epoxidases and related proteins was computed using WAG model for amino acid substitution (selected by PROTTEST) with discrete gamma distribution in four categories. All parameters (gamma shape = 2.158; proportion of invariants = 0.000) were estimated from the dataset. Numbers above branches indicate ML/NJ bootstrap supports. ML bootstraps were computed using the above mentioned model in 300 replicates. An NJ tree was inferred using AsaturA program with cutoff value 0.906 and 1000 replicates. Black stars indicate both bootstraps over 90%. Nodes that display different NJ topology than the one obtained by ML are indicated by “dt”.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2483416&req=5

pone-0002896-g003: Maximum likelihood phylogenetic tree of violaxanthin de-epoxidases and related proteins.A maximum likelihood phylogenetic tree (loglk = −13981.66253) as inferred from amino acid sequences (141 amino acid characters) of violaxanthin de-epoxidases and related proteins was computed using WAG model for amino acid substitution (selected by PROTTEST) with discrete gamma distribution in four categories. All parameters (gamma shape = 2.158; proportion of invariants = 0.000) were estimated from the dataset. Numbers above branches indicate ML/NJ bootstrap supports. ML bootstraps were computed using the above mentioned model in 300 replicates. An NJ tree was inferred using AsaturA program with cutoff value 0.906 and 1000 replicates. Black stars indicate both bootstraps over 90%. Nodes that display different NJ topology than the one obtained by ML are indicated by “dt”.
Mentions: A phylogenetic tree of the diatom and plant VDEs and related genes was generated and rooted by related lipocalin family proteins from both prokaryotes and eukaryotes. As can be seen in the tree (Fig. 3), there is a considerable difference between the ancient lipocalins and VDEs, such that the ancestor of VDE proteins within these lipocalin proteins cannot be specified. The VDE proteins constituted three distinct clusters: VDE, VDL (VDE-like) and VDR (VDE-related) proteins. Two of these clusters (VDE and VDR) are composed of plant and diatom sequences with diatom sequences appearing on the root of each cluster (Fig. 3). Plant sequences are absent from the VDL cluster, which contains, in addition to diatom proteins, sequences from other chromalveolates, such as heterokonts and dinoflagellates (Fig. 3). A single metazoan VDL sequence from the eastern oyster Crassostrea virginica, which has been obtained from ESTs at NCBI, appeared within the VDL proteins; however, the position of this oyster sequence is not supported by bootstraps. Its position is also questioned by the fact that the NJ tree showed a different topology than the ML tree, placing C. virginica at the root of all VDE and related proteins (data not shown). The sequence from C. virginica is the only VDE sequence known from non-photosynthetic eukaryotes and, moreover, when Blast searched in NCBI it yields hits only from photosynthetic eukaryotes. We therefore have serious reservations about the identity of this sequence and speculate that it may be derived from contamination of C. virginica cDNA with material from eukaryotic algae.

Bottom Line: Consistent with the supplemental xanthophyll cycle in diatoms, we found more copies of the genes encoding violaxanthin de-epoxidase (VDE) and zeaxanthin epoxidase (ZEP) enzymes compared with other photosynthetic eukaryotes.Protein domain structures and expression analyses in the pennate diatom Phaeodactylum tricornutum indicate diverse roles for the different ZEP and VDE isoforms and demonstrate that they are differentially regulated by light.These studies therefore reveal the ancient origins of several components of the carotenoid biosynthesis pathway in photosynthetic eukaryotes and provide information about how they have diversified and acquired new functions in the diatoms.

View Article: PubMed Central - PubMed

Affiliation: Cell Signalling Laboratory, Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy.

ABSTRACT
Carotenoids are produced by all photosynthetic organisms, where they play essential roles in light harvesting and photoprotection. The carotenoid biosynthetic pathway of diatoms is largely unstudied, but is of particular interest because these organisms have a very different evolutionary history with respect to the Plantae and are thought to be derived from an ancient secondary endosymbiosis between heterotrophic and autotrophic eukaryotes. Furthermore, diatoms have an additional xanthophyll-based cycle for dissipating excess light energy with respect to green algae and higher plants. To explore the origins and functions of the carotenoid pathway in diatoms we searched for genes encoding pathway components in the recently completed genome sequences of two marine diatoms. Consistent with the supplemental xanthophyll cycle in diatoms, we found more copies of the genes encoding violaxanthin de-epoxidase (VDE) and zeaxanthin epoxidase (ZEP) enzymes compared with other photosynthetic eukaryotes. However, the similarity of these enzymes with those of higher plants indicates that they had very probably diversified before the secondary endosymbiosis had occurred, implying that VDE and ZEP represent early eukaryotic innovations in the Plantae. Consequently, the diatom chromist lineage likely obtained all paralogues of ZEP and VDE genes during the process of secondary endosymbiosis by gene transfer from the nucleus of the algal endosymbiont to the host nucleus. Furthermore, the presence of a ZEP gene in Tetrahymena thermophila provides the first evidence for a secondary plastid gene encoded in a heterotrophic ciliate, providing support for the chromalveolate hypothesis. Protein domain structures and expression analyses in the pennate diatom Phaeodactylum tricornutum indicate diverse roles for the different ZEP and VDE isoforms and demonstrate that they are differentially regulated by light. These studies therefore reveal the ancient origins of several components of the carotenoid biosynthesis pathway in photosynthetic eukaryotes and provide information about how they have diversified and acquired new functions in the diatoms.

Show MeSH
Related in: MedlinePlus