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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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Related in: MedlinePlus

Domain structure of violaxanthin de-epoxidases and related proteins.A) Schematic representation of VDE, VDL and VDR proteins (not to scale). Three different domains are shown; the cysteine-rich domains include the N-terminal targeting sequence. Black and red asterisks indicate the positions of conserved and alternative cysteine residues, respectively. The central lipocalin domain contains the lipocalin binding fold. Conserved and divergent lipocalin motifs (roman numbers) are given in black and red, respectively. The size of the lipocalin motif was determined by sequence alignment of VDE sequences and a representative group of lipocalin proteins. The C-terminal glutamic acid-rich domain indicates the percentage of Glu residues in this domain. B) Alignment of the N-terminal cysteine-rich domains of several plant and diatom VDEs. Also included is a sequence derived from the amoeba Acanthamoeba castellanii. C) Alignment of the lipocalin motifs I, II and III of several different lipocalin VDE, VDL and VDR proteins. The distance (in amino acids) between the three lipocalin motifs is also indicated. The lipocalin motif consensus sequences, as derived from kernel lipocalins (Flower, 1996), are indicated above the alignment and conserved motifs within the alignment are indicated in red. The abbreviations used are: Lip, lipocalin; TIL, temperature induced lipocalin; CHL, chloroplastic lipocalin; PRBR, plasma retinol-binding protein precursor; CC, crustacyanin; At, Arabidopsis thaliana; Cr, Chlamydomonas reinhardtii; Dd, Dictyostelium discoideum; Gv, Gloeobacter violaceus; Hg, Homarus gammarus; Hs, Homo sapiens; Mt, Medicago truncatula; Nt, Nicotiana tabacum; Pt, Phaeodactylum tricornutum; Py, Porphyra yezoensis; Ta, Triticum aestivum; Tp, Thalassiosira pseudonana; Vc, Vibrio cholerae.
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pone-0002896-g002: Domain structure of violaxanthin de-epoxidases and related proteins.A) Schematic representation of VDE, VDL and VDR proteins (not to scale). Three different domains are shown; the cysteine-rich domains include the N-terminal targeting sequence. Black and red asterisks indicate the positions of conserved and alternative cysteine residues, respectively. The central lipocalin domain contains the lipocalin binding fold. Conserved and divergent lipocalin motifs (roman numbers) are given in black and red, respectively. The size of the lipocalin motif was determined by sequence alignment of VDE sequences and a representative group of lipocalin proteins. The C-terminal glutamic acid-rich domain indicates the percentage of Glu residues in this domain. B) Alignment of the N-terminal cysteine-rich domains of several plant and diatom VDEs. Also included is a sequence derived from the amoeba Acanthamoeba castellanii. C) Alignment of the lipocalin motifs I, II and III of several different lipocalin VDE, VDL and VDR proteins. The distance (in amino acids) between the three lipocalin motifs is also indicated. The lipocalin motif consensus sequences, as derived from kernel lipocalins (Flower, 1996), are indicated above the alignment and conserved motifs within the alignment are indicated in red. The abbreviations used are: Lip, lipocalin; TIL, temperature induced lipocalin; CHL, chloroplastic lipocalin; PRBR, plasma retinol-binding protein precursor; CC, crustacyanin; At, Arabidopsis thaliana; Cr, Chlamydomonas reinhardtii; Dd, Dictyostelium discoideum; Gv, Gloeobacter violaceus; Hg, Homarus gammarus; Hs, Homo sapiens; Mt, Medicago truncatula; Nt, Nicotiana tabacum; Pt, Phaeodactylum tricornutum; Py, Porphyra yezoensis; Ta, Triticum aestivum; Tp, Thalassiosira pseudonana; Vc, Vibrio cholerae.

Mentions: A comparison between the domain structures of the plant and diatom VDE proteins shows that the diatom proteins are relatively similar to the plant counterparts and consist of a cysteine-rich N-terminal domain, a lipocalin domain, and a C-terminal glutamic acid-rich domain (Fig. 2). The cysteine residues in the first domain can form one or more disulfide bridges [28] and this domain seems essential for VDE function because deletion of any region in this domain leads to a total loss of VDE activity [36], [37]. The second domain, which is thought to bind the xanthophyll molecule in the all-trans configuration, shows similarity to the eight-stranded β-barrel structure of the lipocalin protein family [38]. The small proteins (±200 aa) of this family are highly divergent in amino acid composition but are conserved in their tertiary structure, which allows them to bind small hydrophobic molecules [39]. Both these domains are generally well conserved between diatoms and plants, indicating that these proteins show similar folding and can bind the same molecules. However, the C-terminal Glu-rich domain is considerably less conserved between diatoms and plants: whereas the C-terminal domain of plant VDEs contains an average of 47% charged residues of which about 25% are glutamic acid residues, the percentage of charged amino acids in the PtVDE and TpVDE domains is 29 and 37% (13 and 18% Glu), respectively. Partial protonation of the glutamic acid-rich domain is thought to increase the binding of VDE to the thylakoid membrane [28], [40], and the divergence of this C-terminal domain may likely affect the pH-dependent binding of the diatom VDE to the thylakoid membrane [41], [42].


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)

Domain structure of violaxanthin de-epoxidases and related proteins.A) Schematic representation of VDE, VDL and VDR proteins (not to scale). Three different domains are shown; the cysteine-rich domains include the N-terminal targeting sequence. Black and red asterisks indicate the positions of conserved and alternative cysteine residues, respectively. The central lipocalin domain contains the lipocalin binding fold. Conserved and divergent lipocalin motifs (roman numbers) are given in black and red, respectively. The size of the lipocalin motif was determined by sequence alignment of VDE sequences and a representative group of lipocalin proteins. The C-terminal glutamic acid-rich domain indicates the percentage of Glu residues in this domain. B) Alignment of the N-terminal cysteine-rich domains of several plant and diatom VDEs. Also included is a sequence derived from the amoeba Acanthamoeba castellanii. C) Alignment of the lipocalin motifs I, II and III of several different lipocalin VDE, VDL and VDR proteins. The distance (in amino acids) between the three lipocalin motifs is also indicated. The lipocalin motif consensus sequences, as derived from kernel lipocalins (Flower, 1996), are indicated above the alignment and conserved motifs within the alignment are indicated in red. The abbreviations used are: Lip, lipocalin; TIL, temperature induced lipocalin; CHL, chloroplastic lipocalin; PRBR, plasma retinol-binding protein precursor; CC, crustacyanin; At, Arabidopsis thaliana; Cr, Chlamydomonas reinhardtii; Dd, Dictyostelium discoideum; Gv, Gloeobacter violaceus; Hg, Homarus gammarus; Hs, Homo sapiens; Mt, Medicago truncatula; Nt, Nicotiana tabacum; Pt, Phaeodactylum tricornutum; Py, Porphyra yezoensis; Ta, Triticum aestivum; Tp, Thalassiosira pseudonana; Vc, Vibrio cholerae.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0002896-g002: Domain structure of violaxanthin de-epoxidases and related proteins.A) Schematic representation of VDE, VDL and VDR proteins (not to scale). Three different domains are shown; the cysteine-rich domains include the N-terminal targeting sequence. Black and red asterisks indicate the positions of conserved and alternative cysteine residues, respectively. The central lipocalin domain contains the lipocalin binding fold. Conserved and divergent lipocalin motifs (roman numbers) are given in black and red, respectively. The size of the lipocalin motif was determined by sequence alignment of VDE sequences and a representative group of lipocalin proteins. The C-terminal glutamic acid-rich domain indicates the percentage of Glu residues in this domain. B) Alignment of the N-terminal cysteine-rich domains of several plant and diatom VDEs. Also included is a sequence derived from the amoeba Acanthamoeba castellanii. C) Alignment of the lipocalin motifs I, II and III of several different lipocalin VDE, VDL and VDR proteins. The distance (in amino acids) between the three lipocalin motifs is also indicated. The lipocalin motif consensus sequences, as derived from kernel lipocalins (Flower, 1996), are indicated above the alignment and conserved motifs within the alignment are indicated in red. The abbreviations used are: Lip, lipocalin; TIL, temperature induced lipocalin; CHL, chloroplastic lipocalin; PRBR, plasma retinol-binding protein precursor; CC, crustacyanin; At, Arabidopsis thaliana; Cr, Chlamydomonas reinhardtii; Dd, Dictyostelium discoideum; Gv, Gloeobacter violaceus; Hg, Homarus gammarus; Hs, Homo sapiens; Mt, Medicago truncatula; Nt, Nicotiana tabacum; Pt, Phaeodactylum tricornutum; Py, Porphyra yezoensis; Ta, Triticum aestivum; Tp, Thalassiosira pseudonana; Vc, Vibrio cholerae.
Mentions: A comparison between the domain structures of the plant and diatom VDE proteins shows that the diatom proteins are relatively similar to the plant counterparts and consist of a cysteine-rich N-terminal domain, a lipocalin domain, and a C-terminal glutamic acid-rich domain (Fig. 2). The cysteine residues in the first domain can form one or more disulfide bridges [28] and this domain seems essential for VDE function because deletion of any region in this domain leads to a total loss of VDE activity [36], [37]. The second domain, which is thought to bind the xanthophyll molecule in the all-trans configuration, shows similarity to the eight-stranded β-barrel structure of the lipocalin protein family [38]. The small proteins (±200 aa) of this family are highly divergent in amino acid composition but are conserved in their tertiary structure, which allows them to bind small hydrophobic molecules [39]. Both these domains are generally well conserved between diatoms and plants, indicating that these proteins show similar folding and can bind the same molecules. However, the C-terminal Glu-rich domain is considerably less conserved between diatoms and plants: whereas the C-terminal domain of plant VDEs contains an average of 47% charged residues of which about 25% are glutamic acid residues, the percentage of charged amino acids in the PtVDE and TpVDE domains is 29 and 37% (13 and 18% Glu), respectively. Partial protonation of the glutamic acid-rich domain is thought to increase the binding of VDE to the thylakoid membrane [28], [40], and the divergence of this C-terminal domain may likely affect the pH-dependent binding of the diatom VDE to the thylakoid membrane [41], [42].

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