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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.

Show MeSH
Hypothesized carotenoid biosynthetic pathway in diatoms.The genes identified in this study, phytoene synthase (PSY), phytoene desaturase (PDS), ξ-carotene desaturase (ZDS), lycopene β-cyclase (LCYB), β-carotene hydroxylase (BCH), lutein deficient-like (LTL), zeaxanthin epoxidase (ZEP), violaxanthin de-epoxidase (VDE) and violaxanthin de-epoxidase-like (VDL), are indicated. The BCH-encoding gene is absent in the P. tricornutum genome, ZEP3 and VDL2 are absent in the T. pseudonana genome. The two xanthophyll cycles are boxed, A) the violaxanthin cycle and B) the diadinoxanthin cycle. α-carotene and lutein are not produced by diatoms. Dashed arrows indicate hypothetical conversion steps, according to Lohr and Wilhelm (1999, 2001).
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pone-0002896-g001: Hypothesized carotenoid biosynthetic pathway in diatoms.The genes identified in this study, phytoene synthase (PSY), phytoene desaturase (PDS), ξ-carotene desaturase (ZDS), lycopene β-cyclase (LCYB), β-carotene hydroxylase (BCH), lutein deficient-like (LTL), zeaxanthin epoxidase (ZEP), violaxanthin de-epoxidase (VDE) and violaxanthin de-epoxidase-like (VDL), are indicated. The BCH-encoding gene is absent in the P. tricornutum genome, ZEP3 and VDL2 are absent in the T. pseudonana genome. The two xanthophyll cycles are boxed, A) the violaxanthin cycle and B) the diadinoxanthin cycle. α-carotene and lutein are not produced by diatoms. Dashed arrows indicate hypothetical conversion steps, according to Lohr and Wilhelm (1999, 2001).

Mentions: Diatoms are believed to have obtained their plastid from a secondary endosymbiosis between a heterotrophic eukaryote and an ancient red alga. This event is postulated to have occurred at least 800 Ma [13]–[15] and may subsequently have given rise to the chromalveolates, which includes the group of algae collectively called Chromista. The chromist algae, Haptophyta (e.g., coccolithophorids), Cryptophyta (e.g., Guillardia theta), Heterokonts (diatoms and brown algae), and tertiary red-symbiotic dinoflagellates, all use chlorophyll a, chlorophyll c, and fucoxanthin as light-harvesting pigments [16]. Fucoxanthin, a carotenoid presumably derived from β-carotene (Fig. 1), absorbs light in the blue range of the light spectrum and is largely responsible for the characteristic brown color of chromist algae. The success of chromist algae may be explained by their ability to maintain photosynthetic activity in the blue-light-dominated oceanic environment [17]–[19]. In particular, diatoms have a huge capacity to dissipate excess absorbed light energy and their non-photochemical quenching (NPQ) levels can be as much as five times the levels registered for higher plants [20]. Moreover, diatoms are able to apply this photoprotective mechanism without significantly altering their light harvesting capacity [21], which allows them to maintain high growth rates over a wide range of light intensities [22].


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)

Hypothesized carotenoid biosynthetic pathway in diatoms.The genes identified in this study, phytoene synthase (PSY), phytoene desaturase (PDS), ξ-carotene desaturase (ZDS), lycopene β-cyclase (LCYB), β-carotene hydroxylase (BCH), lutein deficient-like (LTL), zeaxanthin epoxidase (ZEP), violaxanthin de-epoxidase (VDE) and violaxanthin de-epoxidase-like (VDL), are indicated. The BCH-encoding gene is absent in the P. tricornutum genome, ZEP3 and VDL2 are absent in the T. pseudonana genome. The two xanthophyll cycles are boxed, A) the violaxanthin cycle and B) the diadinoxanthin cycle. α-carotene and lutein are not produced by diatoms. Dashed arrows indicate hypothetical conversion steps, according to Lohr and Wilhelm (1999, 2001).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0002896-g001: Hypothesized carotenoid biosynthetic pathway in diatoms.The genes identified in this study, phytoene synthase (PSY), phytoene desaturase (PDS), ξ-carotene desaturase (ZDS), lycopene β-cyclase (LCYB), β-carotene hydroxylase (BCH), lutein deficient-like (LTL), zeaxanthin epoxidase (ZEP), violaxanthin de-epoxidase (VDE) and violaxanthin de-epoxidase-like (VDL), are indicated. The BCH-encoding gene is absent in the P. tricornutum genome, ZEP3 and VDL2 are absent in the T. pseudonana genome. The two xanthophyll cycles are boxed, A) the violaxanthin cycle and B) the diadinoxanthin cycle. α-carotene and lutein are not produced by diatoms. Dashed arrows indicate hypothetical conversion steps, according to Lohr and Wilhelm (1999, 2001).
Mentions: Diatoms are believed to have obtained their plastid from a secondary endosymbiosis between a heterotrophic eukaryote and an ancient red alga. This event is postulated to have occurred at least 800 Ma [13]–[15] and may subsequently have given rise to the chromalveolates, which includes the group of algae collectively called Chromista. The chromist algae, Haptophyta (e.g., coccolithophorids), Cryptophyta (e.g., Guillardia theta), Heterokonts (diatoms and brown algae), and tertiary red-symbiotic dinoflagellates, all use chlorophyll a, chlorophyll c, and fucoxanthin as light-harvesting pigments [16]. Fucoxanthin, a carotenoid presumably derived from β-carotene (Fig. 1), absorbs light in the blue range of the light spectrum and is largely responsible for the characteristic brown color of chromist algae. The success of chromist algae may be explained by their ability to maintain photosynthetic activity in the blue-light-dominated oceanic environment [17]–[19]. In particular, diatoms have a huge capacity to dissipate excess absorbed light energy and their non-photochemical quenching (NPQ) levels can be as much as five times the levels registered for higher plants [20]. Moreover, diatoms are able to apply this photoprotective mechanism without significantly altering their light harvesting capacity [21], which allows them to maintain high growth rates over a wide range of light intensities [22].

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