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An update on carotenoid biosynthesis in algae: phylogenetic evidence for the existence of two classes of phytoene synthase.

ABSTRACT: Carotenoids play crucial roles in structure and function of the photosynthetic apparatus of bacteria, algae, and higher plants. The entry-step reaction to carotenoid biosynthesis is catalyzed by the phytoene synthase (PSY), which is structurally and functionally related in all organisms. A comparative genomic analysis regarding the PSY revealed that the green algae Ostreococcus and Micromonas possess two orthologous copies of the PSY genes, indicating an ancient gene duplication event that produced two classes of PSY in algae. However, some other green algae (Chlamydomonas reinhardtii, Chlorella vulgaris, and Volvox carteri), red algae (Cyanidioschyzon merolae), diatoms (Thalassiosira pseudonana and Phaeodactylum tricornutum), and higher plants retained only one class of the PSY gene whereas the other gene copy was lost in these species. Further, similar to the situation in higher plants recent gene duplications of PSY have occurred for example in the green alga Dunaliella salina/bardawil. As members of the PSY gene families in some higher plants are differentially regulated during development or stress, the discovery of two classes of PSY gene families in some algae suggests that carotenoid biosynthesis in these algae is differentially regulated in response to development and environmental stress as well.

SUBMITTER: Tran D

PROVIDER: S-EPMC6008256 | biostudies-literature | 2009 Feb

REPOSITORIES: biostudies-literature

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An update on carotenoid biosynthesis in algae: phylogenetic evidence for the existence of two classes of phytoene synthase.

Tran Duc D Haven James J Qiu Wei-Gang WG Polle Juergen E W JE

Planta 20081209 3

Carotenoids play crucial roles in structure and function of the photosynthetic apparatus of bacteria, algae, and higher plants. The entry-step reaction to carotenoid biosynthesis is catalyzed by the phytoene synthase (PSY), which is structurally and functionally related in all organisms. A comparative genomic analysis regarding the PSY revealed that the green algae Ostreococcus and Micromonas possess two orthologous copies of the PSY genes, indicating an ancient gene duplication event that produ ...[more]

PMID: 19066941

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Project description:BACKGROUND:Euglena gracilis, a unicellular phytoflagellate within Euglenida, has attracted much attention as a potential feedstock for renewable energy production. In outdoor open-pond cultivation for biofuel production, excess direct sunlight can inhibit photosynthesis in this alga and decrease its productivity. Carotenoids play important roles in light harvesting during photosynthesis and offer photoprotection for certain non-photosynthetic and photosynthetic organisms including cyanobacteria, algae, and higher plants. Although, Euglenida contains ?-carotene and xanthophylls (such as zeaxanthin, diatoxanthin, diadinoxanthin and 9'-cis neoxanthin), the pathway of carotenoid biosynthesis has not been elucidated. RESULTS:To clarify the carotenoid biosynthetic pathway in E. gracilis, we searched for the putative E. gracilis geranylgeranyl pyrophosphate (GGPP) synthase gene (crtE) and phytoene synthase gene (crtB) by tblastn searches from RNA-seq data and obtained their cDNAs. Complementation experiments in Escherichia coli with carotenoid biosynthetic genes of Pantoea ananatis showed that E. gracilis crtE (EgcrtE) and EgcrtB cDNAs encode GGPP synthase and phytoene synthase, respectively. Phylogenetic analyses indicated that the predicted proteins of EgcrtE and EgcrtB belong to a clade distinct from a group of GGPP synthase and phytoene synthase proteins, respectively, of algae and higher plants. In addition, we investigated the effects of light stress on the expression of crtE and crtB in E. gracilis. Continuous illumination at 460 or 920 ?mol m(-2) s(-1) at 25 °C decreased the E. gracilis cell concentration by 28-40 % and 13-91 %, respectively, relative to the control light intensity (55 ?mol m(-2) s(-1)). When grown under continuous light at 920 ?mol m(-2) s(-1), the algal cells turned reddish-orange and showed a 1.3-fold increase in the crtB expression. In contrast, EgcrtE expression was not significantly affected by the light-stress treatments examined. CONCLUSIONS:We identified genes encoding CrtE and CrtB in E. gracilis and found that their protein products catalyze the early steps of carotenoid biosynthesis. Further, we found that the response of the carotenoid biosynthetic pathway to light stress in E. gracilis is controlled, at least in part, by the level of crtB transcription. This is the first functional analysis of crtE and crtB in Euglena.

Project description:BackgroundAs the first pathway-specific enzyme in carotenoid biosynthesis, phytoene synthase (PSY) is a prime regulatory target. This includes a number of biotechnological approaches that have successfully increased the carotenoid content in agronomically relevant non-green plant tissues through tissue-specific PSY overexpression. We investigated the differential effects of constitutive AtPSY overexpression in green and non-green cells of transgenic Arabidopsis lines. This revealed striking similarities to the situation found in orange carrot roots with respect to carotenoid amounts and sequestration mechanism.Methodology/principal findingsIn Arabidopsis seedlings, carotenoid content remained unaffected by increased AtPSY levels although the protein was almost quantitatively imported into plastids, as shown by western blot analyses. In contrast, non-photosynthetic calli and roots overexpressing AtPSY accumulated carotenoids 10 and 100-fold above the corresponding wild-type tissues and contained 1800 and 500 microg carotenoids per g dry weight, respectively. This increase coincided with a change of the pattern of accumulated carotenoids, as xanthophylls decreased relative to beta-carotene and carotene intermediates accumulated. As shown by polarization microscopy, carotenoids were found deposited in crystals, similar to crystalline-type chromoplasts of non-green tissues present in several other taxa. In fact, orange-colored carrots showed a similar situation with increased PSY protein as well as carotenoid levels and accumulation patterns whereas wild white-rooted carrots were similar to Arabidopsis wild type roots in this respect. Initiation of carotenoid crystal formation by increased PSY protein amounts was further confirmed by overexpressing crtB, a bacterial PSY gene, in white carrots, resulting in increased carotenoid amounts deposited in crystals.ConclusionsThe sequestration of carotenoids into crystals can be driven by the functional overexpression of one biosynthetic enzyme in non-green plastids not requiring a chromoplast developmental program as this does not exist in Arabidopsis. Thus, PSY expression plays a major, rate-limiting role in the transition from white to orange-colored carrots.

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An update on carotenoid biosynthesis in algae: phylogenetic evidence for the existence of two classes of phytoene synthase.

Publications

An update on carotenoid biosynthesis in algae: phylogenetic evidence for the existence of two classes of phytoene synthase.

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