Dataset Information

Ubiquitination of phytoene synthase 1 precursor modulates carotenoid biosynthesis in tomato.

ABSTRACT: Carotenoids are natural pigments that are indispensable to plants and humans, whereas the regulation of carotenoid biosynthesis by post-translational modification remains elusive. Here, we show that a tomato E3 ubiquitin ligase, Plastid Protein Sensing RING E3 ligase 1 (PPSR1), is responsible for the regulation of carotenoid biosynthesis. PPSR1 exhibits self-ubiquitination activity and loss of PPSR1 function leads to an increase in carotenoids in tomato fruit. PPSR1 affects the abundance of 288 proteins, including phytoene synthase 1 (PSY1), the key rate-limiting enzyme in the carotenoid biosynthetic pathway. PSY1 contains two ubiquitinated lysine residues (Lys380 and Lys406) as revealed by the global analysis and characterization of protein ubiquitination. We provide evidence that PPSR1 interacts with PSY1 precursor protein and mediates its degradation via ubiquitination, thereby affecting the steady-state level of PSY1 protein. Our findings not only uncover a regulatory mechanism for controlling carotenoid biosynthesis, but also provide a strategy for developing carotenoid-enriched horticultural crops.

SUBMITTER: Wang P

PROVIDER: S-EPMC7713427 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Ubiquitination of phytoene synthase 1 precursor modulates carotenoid biosynthesis in tomato.

Wang Peiwen P Wang Yuying Y Wang Weihao W Chen Tong T Tian Shiping S Qin Guozheng G

Communications biology 20201203 1

Carotenoids are natural pigments that are indispensable to plants and humans, whereas the regulation of carotenoid biosynthesis by post-translational modification remains elusive. Here, we show that a tomato E3 ubiquitin ligase, Plastid Protein Sensing RING E3 ligase 1 (PPSR1), is responsible for the regulation of carotenoid biosynthesis. PPSR1 exhibits self-ubiquitination activity and loss of PPSR1 function leads to an increase in carotenoids in tomato fruit. PPSR1 affects the abundance of 288 ...[more]

PMID: 33273697

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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:Phytoene is a tomato carotenoid that may contribute to the apparent health benefits of tomato consumption. Although phytoene is a less prominent tomato carotenoid than lycopene, it is a major carotenoid in various human tissues. Phytoene distribution to plasma lipoproteins and tissues differs from lycopene, suggesting the kinetics of phytoene and lycopene differ.The objective of this study was to characterize the kinetic parameters of phytoene absorption, distribution, and excretion in adults, to better understand why biodistribution of phytoene differs from lycopene.Four adults (2 males, 2 females) maintained a controlled phytoene diet (1-5 mg/d) for 42 d. On day 14, each consumed 3.2 mg (13)C-phytoene, produced using tomato cell suspension culture technology. Blood samples were collected at 0, 1-15, 17, 21, and 24 h and 2, 3, 4, 7, 10, 14, 17, 21, and 28 d after (13)C-phytoene consumption. Plasma-unlabeled and plasma-labeled phytoene concentrations were determined using ultra-HPLC-quadrupole time-of-flight-mass spectrometry, and data were fit to a 7-compartment carotenoid kinetic model using WinSAAM 3.0.7 software.Subjects were compliant with a controlled phytoene diet, consuming a mean ± SE of 2.5 ± 0.6 mg/d, resulting in a plasma unlabeled phytoene concentration of 71 ± 14 nmol/L. A maximal plasma (13)C-phytoene concentration of 55.6 ± 5.9 nM was achieved 19.8 ± 9.2 h after consumption, and the plasma half-life was 2.3 ± 0.2 d. Compared with previous results for lycopene, phytoene bioavailability was nearly double at 58% ± 19%, the clearance rate from chylomicrons was slower, and the rates of deposition into and utilization by the slow turnover tissue compartment were nearly 3 times greater.Although only differing from lycopene by 4 double bonds, phytoene exhibits markedly different kinetic characteristics in human plasma, providing insight into metabolic processes contributing to phytoene enrichment in plasma and tissues compared with lycopene. This trial was registered at clinicaltrials.gov as NCT01692340.

Dataset Information

Ubiquitination of phytoene synthase 1 precursor modulates carotenoid biosynthesis in tomato.

Publications

Ubiquitination of phytoene synthase 1 precursor modulates carotenoid biosynthesis in tomato.

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