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Reprogramming of primary metabolism facilitates metabolic engineering of bioactives in tomato fruit

ABSTRACT: Phenylpropanoids are derived from phenylalanine and comprise an important class of plant secondary metabolites that include specialized bioactives with medicinal properties, important phytonutrients, a broad range of natural colours, phytoanticipins, phytoalexins and phytoestrogens. A number of transcription factors have been used to upregulate specific branches of phenylpropanoid metabolism, but by far the most effective has been the fruit-specific expression of AtMYB12 in tomato, which resulted in an astonishing 10% of fruit dry weight accumulating as flavonoids and hydroxycinnamates. We show that AtMYB12 not only increases the demand of flavonoid biosynthesis, but also increases the supply of carbon from primary metabolism, and the supply of energy and reducing power, by upregulating glycolysis, the TCA cycle, the oxidative pentose phosphate pathway, fuelling the shikimate and phenylalanine biosynthetic pathways to supply more aromatic amino acids for secondary metabolism. AtMYB12 directly activates at least some genes encoding enzymes of primary metabolism. The enhanced supply of precursors, energy and reducing power achieved by AtMYB12 expression can be harnessed to engineer high levels of novel phenylpropanoids in tomato fruit, offering an effective production system for bioactives and other high value ingredients.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE61014 | GEO | 2015/10/07

SECONDARY ACCESSION(S): PRJNA260087

REPOSITORIES: GEO

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Project description:Tomato fruit ripening is under the control of ethylene as well as a group of ethylene-independent transcription factors, including NON-RIPENING (NOR) and RIPENING INHIBITOR (RIN). During ripening, the linear carotene lycopene accumulates at the expense of cyclic carotenoids. Fruit-specific overexpression of LYCOPENE β-CYCLASE (LCYb) under the control of the PHYTOENE DESATURASE (PDS) promoter resulted in increased levels of β-carotene and ABA and in decreased ethylene levels. Genes regulated by ABA, or involved in its synthesis and signaling, were overexpressed, while those associated with ethylene and cell wall remodeling were repressed. In agreement with the transcriptional data, LCYb-overexpressing fruits exhibited increased density of cell wall material containing linear, under-methylated pectins and displayed an array of additional ripening phenotypes, including delayed softening, increased turgor, enhanced shelf life and a thicker cuticle with a higher content of cutin monomers and triterpenoids. The levels of several primary metabolites and phenylpropanoids also changed in the transgenics, which could be attributed to delayed fruit ripening and to ABA respectively. Network correlation analysis suggests that ABA, acting through NOR and RIN, is responsible for many of the above phenotypes. These data reinforce suggestions that ABA plays an important role in tomato fruit ripening and provide clues that fruit b-carotene, acting as a precursor for ABA, actively participates in controlling the ripening process rather than merely being an output thereof. Overexpression of a LCYb gene from Arabidopsis under the control of the ripening-associated PDS promoter leads to ripe tomato fruits accumulating high β-carotene levels. Using several independent transgenic lines, we conducted a system-wide study of the effect of increased β-carotene levels on tomato fruit ripening and shelf life. Our data suggest that β-carotene, acting through ABA, is involved in a regulatory loop within the network controlling tomato fruit ripening.

Project description:Purpose: The goals of this study was to provide genome-wide data to investigate the molecular mechanism of ABA regulation in many ripening related biological processes, including fruit color variation, antioxidant capacity, flavonoids biosynthesis and photosynthesis. Methods:By applying the next generation sequencing technology, we conducted a comparative analysis of exogenous ABA and NDGA effects on tomato fruit maturation. Results:The high throughput sequencing results showed that 25728 genes expressed across all three samples, and 10388 of them were identified as significantly differently expressed genes (DEGs). Exogenous ABA was found to enhance the transcription of genes in pigments metabolism, including carotenoids biosynthesis and chlorophyll degradation, whereas NDGA treatment inhibited these progresses. The results also revealed the crucial role of ABA in flavonoids synthesis and regulation of antioxidant system. Intriguingly, we also found that an inhibition of endogenous ABA significantly enhanced the transcriptional abundance of genes involved in fruit photosynthesis. Conclusions:next-generation sequencing enabled us to characterize the transcriptomes of tomato fruit treated with ABA and NDGA. By comparing these transcriptomes with control respectively, we observed that ABA could accelerate fruit maturation by positively regulating many genes related to ripening processes. Our study have turned spotlight on the pathways of fruit pigmentation, including carotenoid biosynthesis and chlorophyll metabolism. Exogenous ABA was able to up-regulate many genes in relation to the carotenoids accumulation and chlorophyll breakdown, thus promoting the color transition of tomato fruit. In addition, ABA has the potential to improve the genes related to antioxidant capacity, such as SODs, CATs, APXs, GSTs, GPXs, TrXs and PrxRs. Besides, the expression changes of genes involved in flavonoids biosynthesis after ABA exposure was striking, suggesting ABA could enhance the defense response by producing more secondary metabolite in tomato fruit. Moreover, the sequencing results also implied high level of ABA could negatively affect photosynthesis of tomato fruit, which needs more investigations to explore the interaction between ABA and photosynthesis in the future.

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Reprogramming of primary metabolism facilitates metabolic engineering of bioactives in tomato fruit

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