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Trichome regulator SlMIXTA-like directly manipulates primary metabolism in tomato fruit.

ABSTRACT: Trichomes are storage compartments for specialized metabolites in many plant species. In trichome, plant primary metabolism is significantly changed, providing substrates for downstream secondary metabolism. However, little is known of how plants coordinate trichome formation and primary metabolism regulation. In this report, tomato (Solanum lycopersicum) trichome regulator SlMIXTA-like is indicated as a metabolic regulation gene by mGWAS analysis. Overexpression of SlMIXTA-like in tomato fruit enhances trichome formation. In addition, SlMIXTA-like can directly bind to the promoter region of gene encoding 3-deoxy-7-phosphoheptulonate synthase (SlDAHPS) to activate its expression. Induction of SlDAHPS expression enhances shikimate pathway activities and provides substrates for downstream secondary metabolism. Our data provide direct evidence that trichome regulator can directly manipulate primary metabolism, in which way plants can coordinate metabolic regulation and the formation of storage compartments for specialized metabolites. The newly identified SlMIXTA-like can be used for future metabolic engineering.

SUBMITTER: Ying S

PROVIDER: S-EPMC6953195 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Trichome regulator SlMIXTA-like directly manipulates primary metabolism in tomato fruit.

Ying Shiyu S Su Min M Wu Yu Y Zhou Lu L Fu Rao R Li Yan Y Guo Hao H Luo Jie J Wang Shouchuang S Zhang Yang Y

Plant biotechnology journal 20190724 2

Trichomes are storage compartments for specialized metabolites in many plant species. In trichome, plant primary metabolism is significantly changed, providing substrates for downstream secondary metabolism. However, little is known of how plants coordinate trichome formation and primary metabolism regulation. In this report, tomato (Solanum lycopersicum) trichome regulator SlMIXTA-like is indicated as a metabolic regulation gene by mGWAS analysis. Overexpression of SlMIXTA-like in tomato fruit ...[more]

PMID: 31254436

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Project description:BACKGROUND: Tomato (Solanum lycopersicum) establishes a beneficial symbiosis with arbuscular mycorrhizal (AM) fungi. The formation of the mycorrhizal association in the roots leads to plant-wide modulation of gene expression. To understand the systemic effect of the fungal symbiosis on the tomato fruit, we used RNA-Seq to perform global transcriptome profiling on Moneymaker tomato fruits at the turning ripening stage. RESULTS: Fruits were collected at 55 days after flowering, from plants colonized with Funneliformis mosseae and from control plants, which were fertilized to avoid responses related to nutrient deficiency. Transcriptome analysis identified 712 genes that are differentially expressed in fruits from mycorrhizal and control plants. Gene Ontology (GO) enrichment analysis of these genes showed 81 overrepresented functional GO classes. Up-regulated GO classes include photosynthesis, stress response, transport, amino acid synthesis and carbohydrate metabolism functions, suggesting a general impact of fungal symbiosis on primary metabolisms and, particularly, on mineral nutrition. Down-regulated GO classes include cell wall, metabolism and ethylene response pathways. Quantitative RT-PCR validated the RNA-Seq results for 12 genes out of 14 when tested at three fruit ripening stages, mature green, breaker and turning. Quantification of fruit nutraceutical and mineral contents produced values consistent with the expression changes observed by RNA-Seq analysis. CONCLUSIONS: This RNA-Seq profiling produced a novel data set that explores the intersection of mycorrhization and fruit development. We found that the fruits of mycorrhizal plants show two transcriptomic "signatures": genes characteristic of a climacteric fleshy fruit, and genes characteristic of mycorrhizal status, like phosphate and sulphate transporters. Moreover, mycorrhizal plants under low nutrient conditions produce fruits with a nutrient content similar to those from non-mycorrhizal plants under high nutrient conditions, indicating that AM fungi can help replace exogenous fertilizer for fruit crops.

Project description:Parthenocarpic tomato can set fruit and develop without pollination and exogenous hormone treatments under unfavorable environmental conditions, which is beneficial to tomato production from late fall to early spring in greenhouses. In this study, the endogenous hormones in the ovaries of the parthenocarpic tomato line "R35-P" (stigma removed or self-pollination) and the non-parthenocarpic tomato line "R35-N" (self-pollination) at four stages between preanthesis and postanthesis investigated, using high-performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). A nearly twofold IAA (indoleacetic acid) content was found in "R35-P" rather than in "R35-N" at -2 and 0 days after anthesis (DAA). Except at -2 DAA, a lower ABA (abscisic acid) content was observed in Pe (stigma removed in "R35-P") compared to that in Ps (self-pollination in "R35-P") or CK (self-pollination in "R35-N"). After pollination, although the content of GA1 (gibberellins acid 1) in CK increased, the levels of GAs (gibberellins acids) were notably low. At all four stages, a lower SA (salicylic acid) content was found in Ps and CK than in Pe, while the content and the change trend were similar in Ps and CK. The variation tendencies of JA (jasmonic acid) varied among Pe, Ps, and CK at the studied periods. Furthermore, KEGG (Kyoto Encyclopedia of Genes and Genomes) enrichment analyses of transcriptomic data identified 175 differentially expressed genes (DEGs) related to plant hormone signal transduction, including 63 auxin-related genes, 27 abscisic acid-related genes, 22 ethylene-related genes, 16 cytokinin-related genes, 16 salicylic acid-related genes, 14 brassinosteroid-related genes, 13 jasmonic acid-related genes, and 4 gibberellin-related genes at -2 DAA and 0 DAA. Our results suggest that the fate of a fruit set or degeneration occurred before anthesis in tomato. Auxins, whose levels were independent of pollination and fertilization, play prominent roles in controlling a fruit set in "R35-P," and other hormones are integrated in a synergistic or antagonistic way.

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Trichome regulator SlMIXTA-like directly manipulates primary metabolism in tomato fruit.

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Trichome regulator SlMIXTA-like directly manipulates primary metabolism in tomato fruit.

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