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Manipulation of ZDS in tomato exposes carotenoid- and ABA-specific effects on fruit development and ripening.

ABSTRACT: Spontaneous mutations in fruit-specific carotenoid biosynthetic genes of tomato (Solanum lycopersicum) have led to improved understanding of ripening-associated carotenogenesis. Here, we confirm that ZDS is encoded by a single gene in tomato transcriptionally regulated by ripening transcription factors RIN, NOR and ethylene. Manipulation of ZDS was achieved through transgenic repression and heterologous over-expression in tomato. CaMV 35S-driven RNAi repression inhibited carotenoid biosynthesis in all aerial tissues examined resulting in elevated levels of ?-carotene isomers and upstream carotenoids, while downstream all trans-lycopene and subsequent photoprotective carotenes and xanthophylls were diminished. Consequently, immature fruit displayed photo-bleaching consistent with reduced levels of the photoprotective carotenes and developmental phenotypes related to a reduction in the carotenoid-derived phytohormone abscisic acid (ABA). ZDS-repressed ripe fruit was devoid of the characteristic red carotenoid, all trans-lycopene and displayed brilliant yellow pigmentation due to elevated 9,9' di-cis-?-carotene. Over-expression of the Arabidopsis thaliana ZDS (AtZDS) gene bypassed endogenous co-suppression and revealed ZDS as an additional bottleneck in ripening-associated carotenogenesis of tomato. Quantitation of carotenoids in addition to multiple ripening parameters in ZDS-altered lines and ABA-deficient fruit-specific carotenoid mutants was used to separate phenotypic consequences of ABA from other effects of ZDS manipulation and reveal a unique and dynamic ?-carotene isomer profile in ripe fruit.

SUBMITTER: McQuinn RP

PROVIDER: S-EPMC7589306 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Manipulation of ZDS in tomato exposes carotenoid- and ABA-specific effects on fruit development and ripening.

McQuinn Ryan P RP Gapper Nigel E NE Gray Amanda G AG Zhong Silin S Tohge Takayuki T Fei Zhangjun Z Fernie Alisdair R AR Giovannoni James J JJ

Plant biotechnology journal 20200420 11

Spontaneous mutations in fruit-specific carotenoid biosynthetic genes of tomato (Solanum lycopersicum) have led to improved understanding of ripening-associated carotenogenesis. Here, we confirm that ZDS is encoded by a single gene in tomato transcriptionally regulated by ripening transcription factors RIN, NOR and ethylene. Manipulation of ZDS was achieved through transgenic repression and heterologous over-expression in tomato. CaMV 35S-driven RNAi repression inhibited carotenoid biosynthesis ...[more]

PMID: 32171044

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Project description:Purpose: The goals of this study was to provide genome-wide data to investigate the molecular mechanism of the interaction between ABA and ethylene during tomato fruit ripening Methods: Regarding the fruits sampled at the 9th day as a well-characterized stage, we used RNA-seq to conducted a comparative analysis of exogenous ABA and NDGA effects on all components involved in biosynthesis and signaling of ethylene and ABA.The identified crucial genes in response to ABA were further performed a ripening time-course analysis by RT-PCR. In addition, we also detected how ethylene affected ABA action at the onset of ripening by treating the fruits with 1-MCP immediately after ABA application. Results: Our study not only illustrated how ABA regulated itself at the transcription level, but also elucidated that ABA can facilitate ethylene production and response by regulating some crucial genes such as LeACS4, LeACO1 and LeETR6 etc. In addition, investigation on the fruits treated with 1-MCP immediately after ABA exposure revealed that ethylene might be essential for the induction of ABA biosynthesis and signaling at the onset of fruit ripening. Furthermore, some specific transcription factors (TFs) known as regulators of ethylene synthesis and sensibility (e.g. MADS-RIN, TAGL1, CNR and NOR etc.) were also observed to be ABA responsive, which implied that ABA influenced ethylene action possibly through the regulation of these TFs expression. Conclusions: Our data suggested that ABA may act as an upstream regulator to modulate ethylene synthesis and signal transduction, which consequently influenced the ripening process. This comprehensive survey not only demonstrated how ABA regulated itself at the molecular level, but also indicated that ABA had a positive impact on ethylene production and action by regulating key genes such as LeACS2, LeACS4, LeACO1 and LeETR6. Besides, our results also revealed that ethylene might be of great importance to induce ABA accumulation and response at the onset of ripening. Moreover, many ripening related TFs, such as MADS-RIN, TAGL1, CNR and NOR, were observed to be affected by ABA, implying that a TF-mediated manner may be involved in the interaction between ABA and ethylene. This study extends our understanding of the mechanism that how ABA-triggered tomato fruit ripening, and illustrates the complex mechanism of reciprocity between ABA and ethylene at the transcription level.

Project description:Light signaling and plant hormones, particularly ethylene and auxins, have been identified as important regulators of carotenoid biosynthesis during tomato fruit ripening. However, whether and how the light and hormonal signaling cascades crosstalk to control this metabolic route remain poorly elucidated. Here, the potential involvement of ethylene and auxins in the light-mediated regulation of tomato fruit carotenogenesis was investigated by comparing the impacts of light treatments and the light-hyperresponsive high pigment-2 (hp2) mutation on both carotenoid synthesis and hormonal signaling. Under either light or dark conditions, the overaccumulation of carotenoids in hp2 ripening fruits was associated with disturbed ethylene production, increased expression of genes encoding master regulators of ripening and higher ethylene sensitivity and signaling output. The increased ethylene sensitivity observed in hp2 fruits was associated with the differential expression of genes encoding ethylene receptors and downstream signaling transduction elements, including the downregulation of the transcription factor ETHYLENE RESPONSE FACTOR.E4, a repressor of carotenoid synthesis. Accordingly, treatments with exogenous ethylene promoted carotenoid biosynthetic genes more intensively in hp2 than in wild-type fruits. Moreover, the loss of HP2 function drastically altered auxin signaling in tomato fruits, resulting in higher activation of the auxin-responsive promoter DR5, severe down-regulation of AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) genes and altered accumulation of AUXIN RESPONSE FACTOR (ARF) transcripts. Both tomato ARF2 paralogues (Sl-ARF2a and SlARF2b) were up-regulated in hp2 fruits, which agrees with the promotive roles played by these ARFs in tomato fruit ripening and carotenoid biosynthesis. Among the genes differentially expressed in hp2 fruits, the additive effect of light treatment and loss of HP2 function was particularly evident for those encoding carotenoid biosynthetic enzymes, ethylene-related transcription factors, Aux/IAAs and ARFs. Altogether, the data uncover the involvement of ethylene and auxin as part of the light signaling cascades controlling tomato fruit metabolism and provide a new link between light signaling, plant hormone sensitivity and carotenoid metabolism in ripening fruits.

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Manipulation of ZDS in tomato exposes carotenoid- and ABA-specific effects on fruit development and ripening.

Publications

Manipulation of ZDS in tomato exposes carotenoid- and ABA-specific effects on fruit development and ripening.

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