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

Authors: MCQUINN, RYAN - Cornell University; GAPPER, NIGEL - Boyce Thompson Institute; GRAY, AMANDA - Boyce Thompson Institute; ZHONG, SILIN - Boyce Thompson Institute; TOHGE, TAKAYUKI - Max Planck Institute Of Molecular Plant Physiology; FEI, ZHANGJUN - Boyce Thompson Institute; FERNIE, ALISDAIR - Max Planck Institute Of Molecular Plant Physiology; Giovannoni, James

Submitted to: Plant Biotechnology Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/21/2020
Publication Date: 3/14/2020
Citation: Mcquinn, R., Gapper, N., Gray, A., Zhong, S., Tohge, T., Fei, Z., Fernie, A., Giovannoni, J.J. 2020. Manipulation of ZDS in tomato exposes carotenoid- and ABA-specific effects on fruit development and ripening. Plant Biotechnology Journal. https://doi.org/10.1111/pbi.13377.
DOI: https://doi.org/10.1111/pbi.13377

Interpretive Summary: Carotenoids play pivotal roles throughout plant development, among the most observable being coloration of ripe fruit and flowers for attraction of seed dispersing animals and pollinators. They also have nutritional quality and contribute to health attributes of fruits and vegetables. A key step in carotenoid synthesis is catalyzed by the enzyme ZDS. In this study we manipulated ZDS in tomato to show the potential of this enzyme and the gene encoding it for elevating fruit nutritional quality. We also demonstrate that a downstream product of the activity of this enzyme, abscisic acid or ABA, is a regulator of ripening and lowering ABA via manipulation of ZDS results in extended fruit shelf-life.

Technical 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 master regulators 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 gama-carotene isomers and upstream carotenoids, while downstream all trans-lycopene and subsequent photoprotective carotenes and xanthophylls were diminished. Consequently, immature fruit displayed photobleaching 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 were devoid of the characteristic red carotenoid, all trans-lycopene, and displayed brilliant yellow pigmentation due to elevated 9,9’ di-cis-gama-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 alteration and reveal a unique and dynamic gama-carotene isomer profile in ripe fruit.