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Edited by Zachary B. Lippman, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, and accepted by Editorial Board Member Joseph R. Ecker August 3, 2020 (received for review June 26, 2020)
Significance
Fruit set, which is triggered by the phytohormone gibberellin (GA), is the developmental transition of ovaries into fruits. Our multiomics approaches revealed that PROCERA-dependent GA responses rewired central carbon metabolism, predominantly under transcriptional control. The kinetic analysis approach used in this study enabled us to construct a carbon flux model of the earliest processes that occur during fruit set. The model revealed that fruit set coincided with the temporal changes in sugar compartmentalization due to the coordinated actions of the enzymes and tonoplastic carriers and highlighted that fructokinase likely contributed to early ovary growth by pulling fructose out of the vacuole to feed the downstream pathways for biosynthesis of cell wall components and energy provision.
Abstract
Fruit set is the process whereby ovaries develop into fruits after pollination and fertilization. The process is induced by the phytohormone gibberellin (GA) in tomatoes, as determined by the constitutive GA response mutant procera. However, the role of GA on the metabolic behavior in fruit-setting ovaries remains largely unknown. This study explored the biochemical mechanisms of fruit set using a network analysis of integrated transcriptome, proteome, metabolome, and enzyme activity data. Our results revealed that fruit set involves the activation of central carbon metabolism, with increased hexoses, hexose phosphates, and downstream metabolites, including intermediates and derivatives of glycolysis, the tricarboxylic acid cycle, and associated organic and amino acids. The network analysis also identified the transcriptional hub gene SlHB15A, that coordinated metabolic activation. Furthermore, a kinetic model of sucrose metabolism predicted that the sucrose cycle had high activity levels in unpollinated ovaries, whereas it was shut down when sugars rapidly accumulated in vacuoles in fruit-setting ovaries, in a time-dependent manner via tonoplastic sugar carriers. Moreover, fruit set at least partly required the activity of fructokinase, which may pull fructose out of the vacuole, and this could feed the downstream pathways. Collectively, our results indicate that GA cascades enhance sink capacities, by up-regulating central metabolic enzyme capacities at both transcriptional and posttranscriptional levels. This leads to increased sucrose uptake and carbon fluxes for the production of the constituents of biomass and energy that are essential for rapid ovary growth during the initiation of fruit set.
Footnotes
↵1Present address: Institute of Global Innovation Research, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-8509, Japan.
- ↵2To whom correspondence may be addressed. Email: ariizumi.toru.ge{at}u.tsukuba.ac.jp.
Author contributions: T.A. designed research; Y. Shinozaki, B.P.B., M.T., S.H., K.E., M.-H.A., K.N., Y. Suzuki, H. Enomoto, M. Kusano, T.M., M. Kojima, M. Kobayashi, Y.O., C.B., D.P., and T.A. performed research; Y. Shinozaki, B.P.B., K.M., S.K., A.F., H.S., K.S., Y.G., and T.A. analyzed data; and Y. Shinozaki, B.P.B., Y.G., H. Ezura, and T.A. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission. Z.B.L. is a guest editor invited by the Editorial Board.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2011859117/-/DCSupplemental.
Data Availability.
Nucleotide sequence data have been deposited in DNA Data Bank of Japan (DDBJ) Sequence Read Archive (DRA010267). All study data are included in the article and supporting information.
Published under the PNAS license.
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Fruit setting rewires central metabolism via gibberellin cascades
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