RRC ID 60947
Author Shinozaki Y, Beauvoit BP, Takahara M, Hao S, Ezura K, Andrieu MH, Nishida K, Mori K, Suzuki Y, Kuhara S, Enomoto H, Kusano M, Fukushima A, Mori T, Kojima M, Kobayashi M, Sakakibara H, Saito K, Ohtani Y, Bénard C, Prodhomme D, Gibon Y, Ezura H, Ariizumi T.
Title Fruit setting rewires central metabolism via gibberellin cascades.
Journal Proc Natl Acad Sci U S A
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.
Volume 117(38)
Pages 23970-23981
Published 2020-9-22
DOI 10.1073/pnas.2011859117
PII 2011859117
PMID 32883877
PMC PMC7519230
MeSH Carbon / metabolism Fruit* / genetics Fruit* / growth & development Fruit* / metabolism Gibberellins / metabolism* Metabolic Networks and Pathways / genetics Plant Growth Regulators / metabolism* Plant Proteins / genetics Plant Proteins / metabolism Plants, Genetically Modified / genetics Plants, Genetically Modified / growth & development Plants, Genetically Modified / metabolism Solanum lycopersicum / genetics Solanum lycopersicum / growth & development Solanum lycopersicum / metabolism Sucrose / metabolism Transcriptome / genetics
IF 9.412
Tomato TOMJPF00001(Micro-Tom)