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Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit.

ABSTRACT: Respiration of bulky plant organs such as fleshy fruits depends on oxygen (O₂) availability and often decreases with O₂ concentration to avoid anoxia, but the relationship between O₂ diffusional resistance and metabolic adjustments remains unclear. Melon fruit (Cucumis melo L.) was used to study relationships between O₂ availability and metabolism in fleshy fruits. Enzyme activities, primary metabolites and O₂ partial pressure were quantified from the periphery to the inner fruit mesocarp, at three stages of development. Hypoxia was gradually established during fruit development, but there was no strong oxygen gradient between the outer- and the inner mesocarp. These trends were confirmed by a mathematical modeling approach combining O₂ diffusion equations and O₂ demand estimates of the mesocarp tissue. A multivariate analysis of metabolites, enzyme activities, O₂ demand and concentration reveals that metabolite gradients and enzyme capacities observed in melon fruits reflect continuous metabolic adjustments thus ensuring a timely maturation of the mesocarp. The present results suggest that the metabolic adjustments, especially the tuning of the capacity of cytochrome c oxidase (COX) to O₂-availability that occurs during growth development, contribute to optimizing the O₂-demand and avoiding the establishment of an O₂ gradient within the flesh.

SUBMITTER: Mori K

PROVIDER: S-EPMC6529934 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundIn climacteric fruit-bearing species, the onset of fruit ripening is marked by a transient rise in respiration rate and autocatalytic ethylene production, followed by rapid deterioration in fruit quality. In non-climacteric species, there is no increase in respiration or ethylene production at the beginning or during fruit ripening. Melon is unusual in having climacteric and non-climacteric varieties, providing an interesting model system to compare both ripening types. Transcriptomic analysis of developing melon fruits from Védrantais and Dulce (climacteric) and Piel de sapo and PI 161375 (non-climacteric) varieties was performed to understand the molecular mechanisms that differentiate the two fruit ripening types.ResultsFruits were harvested at 15, 25, 35 days after pollination and at fruit maturity. Transcript profiling was performed using an oligo-based microarray with 75 K probes. Genes linked to characteristic traits of fruit ripening were differentially expressed between climacteric and non-climacteric types, as well as several transcription factor genes and genes encoding enzymes involved in sucrose catabolism. The expression patterns of some genes in PI 161375 fruits were either intermediate between. Piel de sapo and the climacteric varieties, or more similar to the latter. PI 161375 fruits also accumulated some carotenoids, a characteristic trait of climacteric varieties.ConclusionsSimultaneous changes in transcript abundance indicate that there is coordinated reprogramming of gene expression during fruit development and at the onset of ripening in both climacteric and non-climacteric fruits. The expression patterns of genes related to ethylene metabolism, carotenoid accumulation, cell wall integrity and transcriptional regulation varied between genotypes and was consistent with the differences in their fruit ripening characteristics. There were differences between climacteric and non-climacteric varieties in the expression of genes related to sugar metabolism suggesting that they may be potential determinants of sucrose content and post-harvest stability of sucrose levels in fruit. Several transcription factor genes were also identified that were differentially expressed in both types, implicating them in regulation of ripening behaviour. The intermediate nature of PI 161375 suggested that classification of melon fruit ripening behaviour into just two distinct types is an over-simplification, and that in reality there is a continuous spectrum of fruit ripening behaviour.

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Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit.

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