Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early development

Abstract Background The major fleshy tissues of the apple fruit are spatially separable into cortex and pith. These tissues display differential growth during development. Key features of such differential growth, and sink metabolic programs supporting it have not been investigated previously. We hy...

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Main Authors: Shan Jing, Anish Malladi
Format: Article
Language:English
Published: BMC 2020-02-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-020-2280-2
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spelling doaj-58aac4626ab14fffa8e4feed522c08142021-02-14T12:17:26ZengBMCBMC Plant Biology1471-22292020-02-0120111910.1186/s12870-020-2280-2Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early developmentShan Jing0Anish Malladi1Department of Horticulture, University of GeorgiaDepartment of Horticulture, University of GeorgiaAbstract Background The major fleshy tissues of the apple fruit are spatially separable into cortex and pith. These tissues display differential growth during development. Key features of such differential growth, and sink metabolic programs supporting it have not been investigated previously. We hypothesized that differential growth between these fruit tissues is supported by differential sink metabolic programs, particularly during early development. Growth, metabolite concentrations, and transcript abundance of metabolism-related genes were measured to determine characteristics of differential growth and their underlying metabolic programs. Results The cortex displayed > 5-fold higher growth than the pith during early fruit development, indicating that differential growth was established during this period. Further, when resource availability was increased through sink-removal, cortex growth was preferentially enhanced. Greatest diversity in metabolic programs between these tissues was evident during early fruit development. Higher cortex growth during early development was facilitated by increased catabolism of imported carbon (C) resources, sorbitol and sucrose, and the nitrogen (N) resource, asparagine. It was also associated with enhanced primary C metabolism, and C storage as malate and quinate. The pith metabolic program during this period involved limited allocation of C and N to growth, but greater allocation to storage, and enhanced sucrose-sucrose cycling. Conclusions Together, these data indicate that the fruit cortex tissue displays a resource intensive metabolic program during early fruit development. This provides the C backbones, proteins, energy and osmolytes to support its higher growth.https://doi.org/10.1186/s12870-020-2280-2Carbon metabolismCell productionFruit growth and developmentFruit load reductionMetabolic profilingNitrogen metabolism
collection DOAJ
language English
format Article
sources DOAJ
author Shan Jing
Anish Malladi
spellingShingle Shan Jing
Anish Malladi
Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early development
BMC Plant Biology
Carbon metabolism
Cell production
Fruit growth and development
Fruit load reduction
Metabolic profiling
Nitrogen metabolism
author_facet Shan Jing
Anish Malladi
author_sort Shan Jing
title Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early development
title_short Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early development
title_full Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early development
title_fullStr Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early development
title_full_unstemmed Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early development
title_sort higher growth of the apple (malus × domestica borkh.) fruit cortex is supported by resource intensive metabolism during early development
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2020-02-01
description Abstract Background The major fleshy tissues of the apple fruit are spatially separable into cortex and pith. These tissues display differential growth during development. Key features of such differential growth, and sink metabolic programs supporting it have not been investigated previously. We hypothesized that differential growth between these fruit tissues is supported by differential sink metabolic programs, particularly during early development. Growth, metabolite concentrations, and transcript abundance of metabolism-related genes were measured to determine characteristics of differential growth and their underlying metabolic programs. Results The cortex displayed > 5-fold higher growth than the pith during early fruit development, indicating that differential growth was established during this period. Further, when resource availability was increased through sink-removal, cortex growth was preferentially enhanced. Greatest diversity in metabolic programs between these tissues was evident during early fruit development. Higher cortex growth during early development was facilitated by increased catabolism of imported carbon (C) resources, sorbitol and sucrose, and the nitrogen (N) resource, asparagine. It was also associated with enhanced primary C metabolism, and C storage as malate and quinate. The pith metabolic program during this period involved limited allocation of C and N to growth, but greater allocation to storage, and enhanced sucrose-sucrose cycling. Conclusions Together, these data indicate that the fruit cortex tissue displays a resource intensive metabolic program during early fruit development. This provides the C backbones, proteins, energy and osmolytes to support its higher growth.
topic Carbon metabolism
Cell production
Fruit growth and development
Fruit load reduction
Metabolic profiling
Nitrogen metabolism
url https://doi.org/10.1186/s12870-020-2280-2
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