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Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest

BACKGROUND: Mature fruit cracking during the normal season in African Pride (AP) atemoya is a major problem in postharvest storage. Our current understanding of the molecular mechanism underlying fruit cracking is limited. The aim of this study was to unravel the role starch degradation and cell wal...

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Autores principales: Chen, Jingjing, Duan, Yajie, Hu, Yulin, Li, Weiming, Sun, Dequan, Hu, Huigang, Xie, Jianghui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6537181/
https://www.ncbi.nlm.nih.gov/pubmed/31132986
http://dx.doi.org/10.1186/s12870-019-1756-4
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author Chen, Jingjing
Duan, Yajie
Hu, Yulin
Li, Weiming
Sun, Dequan
Hu, Huigang
Xie, Jianghui
author_facet Chen, Jingjing
Duan, Yajie
Hu, Yulin
Li, Weiming
Sun, Dequan
Hu, Huigang
Xie, Jianghui
author_sort Chen, Jingjing
collection PubMed
description BACKGROUND: Mature fruit cracking during the normal season in African Pride (AP) atemoya is a major problem in postharvest storage. Our current understanding of the molecular mechanism underlying fruit cracking is limited. The aim of this study was to unravel the role starch degradation and cell wall polysaccharide metabolism in fruit ripening and cracking after harvest through transcriptome analysis. RESULTS: Transcriptome analysis of AP atemoya pericarp from cracking fruits of ethylene treatments and controls was performed. KEGG pathway analysis revealed that the starch and sucrose metabolism pathway was significantly enriched, and approximately 39 DEGs could be functionally annotated, which included starch, cellulose, pectin, and other sugar metabolism-related genes. Starch, protopectin, and soluble pectin contents among the different cracking stages after ethylene treatment and the controls were monitored. The results revealed that ethylene accelerated starch degradation, inhibited protopectin synthesis, and enhanced the soluble pectin content, compared to the control, which coincides with the phenotype of ethylene-induced fruit cracking. Key genes implicated in the starch, pectin, and cellulose degradation were further investigated using RT-qPCR analysis. The results revealed that alpha-amylase 1 (AMY1), alpha-amylase 3 (AMY3), beta-amylase 1 (BAM1), beta-amylase 3 (BAM3), beta-amylase 9 (BAM9), pullulanase (PUL), and glycogen debranching enzyme (glgX), were the major genes involved in starch degradation. AMY1, BAM3, BAM9, PUL, and glgX all were upregulated and had higher expression levels with ethylene treatment compared to the controls, suggesting that ethylene treatment may be responsible for accelerating starch degradation. The expression profile of alpha-1,4-galacturonosyltransferase (GAUT) and granule-bound starch synthase (GBSS) coincided with protopectin content changes and could involve protopectin synthesis. Pectinesterase (PE), polygalacturonase (PG), and pectate lyase (PEL) all involved in pectin degradation; PE was significantly upregulated by ethylene and was the key enzyme implicated pectin degradation. CONCLUSION: Both KEGG pathway enrichment analysis of DEGs and material content analysis confirmed that starch decomposition into soluble sugars and cell wall polysaccharides metabolism are closely related to the ripening and cracking of AP atemoya. A link between gene up- or downregulation during different cracking stages of atemoya fruits and how their expression affects starch and pectin contents were established by RT-qPCR analysis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1756-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-65371812019-05-30 Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest Chen, Jingjing Duan, Yajie Hu, Yulin Li, Weiming Sun, Dequan Hu, Huigang Xie, Jianghui BMC Plant Biol Research Article BACKGROUND: Mature fruit cracking during the normal season in African Pride (AP) atemoya is a major problem in postharvest storage. Our current understanding of the molecular mechanism underlying fruit cracking is limited. The aim of this study was to unravel the role starch degradation and cell wall polysaccharide metabolism in fruit ripening and cracking after harvest through transcriptome analysis. RESULTS: Transcriptome analysis of AP atemoya pericarp from cracking fruits of ethylene treatments and controls was performed. KEGG pathway analysis revealed that the starch and sucrose metabolism pathway was significantly enriched, and approximately 39 DEGs could be functionally annotated, which included starch, cellulose, pectin, and other sugar metabolism-related genes. Starch, protopectin, and soluble pectin contents among the different cracking stages after ethylene treatment and the controls were monitored. The results revealed that ethylene accelerated starch degradation, inhibited protopectin synthesis, and enhanced the soluble pectin content, compared to the control, which coincides with the phenotype of ethylene-induced fruit cracking. Key genes implicated in the starch, pectin, and cellulose degradation were further investigated using RT-qPCR analysis. The results revealed that alpha-amylase 1 (AMY1), alpha-amylase 3 (AMY3), beta-amylase 1 (BAM1), beta-amylase 3 (BAM3), beta-amylase 9 (BAM9), pullulanase (PUL), and glycogen debranching enzyme (glgX), were the major genes involved in starch degradation. AMY1, BAM3, BAM9, PUL, and glgX all were upregulated and had higher expression levels with ethylene treatment compared to the controls, suggesting that ethylene treatment may be responsible for accelerating starch degradation. The expression profile of alpha-1,4-galacturonosyltransferase (GAUT) and granule-bound starch synthase (GBSS) coincided with protopectin content changes and could involve protopectin synthesis. Pectinesterase (PE), polygalacturonase (PG), and pectate lyase (PEL) all involved in pectin degradation; PE was significantly upregulated by ethylene and was the key enzyme implicated pectin degradation. CONCLUSION: Both KEGG pathway enrichment analysis of DEGs and material content analysis confirmed that starch decomposition into soluble sugars and cell wall polysaccharides metabolism are closely related to the ripening and cracking of AP atemoya. A link between gene up- or downregulation during different cracking stages of atemoya fruits and how their expression affects starch and pectin contents were established by RT-qPCR analysis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1756-4) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-27 /pmc/articles/PMC6537181/ /pubmed/31132986 http://dx.doi.org/10.1186/s12870-019-1756-4 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Chen, Jingjing
Duan, Yajie
Hu, Yulin
Li, Weiming
Sun, Dequan
Hu, Huigang
Xie, Jianghui
Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest
title Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest
title_full Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest
title_fullStr Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest
title_full_unstemmed Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest
title_short Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest
title_sort transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6537181/
https://www.ncbi.nlm.nih.gov/pubmed/31132986
http://dx.doi.org/10.1186/s12870-019-1756-4
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