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Transcriptome Analysis and Ultrastructure Observation Reveal that Hawthorn Fruit Softening Is due to Cellulose/Hemicellulose Degradation

Softening, a common phenomenon in many fruits, is a well coordinated and genetically determined process. However, the process of flesh softening during ripening has rarely been described in hawthorn. In this study, we found that ‘Ruanrou Shanlihong 3 Hao’ fruits became softer during ripening, wherea...

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Autores principales: Xu, Jiayu, Zhao, Yuhui, Zhang, Xiao, Zhang, Lijie, Hou, Yali, Dong, Wenxuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5063854/
https://www.ncbi.nlm.nih.gov/pubmed/27790234
http://dx.doi.org/10.3389/fpls.2016.01524
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author Xu, Jiayu
Zhao, Yuhui
Zhang, Xiao
Zhang, Lijie
Hou, Yali
Dong, Wenxuan
author_facet Xu, Jiayu
Zhao, Yuhui
Zhang, Xiao
Zhang, Lijie
Hou, Yali
Dong, Wenxuan
author_sort Xu, Jiayu
collection PubMed
description Softening, a common phenomenon in many fruits, is a well coordinated and genetically determined process. However, the process of flesh softening during ripening has rarely been described in hawthorn. In this study, we found that ‘Ruanrou Shanlihong 3 Hao’ fruits became softer during ripening, whereas ‘Qiu JinXing’ fruits remained hard. At late developmental stages, the firmness of ‘Ruanrou Shanlihong 3 Hao’ fruits rapidly declined, and that of ‘Qiu JinXing’ fruits remained essentially unchanged. According to transmission electron microscopy, the middle lamella of ‘Qiu JinXing’ and ‘Ruanrou Shanlihong 3 Hao’ fruit flesh was largely degraded as the fruits matured. Microfilaments in ‘Qiu JinXing’ flesh were arranged close together and were deep in color, whereas those in ‘Ruanrou Shanlihong 3 Hao’ fruit flesh were arranged loosely, partially degraded and light in color. RNA-Seq analysis yielded approximately 46.72 Gb of clean data and 72,837 unigenes. Galactose metabolism and pentose and glucuronate interconversions are involved in cell wall metabolism, play an important role in hawthorn texture. We identified 85 unigenes related to the cell wall between hard- and soft-fleshed hawthorn fruits. Based on data analysis and real-time PCR, we suggest that β-GAL and PE4 have important functions in early fruit softening. The genes Ffase, Gns,α-GAL, PE63, XTH, and CWP, which are involved in cell wall degradation, are responsible for the different textures of hawthorn fruits. Thus, we hypothesize that the different textures of ‘Qiu JinXing’ and ‘Ruanrou Shanlihong 3 Hao’ fruits at maturity mainly result from cellulose/hemicelluloses degradation rather than from lamella degradation. Overall, we propose that different types of hydrolytic enzymes in cells interact to degrade the cell wall, resulting in ultramicroscopic Structure changes in the cell wall and, consequently, fruit softening. These results provide fundamental insight regarding the mechanisms by which hawthorn fruits acquire different textures and also lay a solid foundation for further research.
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spelling pubmed-50638542016-10-27 Transcriptome Analysis and Ultrastructure Observation Reveal that Hawthorn Fruit Softening Is due to Cellulose/Hemicellulose Degradation Xu, Jiayu Zhao, Yuhui Zhang, Xiao Zhang, Lijie Hou, Yali Dong, Wenxuan Front Plant Sci Plant Science Softening, a common phenomenon in many fruits, is a well coordinated and genetically determined process. However, the process of flesh softening during ripening has rarely been described in hawthorn. In this study, we found that ‘Ruanrou Shanlihong 3 Hao’ fruits became softer during ripening, whereas ‘Qiu JinXing’ fruits remained hard. At late developmental stages, the firmness of ‘Ruanrou Shanlihong 3 Hao’ fruits rapidly declined, and that of ‘Qiu JinXing’ fruits remained essentially unchanged. According to transmission electron microscopy, the middle lamella of ‘Qiu JinXing’ and ‘Ruanrou Shanlihong 3 Hao’ fruit flesh was largely degraded as the fruits matured. Microfilaments in ‘Qiu JinXing’ flesh were arranged close together and were deep in color, whereas those in ‘Ruanrou Shanlihong 3 Hao’ fruit flesh were arranged loosely, partially degraded and light in color. RNA-Seq analysis yielded approximately 46.72 Gb of clean data and 72,837 unigenes. Galactose metabolism and pentose and glucuronate interconversions are involved in cell wall metabolism, play an important role in hawthorn texture. We identified 85 unigenes related to the cell wall between hard- and soft-fleshed hawthorn fruits. Based on data analysis and real-time PCR, we suggest that β-GAL and PE4 have important functions in early fruit softening. The genes Ffase, Gns,α-GAL, PE63, XTH, and CWP, which are involved in cell wall degradation, are responsible for the different textures of hawthorn fruits. Thus, we hypothesize that the different textures of ‘Qiu JinXing’ and ‘Ruanrou Shanlihong 3 Hao’ fruits at maturity mainly result from cellulose/hemicelluloses degradation rather than from lamella degradation. Overall, we propose that different types of hydrolytic enzymes in cells interact to degrade the cell wall, resulting in ultramicroscopic Structure changes in the cell wall and, consequently, fruit softening. These results provide fundamental insight regarding the mechanisms by which hawthorn fruits acquire different textures and also lay a solid foundation for further research. Frontiers Media S.A. 2016-10-14 /pmc/articles/PMC5063854/ /pubmed/27790234 http://dx.doi.org/10.3389/fpls.2016.01524 Text en Copyright © 2016 Xu, Zhao, Zhang, Zhang, Hou and Dong. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Xu, Jiayu
Zhao, Yuhui
Zhang, Xiao
Zhang, Lijie
Hou, Yali
Dong, Wenxuan
Transcriptome Analysis and Ultrastructure Observation Reveal that Hawthorn Fruit Softening Is due to Cellulose/Hemicellulose Degradation
title Transcriptome Analysis and Ultrastructure Observation Reveal that Hawthorn Fruit Softening Is due to Cellulose/Hemicellulose Degradation
title_full Transcriptome Analysis and Ultrastructure Observation Reveal that Hawthorn Fruit Softening Is due to Cellulose/Hemicellulose Degradation
title_fullStr Transcriptome Analysis and Ultrastructure Observation Reveal that Hawthorn Fruit Softening Is due to Cellulose/Hemicellulose Degradation
title_full_unstemmed Transcriptome Analysis and Ultrastructure Observation Reveal that Hawthorn Fruit Softening Is due to Cellulose/Hemicellulose Degradation
title_short Transcriptome Analysis and Ultrastructure Observation Reveal that Hawthorn Fruit Softening Is due to Cellulose/Hemicellulose Degradation
title_sort transcriptome analysis and ultrastructure observation reveal that hawthorn fruit softening is due to cellulose/hemicellulose degradation
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5063854/
https://www.ncbi.nlm.nih.gov/pubmed/27790234
http://dx.doi.org/10.3389/fpls.2016.01524
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