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Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit

Fruit ripening in response to propylene (an ethylene analog), 1-methylcyclopropene (1-MCP, an ethylene action inhibitor), and low temperature (5°C) treatments was characterized in “Kosui” kiwifruit (Actinidia rufa × A. chinensis). Propylene treatment induced ethylene production, with increased expre...

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Autores principales: Mitalo, Oscar W., Tokiwa, Sumire, Kondo, Yuki, Otsuki, Takumi, Galis, Ivan, Suezawa, Katsuhiko, Kataoka, Ikuo, Doan, Anh T., Nakano, Ryohei, Ushijima, Koichiro, Kubo, Yasutaka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6625211/
https://www.ncbi.nlm.nih.gov/pubmed/31333713
http://dx.doi.org/10.3389/fpls.2019.00888
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author Mitalo, Oscar W.
Tokiwa, Sumire
Kondo, Yuki
Otsuki, Takumi
Galis, Ivan
Suezawa, Katsuhiko
Kataoka, Ikuo
Doan, Anh T.
Nakano, Ryohei
Ushijima, Koichiro
Kubo, Yasutaka
author_facet Mitalo, Oscar W.
Tokiwa, Sumire
Kondo, Yuki
Otsuki, Takumi
Galis, Ivan
Suezawa, Katsuhiko
Kataoka, Ikuo
Doan, Anh T.
Nakano, Ryohei
Ushijima, Koichiro
Kubo, Yasutaka
author_sort Mitalo, Oscar W.
collection PubMed
description Fruit ripening in response to propylene (an ethylene analog), 1-methylcyclopropene (1-MCP, an ethylene action inhibitor), and low temperature (5°C) treatments was characterized in “Kosui” kiwifruit (Actinidia rufa × A. chinensis). Propylene treatment induced ethylene production, with increased expression levels of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase 1 (AcACS1) and ACC oxidase 2 (AcACO2), and rapid fruit softening together with increased expression levels of polygalacturonase (AcPG) and expansin 1 (AcEXP1) within 5 days (d). Fruit soluble solids concentration (SSC) and contents of sucrose, glucose, and fructose together with the expression levels of β-amylase 1 (Acβ-AMY1), Acβ-AMY2, and invertase (AcINV3-1) increased rapidly after 5 d exposure to propylene. Furthermore, propylene exposure for 5 d was sufficient to induce the production of key aroma volatile compounds, ethyl- and methyl butanoate, accompanied with increased expression levels of alcohol acyl transferase (AcAAT). Application of 1-MCP at the start of the experiment, followed by continuous exposure to propylene, significantly delayed fruit softening, changes in SSC and sugars, and strongly suppressed the production of ethylene, aroma volatiles, and expression of associated genes. During storage, fruit softening, SSC and sugar increase, and increased expression of genes associated with cell wall modification and carbohydrate metabolism were registered without detectable ethylene production; however, these changes occurred faster at 5°C compared to 22°C. Interestingly, ethyl and methyl butanoate as well as AcAAT expression were undetectable in kiwifruit during storage, while they were rescued by post-storage propylene exposure, indicating that the production of aroma volatile compounds is strongly ethylene-dependent. Transcript levels of a NAC-related transcription factor (TF), AcNAC3, increased in response to both propylene and low temperature treatments, while AcNAC5 was exclusively up-regulated by propylene. By contrast, transcript levels of a MADS-box TF, AcMADS2, exclusively increased in response to low temperature. The above findings indicate that kiwifruit ripening is inducible by either ethylene or low temperature signals. However, fruit ripened by low temperature were deficient in ethylene-dependent aroma volatiles, suggesting that ethylene signaling is non-functional during low temperature-modulated ripening in kiwifruit. These data provide further evidence that ethylene-dependent and low temperature-modulated ripening in kiwifruit involve different regulatory mechanisms.
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spelling pubmed-66252112019-07-22 Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit Mitalo, Oscar W. Tokiwa, Sumire Kondo, Yuki Otsuki, Takumi Galis, Ivan Suezawa, Katsuhiko Kataoka, Ikuo Doan, Anh T. Nakano, Ryohei Ushijima, Koichiro Kubo, Yasutaka Front Plant Sci Plant Science Fruit ripening in response to propylene (an ethylene analog), 1-methylcyclopropene (1-MCP, an ethylene action inhibitor), and low temperature (5°C) treatments was characterized in “Kosui” kiwifruit (Actinidia rufa × A. chinensis). Propylene treatment induced ethylene production, with increased expression levels of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase 1 (AcACS1) and ACC oxidase 2 (AcACO2), and rapid fruit softening together with increased expression levels of polygalacturonase (AcPG) and expansin 1 (AcEXP1) within 5 days (d). Fruit soluble solids concentration (SSC) and contents of sucrose, glucose, and fructose together with the expression levels of β-amylase 1 (Acβ-AMY1), Acβ-AMY2, and invertase (AcINV3-1) increased rapidly after 5 d exposure to propylene. Furthermore, propylene exposure for 5 d was sufficient to induce the production of key aroma volatile compounds, ethyl- and methyl butanoate, accompanied with increased expression levels of alcohol acyl transferase (AcAAT). Application of 1-MCP at the start of the experiment, followed by continuous exposure to propylene, significantly delayed fruit softening, changes in SSC and sugars, and strongly suppressed the production of ethylene, aroma volatiles, and expression of associated genes. During storage, fruit softening, SSC and sugar increase, and increased expression of genes associated with cell wall modification and carbohydrate metabolism were registered without detectable ethylene production; however, these changes occurred faster at 5°C compared to 22°C. Interestingly, ethyl and methyl butanoate as well as AcAAT expression were undetectable in kiwifruit during storage, while they were rescued by post-storage propylene exposure, indicating that the production of aroma volatile compounds is strongly ethylene-dependent. Transcript levels of a NAC-related transcription factor (TF), AcNAC3, increased in response to both propylene and low temperature treatments, while AcNAC5 was exclusively up-regulated by propylene. By contrast, transcript levels of a MADS-box TF, AcMADS2, exclusively increased in response to low temperature. The above findings indicate that kiwifruit ripening is inducible by either ethylene or low temperature signals. However, fruit ripened by low temperature were deficient in ethylene-dependent aroma volatiles, suggesting that ethylene signaling is non-functional during low temperature-modulated ripening in kiwifruit. These data provide further evidence that ethylene-dependent and low temperature-modulated ripening in kiwifruit involve different regulatory mechanisms. Frontiers Media S.A. 2019-07-05 /pmc/articles/PMC6625211/ /pubmed/31333713 http://dx.doi.org/10.3389/fpls.2019.00888 Text en Copyright © 2019 Mitalo, Tokiwa, Kondo, Otsuki, Galis, Suezawa, Kataoka, Doan, Nakano, Ushijima and Kubo. 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) and the copyright owner(s) 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
Mitalo, Oscar W.
Tokiwa, Sumire
Kondo, Yuki
Otsuki, Takumi
Galis, Ivan
Suezawa, Katsuhiko
Kataoka, Ikuo
Doan, Anh T.
Nakano, Ryohei
Ushijima, Koichiro
Kubo, Yasutaka
Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit
title Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit
title_full Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit
title_fullStr Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit
title_full_unstemmed Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit
title_short Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit
title_sort low temperature storage stimulates fruit softening and sugar accumulation without ethylene and aroma volatile production in kiwifruit
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6625211/
https://www.ncbi.nlm.nih.gov/pubmed/31333713
http://dx.doi.org/10.3389/fpls.2019.00888
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