Atypical Climacteric and Functional Ethylene Metabolism and Signaling During Fruit Ripening in Blueberry (Vaccinium sp.)

Climacteric fruits display an increase in respiration and ethylene production during the onset of ripening, while such changes are minimal in non-climacteric fruits. Ethylene is a primary regulator of ripening in climacteric fruits. The ripening behavior and role of ethylene in blueberry (Vaccinium...

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Main Authors: Yi-Wen Wang, Tej P. Acharya, Anish Malladi, Hsuan-Ju Tsai, D. Scott NeSmith, John W. Doyle, Savithri U. Nambeesan
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.932642/full
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author Yi-Wen Wang
Yi-Wen Wang
Tej P. Acharya
Anish Malladi
Hsuan-Ju Tsai
Hsuan-Ju Tsai
D. Scott NeSmith
John W. Doyle
Savithri U. Nambeesan
author_facet Yi-Wen Wang
Yi-Wen Wang
Tej P. Acharya
Anish Malladi
Hsuan-Ju Tsai
Hsuan-Ju Tsai
D. Scott NeSmith
John W. Doyle
Savithri U. Nambeesan
author_sort Yi-Wen Wang
collection DOAJ
description Climacteric fruits display an increase in respiration and ethylene production during the onset of ripening, while such changes are minimal in non-climacteric fruits. Ethylene is a primary regulator of ripening in climacteric fruits. The ripening behavior and role of ethylene in blueberry (Vaccinium sp.) ripening is controversial. This work aimed to clarify the fruit ripening behavior and the associated role of ethylene in blueberry. Southern highbush (Vaccinium corymbosum hybrids) and rabbiteye (Vaccinium ashei) blueberry displayed an increase in the rate of respiration and ethylene evolution, both reaching a maxima around the Pink and Ripe stages of fruit development, consistent with climacteric fruit ripening behavior. Increase in ethylene evolution was associated with increases in transcript abundance of its biosynthesis genes, AMINOCYCLOPROPANE CARBOXYLATE (ACC) SYNTHASE1 (ACS1) and ACC OXIDASE2 (ACO2), implicating them in developmental ethylene production during ripening. Blueberry fruit did not display autocatalytic system 2 ethylene during ripening as ACS transcript abundance and ACC concentration were not enhanced upon treatment with an ethylene-releasing compound (ethephon). However, ACO transcript abundance was enhanced in response to ethephon, suggesting that ACO was not rate-limiting. Transcript abundance of multiple genes associated with ethylene signal transduction was upregulated concomitant with developmental increase in ethylene evolution, and in response to exogenous ethylene. As these changes require ethylene signal transduction, fruit ripening in blueberry appears to involve functional ethylene signaling. Together, these data indicate that blueberry fruit display atypical climacteric ripening, characterized by a respiratory climacteric, developmentally regulated but non-autocatalytic increase in ethylene evolution, and functional ethylene signaling.
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spelling doaj.art-3c05c091310d4965a7ae7ec32c87d0322022-12-22T02:38:56ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-06-011310.3389/fpls.2022.932642932642Atypical Climacteric and Functional Ethylene Metabolism and Signaling During Fruit Ripening in Blueberry (Vaccinium sp.)Yi-Wen Wang0Yi-Wen Wang1Tej P. Acharya2Anish Malladi3Hsuan-Ju Tsai4Hsuan-Ju Tsai5D. Scott NeSmith6John W. Doyle7Savithri U. Nambeesan8Department of Horticulture, University of Georgia, Athens, GA, United StatesCenter for Applied Genetic Technologies, University of Georgia, Athens, GA, United StatesDepartment of Horticulture, University of Georgia, Athens, GA, United StatesDepartment of Horticulture, University of Georgia, Athens, GA, United StatesDepartment of Horticulture, University of Georgia, Athens, GA, United StatesTaiwan Agricultural Research Institute Council of Agriculture, Taichung, TaiwanDepartment of Horticulture, University of Georgia, Griffin, GA, United StatesDepartment of Horticulture, University of Georgia, Athens, GA, United StatesDepartment of Horticulture, University of Georgia, Athens, GA, United StatesClimacteric fruits display an increase in respiration and ethylene production during the onset of ripening, while such changes are minimal in non-climacteric fruits. Ethylene is a primary regulator of ripening in climacteric fruits. The ripening behavior and role of ethylene in blueberry (Vaccinium sp.) ripening is controversial. This work aimed to clarify the fruit ripening behavior and the associated role of ethylene in blueberry. Southern highbush (Vaccinium corymbosum hybrids) and rabbiteye (Vaccinium ashei) blueberry displayed an increase in the rate of respiration and ethylene evolution, both reaching a maxima around the Pink and Ripe stages of fruit development, consistent with climacteric fruit ripening behavior. Increase in ethylene evolution was associated with increases in transcript abundance of its biosynthesis genes, AMINOCYCLOPROPANE CARBOXYLATE (ACC) SYNTHASE1 (ACS1) and ACC OXIDASE2 (ACO2), implicating them in developmental ethylene production during ripening. Blueberry fruit did not display autocatalytic system 2 ethylene during ripening as ACS transcript abundance and ACC concentration were not enhanced upon treatment with an ethylene-releasing compound (ethephon). However, ACO transcript abundance was enhanced in response to ethephon, suggesting that ACO was not rate-limiting. Transcript abundance of multiple genes associated with ethylene signal transduction was upregulated concomitant with developmental increase in ethylene evolution, and in response to exogenous ethylene. As these changes require ethylene signal transduction, fruit ripening in blueberry appears to involve functional ethylene signaling. Together, these data indicate that blueberry fruit display atypical climacteric ripening, characterized by a respiratory climacteric, developmentally regulated but non-autocatalytic increase in ethylene evolution, and functional ethylene signaling.https://www.frontiersin.org/articles/10.3389/fpls.2022.932642/fullrespirationethyleneripeningblueberryfruit development
spellingShingle Yi-Wen Wang
Yi-Wen Wang
Tej P. Acharya
Anish Malladi
Hsuan-Ju Tsai
Hsuan-Ju Tsai
D. Scott NeSmith
John W. Doyle
Savithri U. Nambeesan
Atypical Climacteric and Functional Ethylene Metabolism and Signaling During Fruit Ripening in Blueberry (Vaccinium sp.)
Frontiers in Plant Science
respiration
ethylene
ripening
blueberry
fruit development
title Atypical Climacteric and Functional Ethylene Metabolism and Signaling During Fruit Ripening in Blueberry (Vaccinium sp.)
title_full Atypical Climacteric and Functional Ethylene Metabolism and Signaling During Fruit Ripening in Blueberry (Vaccinium sp.)
title_fullStr Atypical Climacteric and Functional Ethylene Metabolism and Signaling During Fruit Ripening in Blueberry (Vaccinium sp.)
title_full_unstemmed Atypical Climacteric and Functional Ethylene Metabolism and Signaling During Fruit Ripening in Blueberry (Vaccinium sp.)
title_short Atypical Climacteric and Functional Ethylene Metabolism and Signaling During Fruit Ripening in Blueberry (Vaccinium sp.)
title_sort atypical climacteric and functional ethylene metabolism and signaling during fruit ripening in blueberry vaccinium sp
topic respiration
ethylene
ripening
blueberry
fruit development
url https://www.frontiersin.org/articles/10.3389/fpls.2022.932642/full
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