Ozone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethylene

Abstract Background Understanding the mechanisms involved in climacteric fruit ripening is key to improve fruit harvest quality and postharvest performance. Kiwifruit (Actinidia deliciosa cv. ‘Hayward’) ripening involves a series of metabolic changes regulated by ethylene. Although 1-methylcycloprop...

Full description

Bibliographic Details
Main Authors: Ioannis S. Minas, Georgia Tanou, Afroditi Krokida, Evangelos Karagiannis, Maya Belghazi, Miltiadis Vasilakakis, Kalliope K. Papadopoulou, Athanassios Molassiotis
Format: Article
Language:English
Published: BMC 2018-12-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-018-1584-y
id doaj-676c7cd79b22469991e20edf22e8b5a2
record_format Article
spelling doaj-676c7cd79b22469991e20edf22e8b5a22020-11-25T01:55:52ZengBMCBMC Plant Biology1471-22292018-12-0118111910.1186/s12870-018-1584-yOzone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethyleneIoannis S. Minas0Georgia Tanou1Afroditi Krokida2Evangelos Karagiannis3Maya Belghazi4Miltiadis Vasilakakis5Kalliope K. Papadopoulou6Athanassios Molassiotis7Laboratory of Pomology, Department of Agriculture, Aristotle University of ThessalonikiLaboratory of Pomology, Department of Agriculture, Aristotle University of ThessalonikiDepartment of Biochemistry and Biotechnology, University of ThessalyLaboratory of Pomology, Department of Agriculture, Aristotle University of ThessalonikiUMR 7286 - CRN2M, Centre d’ Analyses Protéomiques de Marseille (CAPM), CNRS, Aix-Marseille UniversitéLaboratory of Pomology, Department of Agriculture, Aristotle University of ThessalonikiDepartment of Biochemistry and Biotechnology, University of ThessalyLaboratory of Pomology, Department of Agriculture, Aristotle University of ThessalonikiAbstract Background Understanding the mechanisms involved in climacteric fruit ripening is key to improve fruit harvest quality and postharvest performance. Kiwifruit (Actinidia deliciosa cv. ‘Hayward’) ripening involves a series of metabolic changes regulated by ethylene. Although 1-methylcyclopropene (1-MCP, inhibitor of ethylene action) or ozone (O3) exposure suppresses ethylene-related kiwifruit ripening, how these molecules interact during ripening is unknown. Results Harvested ‘Hayward’ kiwifruits were treated with 1-MCP and exposed to ethylene-free cold storage (0 °C, RH 95%) with ambient atmosphere (control) or atmosphere enriched with O3 (0.3 μL L− 1) for up to 6 months. Their subsequent ripening performance at 20 °C (90% RH) was characterized. Treatment with either 1-MCP or O3 inhibited endogenous ethylene biosynthesis and delayed fruit ripening at 20 °C. 1-MCP and O3 in combination severely inhibited kiwifruit ripening, significantly extending fruit storage potential. To characterize ethylene sensitivity of kiwifruit following 1-MCP and O3 treatments, fruit were exposed to exogenous ethylene (100 μL L− 1, 24 h) upon transfer to 20 °C following 4 and 6 months of cold storage. Exogenous ethylene treatment restored ethylene biosynthesis in fruit previously exposed in an O3-enriched atmosphere. Comparative proteomics analysis showed separate kiwifruit ripening responses, unraveled common 1-MCP- and O3-dependent metabolic pathways and identified specific proteins associated with these different ripening behaviors. Protein components that were differentially expressed following exogenous ethylene exposure after 1-MCP or O3 treatment were identified and their protein-protein interaction networks were determined. The expression of several kiwifruit ripening related genes, such as 1-aminocyclopropane-1-carboxylic acid oxidase (ACO1), ethylene receptor (ETR1), lipoxygenase (LOX1), geranylgeranyl diphosphate synthase (GGP1), and expansin (EXP2), was strongly affected by O3, 1-MCP, their combination, and exogenously applied ethylene. Conclusions Our findings suggest that the combination of 1-MCP and O3 functions as a robust repressive modulator of kiwifruit ripening and provide new insight into the metabolic events underlying ethylene-induced and ethylene-independent ripening outcomes.http://link.springer.com/article/10.1186/s12870-018-1584-yActinidia deliciosaClimactericCold storageEthylene biosynthesisGene expressionKiwifruit ripening
collection DOAJ
language English
format Article
sources DOAJ
author Ioannis S. Minas
Georgia Tanou
Afroditi Krokida
Evangelos Karagiannis
Maya Belghazi
Miltiadis Vasilakakis
Kalliope K. Papadopoulou
Athanassios Molassiotis
spellingShingle Ioannis S. Minas
Georgia Tanou
Afroditi Krokida
Evangelos Karagiannis
Maya Belghazi
Miltiadis Vasilakakis
Kalliope K. Papadopoulou
Athanassios Molassiotis
Ozone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethylene
BMC Plant Biology
Actinidia deliciosa
Climacteric
Cold storage
Ethylene biosynthesis
Gene expression
Kiwifruit ripening
author_facet Ioannis S. Minas
Georgia Tanou
Afroditi Krokida
Evangelos Karagiannis
Maya Belghazi
Miltiadis Vasilakakis
Kalliope K. Papadopoulou
Athanassios Molassiotis
author_sort Ioannis S. Minas
title Ozone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethylene
title_short Ozone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethylene
title_full Ozone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethylene
title_fullStr Ozone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethylene
title_full_unstemmed Ozone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethylene
title_sort ozone-induced inhibition of kiwifruit ripening is amplified by 1-methylcyclopropene and reversed by exogenous ethylene
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2018-12-01
description Abstract Background Understanding the mechanisms involved in climacteric fruit ripening is key to improve fruit harvest quality and postharvest performance. Kiwifruit (Actinidia deliciosa cv. ‘Hayward’) ripening involves a series of metabolic changes regulated by ethylene. Although 1-methylcyclopropene (1-MCP, inhibitor of ethylene action) or ozone (O3) exposure suppresses ethylene-related kiwifruit ripening, how these molecules interact during ripening is unknown. Results Harvested ‘Hayward’ kiwifruits were treated with 1-MCP and exposed to ethylene-free cold storage (0 °C, RH 95%) with ambient atmosphere (control) or atmosphere enriched with O3 (0.3 μL L− 1) for up to 6 months. Their subsequent ripening performance at 20 °C (90% RH) was characterized. Treatment with either 1-MCP or O3 inhibited endogenous ethylene biosynthesis and delayed fruit ripening at 20 °C. 1-MCP and O3 in combination severely inhibited kiwifruit ripening, significantly extending fruit storage potential. To characterize ethylene sensitivity of kiwifruit following 1-MCP and O3 treatments, fruit were exposed to exogenous ethylene (100 μL L− 1, 24 h) upon transfer to 20 °C following 4 and 6 months of cold storage. Exogenous ethylene treatment restored ethylene biosynthesis in fruit previously exposed in an O3-enriched atmosphere. Comparative proteomics analysis showed separate kiwifruit ripening responses, unraveled common 1-MCP- and O3-dependent metabolic pathways and identified specific proteins associated with these different ripening behaviors. Protein components that were differentially expressed following exogenous ethylene exposure after 1-MCP or O3 treatment were identified and their protein-protein interaction networks were determined. The expression of several kiwifruit ripening related genes, such as 1-aminocyclopropane-1-carboxylic acid oxidase (ACO1), ethylene receptor (ETR1), lipoxygenase (LOX1), geranylgeranyl diphosphate synthase (GGP1), and expansin (EXP2), was strongly affected by O3, 1-MCP, their combination, and exogenously applied ethylene. Conclusions Our findings suggest that the combination of 1-MCP and O3 functions as a robust repressive modulator of kiwifruit ripening and provide new insight into the metabolic events underlying ethylene-induced and ethylene-independent ripening outcomes.
topic Actinidia deliciosa
Climacteric
Cold storage
Ethylene biosynthesis
Gene expression
Kiwifruit ripening
url http://link.springer.com/article/10.1186/s12870-018-1584-y
work_keys_str_mv AT ioannissminas ozoneinducedinhibitionofkiwifruitripeningisamplifiedby1methylcyclopropeneandreversedbyexogenousethylene
AT georgiatanou ozoneinducedinhibitionofkiwifruitripeningisamplifiedby1methylcyclopropeneandreversedbyexogenousethylene
AT afroditikrokida ozoneinducedinhibitionofkiwifruitripeningisamplifiedby1methylcyclopropeneandreversedbyexogenousethylene
AT evangeloskaragiannis ozoneinducedinhibitionofkiwifruitripeningisamplifiedby1methylcyclopropeneandreversedbyexogenousethylene
AT mayabelghazi ozoneinducedinhibitionofkiwifruitripeningisamplifiedby1methylcyclopropeneandreversedbyexogenousethylene
AT miltiadisvasilakakis ozoneinducedinhibitionofkiwifruitripeningisamplifiedby1methylcyclopropeneandreversedbyexogenousethylene
AT kalliopekpapadopoulou ozoneinducedinhibitionofkiwifruitripeningisamplifiedby1methylcyclopropeneandreversedbyexogenousethylene
AT athanassiosmolassiotis ozoneinducedinhibitionofkiwifruitripeningisamplifiedby1methylcyclopropeneandreversedbyexogenousethylene
_version_ 1724982891723620352