Transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripening

Cold storage is widely used to extend the postharvest life of most horticultural crops, including tomatoes, but this practice triggers cold stress and leads to the development of undesirable chilling injury (CI) symptoms. The underlying mechanisms of cold stress response and CI development in fruits...

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Main Authors: Oscar W. Mitalo, Seung Wong Kang, Long T. Tran, Yasutaka Kubo, Tohru Ariizumi, Hiroshi Ezura
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1227349/full
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author Oscar W. Mitalo
Seung Wong Kang
Seung Wong Kang
Long T. Tran
Yasutaka Kubo
Tohru Ariizumi
Tohru Ariizumi
Hiroshi Ezura
Hiroshi Ezura
author_facet Oscar W. Mitalo
Seung Wong Kang
Seung Wong Kang
Long T. Tran
Yasutaka Kubo
Tohru Ariizumi
Tohru Ariizumi
Hiroshi Ezura
Hiroshi Ezura
author_sort Oscar W. Mitalo
collection DOAJ
description Cold storage is widely used to extend the postharvest life of most horticultural crops, including tomatoes, but this practice triggers cold stress and leads to the development of undesirable chilling injury (CI) symptoms. The underlying mechanisms of cold stress response and CI development in fruits remain unclear as they are often intermingled with fruit ripening changes. To gain insight into cold responses in fruits, we examined the effect of the potent ethylene signaling inhibitor 1-methylcyclopropene (1-MCP) on fruit ripening, CI occurrence and gene expression in mature green tomatoes during storage at 20°C and 5°C. 1-MCP treatments effectively inhibited ethylene production and peel color changes during storage at 20°C. Storage at 5°C also inhibited both ethylene production and peel color change; during rewarming at 20°C, 1-MCP treatments inhibited peel color change but failed to inhibit ethylene production. Furthermore, fruits stored at 5°C for 14 d developed CI symptoms (surface pitting and decay) during the rewarming period at 20°C regardless of 1-MCP treatment. Subsequent RNA-Seq analysis revealed that cold stress triggers a large-scale transcriptomic adjustment, as noticeably more genes were differentially expressed at 5°C (8,406) than at 20°C (4,814). More importantly, we have found some important divergences among genes involved in fruit ripening (up- or down-regulated at 20°C; inhibited by 1-MCP treatment) and those involved in cold stress (up- or down-regulated at 5°C; unaffected by 1-MCP treatment). Transcriptomic adjustments unique to cold stress response were associated with ribosome biogenesis, NcRNA metabolism, DNA methylation, chromatin formation/remodeling, and alternative splicing events. These data should foster further research into cold stress response mechanisms in fruits with the ultimate aim of improving tolerance to low temperature and reduction of CI symptoms during cold storage.
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spelling doaj.art-4c34bcab16024adc8e7581e2a90548d62023-07-28T11:59:28ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-07-011410.3389/fpls.2023.12273491227349Transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripeningOscar W. Mitalo0Seung Wong Kang1Seung Wong Kang2Long T. Tran3Yasutaka Kubo4Tohru Ariizumi5Tohru Ariizumi6Hiroshi Ezura7Hiroshi Ezura8Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanGraduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanTsukuba-Plant Innovation Research Center, University of Tsukuba, Tsukuba, JapanGraduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanGraduate School of Environmental and Life Science, Okayama University, Okayama, JapanGraduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanTsukuba-Plant Innovation Research Center, University of Tsukuba, Tsukuba, JapanGraduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanTsukuba-Plant Innovation Research Center, University of Tsukuba, Tsukuba, JapanCold storage is widely used to extend the postharvest life of most horticultural crops, including tomatoes, but this practice triggers cold stress and leads to the development of undesirable chilling injury (CI) symptoms. The underlying mechanisms of cold stress response and CI development in fruits remain unclear as they are often intermingled with fruit ripening changes. To gain insight into cold responses in fruits, we examined the effect of the potent ethylene signaling inhibitor 1-methylcyclopropene (1-MCP) on fruit ripening, CI occurrence and gene expression in mature green tomatoes during storage at 20°C and 5°C. 1-MCP treatments effectively inhibited ethylene production and peel color changes during storage at 20°C. Storage at 5°C also inhibited both ethylene production and peel color change; during rewarming at 20°C, 1-MCP treatments inhibited peel color change but failed to inhibit ethylene production. Furthermore, fruits stored at 5°C for 14 d developed CI symptoms (surface pitting and decay) during the rewarming period at 20°C regardless of 1-MCP treatment. Subsequent RNA-Seq analysis revealed that cold stress triggers a large-scale transcriptomic adjustment, as noticeably more genes were differentially expressed at 5°C (8,406) than at 20°C (4,814). More importantly, we have found some important divergences among genes involved in fruit ripening (up- or down-regulated at 20°C; inhibited by 1-MCP treatment) and those involved in cold stress (up- or down-regulated at 5°C; unaffected by 1-MCP treatment). Transcriptomic adjustments unique to cold stress response were associated with ribosome biogenesis, NcRNA metabolism, DNA methylation, chromatin formation/remodeling, and alternative splicing events. These data should foster further research into cold stress response mechanisms in fruits with the ultimate aim of improving tolerance to low temperature and reduction of CI symptoms during cold storage.https://www.frontiersin.org/articles/10.3389/fpls.2023.1227349/fullcold stresschilling injury“Micro-Tom”“Moneymaker”RNA-Seqripening
spellingShingle Oscar W. Mitalo
Seung Wong Kang
Seung Wong Kang
Long T. Tran
Yasutaka Kubo
Tohru Ariizumi
Tohru Ariizumi
Hiroshi Ezura
Hiroshi Ezura
Transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripening
Frontiers in Plant Science
cold stress
chilling injury
“Micro-Tom”
“Moneymaker”
RNA-Seq
ripening
title Transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripening
title_full Transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripening
title_fullStr Transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripening
title_full_unstemmed Transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripening
title_short Transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripening
title_sort transcriptomic analysis in tomato fruit reveals divergences in genes involved in cold stress response and fruit ripening
topic cold stress
chilling injury
“Micro-Tom”
“Moneymaker”
RNA-Seq
ripening
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1227349/full
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