Examining the Role of Low Temperature in Satsuma Mandarin Fruit Peel Degreening via Comparative Physiological and Transcriptomic Analysis

Peel degreening is the most conspicuous aspect of fruit ripening in many citrus fruits because of its importance for marketability. In this study, peel degreening in response to propylene (an ethylene analog) and at varying storage temperatures was characterized in Satsuma mandarin (Citrus unshiu Ma...

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Main Authors: Oscar W. Mitalo, William O. Asiche, Seung W. Kang, Hiroshi Ezura, Takashi Akagi, Yasutaka Kubo, Koichiro Ushijima
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.918226/full
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author Oscar W. Mitalo
Oscar W. Mitalo
William O. Asiche
Seung W. Kang
Seung W. Kang
Hiroshi Ezura
Hiroshi Ezura
Takashi Akagi
Yasutaka Kubo
Koichiro Ushijima
author_facet Oscar W. Mitalo
Oscar W. Mitalo
William O. Asiche
Seung W. Kang
Seung W. Kang
Hiroshi Ezura
Hiroshi Ezura
Takashi Akagi
Yasutaka Kubo
Koichiro Ushijima
author_sort Oscar W. Mitalo
collection DOAJ
description Peel degreening is the most conspicuous aspect of fruit ripening in many citrus fruits because of its importance for marketability. In this study, peel degreening in response to propylene (an ethylene analog) and at varying storage temperatures was characterized in Satsuma mandarin (Citrus unshiu Marc.) fruit. Propylene treatment triggered rapid peel degreening (within 4–6 days), indicated by an increase in the citrus color index (CCI) and chlorophyll loss. Peel degreening was also observed in fruit at 10°C and 15°C after 28–42 days, with gradual CCI increase and chlorophyll reduction. However, fruit at 5°C, 20°C, and 25°C remained green, and no substantial changes in peel CCI and chlorophyll content were recorded during the 42-day storage duration. The transcriptomes of peels of fruit treated with propylene for 4 days and those stored at varying temperatures for 28 days were then analyzed by RNA-Seq. We identified three categories of differentially expressed genes that were regulated by (i) propylene (and by analogy, ethylene) alone, (ii) low temperature (5°C, 10°C, or 15°C vs. 25°C) alone, and (iii) either propylene or low temperature. Gene-encoding proteins associated with chlorophyll degradation (such as CuSGR1, CuNOL, CuACD2, CuCAB2, and CuLHCB2) and a transcription factor (CuERF114) were differentially expressed by propylene or low temperature. To further examine temperature-induced pathways, we also monitored gene expression during on-tree fruit maturation vs. postharvest. The onset of on-tree peel degreening coincided with autumnal drops in field temperatures, and it was accompanied by differential expression of low temperature-regulated genes. On the contrary, genes that were exclusively regulated by propylene (such as CuCOPT1 and CuPOX-A2) displayed insignificant expression changes during on-tree peel degreening. These findings indicate that low temperatures could be involved in the fruit ripening-related peel degreening independently of ethylene.
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spelling doaj.art-c3f8e81cc1f748508f58fa2d65553fb72022-12-22T01:26:14ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-07-011310.3389/fpls.2022.918226918226Examining the Role of Low Temperature in Satsuma Mandarin Fruit Peel Degreening via Comparative Physiological and Transcriptomic AnalysisOscar W. Mitalo0Oscar W. Mitalo1William O. Asiche2Seung W. Kang3Seung W. Kang4Hiroshi Ezura5Hiroshi Ezura6Takashi Akagi7Yasutaka Kubo8Koichiro Ushijima9Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanGraduate School of Environmental and Life Science, Okayama University, Okayama, JapanDepartment of Research and Development, Del Monte Kenya Ltd, Thika, KenyaGraduate 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, JapanGraduate School of Environmental and Life Science, Okayama University, Okayama, JapanGraduate School of Environmental and Life Science, Okayama University, Okayama, JapanGraduate School of Environmental and Life Science, Okayama University, Okayama, JapanPeel degreening is the most conspicuous aspect of fruit ripening in many citrus fruits because of its importance for marketability. In this study, peel degreening in response to propylene (an ethylene analog) and at varying storage temperatures was characterized in Satsuma mandarin (Citrus unshiu Marc.) fruit. Propylene treatment triggered rapid peel degreening (within 4–6 days), indicated by an increase in the citrus color index (CCI) and chlorophyll loss. Peel degreening was also observed in fruit at 10°C and 15°C after 28–42 days, with gradual CCI increase and chlorophyll reduction. However, fruit at 5°C, 20°C, and 25°C remained green, and no substantial changes in peel CCI and chlorophyll content were recorded during the 42-day storage duration. The transcriptomes of peels of fruit treated with propylene for 4 days and those stored at varying temperatures for 28 days were then analyzed by RNA-Seq. We identified three categories of differentially expressed genes that were regulated by (i) propylene (and by analogy, ethylene) alone, (ii) low temperature (5°C, 10°C, or 15°C vs. 25°C) alone, and (iii) either propylene or low temperature. Gene-encoding proteins associated with chlorophyll degradation (such as CuSGR1, CuNOL, CuACD2, CuCAB2, and CuLHCB2) and a transcription factor (CuERF114) were differentially expressed by propylene or low temperature. To further examine temperature-induced pathways, we also monitored gene expression during on-tree fruit maturation vs. postharvest. The onset of on-tree peel degreening coincided with autumnal drops in field temperatures, and it was accompanied by differential expression of low temperature-regulated genes. On the contrary, genes that were exclusively regulated by propylene (such as CuCOPT1 and CuPOX-A2) displayed insignificant expression changes during on-tree peel degreening. These findings indicate that low temperatures could be involved in the fruit ripening-related peel degreening independently of ethylene.https://www.frontiersin.org/articles/10.3389/fpls.2022.918226/fullchlorophyllcitrusdegreeningethyleneRNA-Seqon-tree
spellingShingle Oscar W. Mitalo
Oscar W. Mitalo
William O. Asiche
Seung W. Kang
Seung W. Kang
Hiroshi Ezura
Hiroshi Ezura
Takashi Akagi
Yasutaka Kubo
Koichiro Ushijima
Examining the Role of Low Temperature in Satsuma Mandarin Fruit Peel Degreening via Comparative Physiological and Transcriptomic Analysis
Frontiers in Plant Science
chlorophyll
citrus
degreening
ethylene
RNA-Seq
on-tree
title Examining the Role of Low Temperature in Satsuma Mandarin Fruit Peel Degreening via Comparative Physiological and Transcriptomic Analysis
title_full Examining the Role of Low Temperature in Satsuma Mandarin Fruit Peel Degreening via Comparative Physiological and Transcriptomic Analysis
title_fullStr Examining the Role of Low Temperature in Satsuma Mandarin Fruit Peel Degreening via Comparative Physiological and Transcriptomic Analysis
title_full_unstemmed Examining the Role of Low Temperature in Satsuma Mandarin Fruit Peel Degreening via Comparative Physiological and Transcriptomic Analysis
title_short Examining the Role of Low Temperature in Satsuma Mandarin Fruit Peel Degreening via Comparative Physiological and Transcriptomic Analysis
title_sort examining the role of low temperature in satsuma mandarin fruit peel degreening via comparative physiological and transcriptomic analysis
topic chlorophyll
citrus
degreening
ethylene
RNA-Seq
on-tree
url https://www.frontiersin.org/articles/10.3389/fpls.2022.918226/full
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