The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato

Fruit ripening is a fine-tuned process involving wholesale changes to both the structure and metabolism of the fruit. Now, the CHLORAD proteolytic pathway is shown to regulate chromoplast development, thus altering the ripening process of tomato fruits. The maturation of green fleshy fruit to become...

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Main Authors: Ling, Qihua, Sadali, Najiah Mohd, Soufi, Ziad, Zhou, Yuan, Huang, Binquan, Zeng, Yunliu, Rodriguez-Concepcion, Manuel, Jarvis, R. Paul
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Published: Nature Research 2021
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Online Access:http://eprints.um.edu.my/34106/
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spelling my.um.eprints.341062022-06-13T08:59:34Z http://eprints.um.edu.my/34106/ The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato Ling, Qihua Sadali, Najiah Mohd Soufi, Ziad Zhou, Yuan Huang, Binquan Zeng, Yunliu Rodriguez-Concepcion, Manuel Jarvis, R. Paul Q Science (General) Fruit ripening is a fine-tuned process involving wholesale changes to both the structure and metabolism of the fruit. Now, the CHLORAD proteolytic pathway is shown to regulate chromoplast development, thus altering the ripening process of tomato fruits. The maturation of green fleshy fruit to become colourful and flavoursome is an important strategy for plant reproduction and dispersal. In tomato (Solanum lycopersicum) and many other species, fruit ripening is intimately linked to the biogenesis of chromoplasts, the plastids that are abundant in ripe fruit and specialized for the accumulation of carotenoid pigments. Chromoplasts develop from pre-existing chloroplasts in the fruit, but the mechanisms underlying this transition are poorly understood. Here, we reveal a role for the chloroplast-associated protein degradation (CHLORAD) proteolytic pathway in chromoplast differentiation. Knockdown of the plastid ubiquitin E3 ligase SP1, or its homologue SPL2, delays tomato fruit ripening, whereas overexpression of SP1 accelerates ripening, as judged by colour changes. We demonstrate that SP1 triggers broader effects on fruit ripening, including fruit softening, and gene expression and metabolism changes, by promoting the chloroplast-to-chromoplast transition. Moreover, we show that tomato SP1 and SPL2 regulate leaf senescence, revealing conserved functions of CHLORAD in plants. We conclude that SP1 homologues control plastid transitions during fruit ripening and leaf senescence by enabling reconfiguration of the plastid protein import machinery to effect proteome reorganization. The work highlights the critical role of chromoplasts in fruit ripening, and provides a theoretical basis for engineering crop improvements. Nature Research 2021-05 Article PeerReviewed Ling, Qihua and Sadali, Najiah Mohd and Soufi, Ziad and Zhou, Yuan and Huang, Binquan and Zeng, Yunliu and Rodriguez-Concepcion, Manuel and Jarvis, R. Paul (2021) The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato. Nature Plants, 7 (5). 655+. ISSN 2055-026X, DOI https://doi.org/10.1038/s41477-021-00916-y <https://doi.org/10.1038/s41477-021-00916-y>. 10.1038/s41477-021-00916-y
institution Universiti Malaya
building UM Library
collection Institutional Repository
continent Asia
country Malaysia
content_provider Universiti Malaya
content_source UM Research Repository
url_provider http://eprints.um.edu.my/
topic Q Science (General)
spellingShingle Q Science (General)
Ling, Qihua
Sadali, Najiah Mohd
Soufi, Ziad
Zhou, Yuan
Huang, Binquan
Zeng, Yunliu
Rodriguez-Concepcion, Manuel
Jarvis, R. Paul
The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
description Fruit ripening is a fine-tuned process involving wholesale changes to both the structure and metabolism of the fruit. Now, the CHLORAD proteolytic pathway is shown to regulate chromoplast development, thus altering the ripening process of tomato fruits. The maturation of green fleshy fruit to become colourful and flavoursome is an important strategy for plant reproduction and dispersal. In tomato (Solanum lycopersicum) and many other species, fruit ripening is intimately linked to the biogenesis of chromoplasts, the plastids that are abundant in ripe fruit and specialized for the accumulation of carotenoid pigments. Chromoplasts develop from pre-existing chloroplasts in the fruit, but the mechanisms underlying this transition are poorly understood. Here, we reveal a role for the chloroplast-associated protein degradation (CHLORAD) proteolytic pathway in chromoplast differentiation. Knockdown of the plastid ubiquitin E3 ligase SP1, or its homologue SPL2, delays tomato fruit ripening, whereas overexpression of SP1 accelerates ripening, as judged by colour changes. We demonstrate that SP1 triggers broader effects on fruit ripening, including fruit softening, and gene expression and metabolism changes, by promoting the chloroplast-to-chromoplast transition. Moreover, we show that tomato SP1 and SPL2 regulate leaf senescence, revealing conserved functions of CHLORAD in plants. We conclude that SP1 homologues control plastid transitions during fruit ripening and leaf senescence by enabling reconfiguration of the plastid protein import machinery to effect proteome reorganization. The work highlights the critical role of chromoplasts in fruit ripening, and provides a theoretical basis for engineering crop improvements.
format Article
author Ling, Qihua
Sadali, Najiah Mohd
Soufi, Ziad
Zhou, Yuan
Huang, Binquan
Zeng, Yunliu
Rodriguez-Concepcion, Manuel
Jarvis, R. Paul
author_facet Ling, Qihua
Sadali, Najiah Mohd
Soufi, Ziad
Zhou, Yuan
Huang, Binquan
Zeng, Yunliu
Rodriguez-Concepcion, Manuel
Jarvis, R. Paul
author_sort Ling, Qihua
title The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
title_short The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
title_full The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
title_fullStr The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
title_full_unstemmed The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
title_sort chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
publisher Nature Research
publishDate 2021
url http://eprints.um.edu.my/34106/
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score 13.211869