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

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.

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Abstract

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.

Item Type: Article
Funders: UK Research & Innovation (UKRI) Biotechnology and Biological Sciences Research Council (BBSRC) [Grant No: BB/K018442/1&BB/H008039/1&BB/R005591/1&BB/R016984/1&BB/R009333/1]
Uncontrolled Keywords: Fruit ripening; Engineering crop
Subjects: Q Science > Q Science (General)
Divisions: Deputy Vice Chancellor (Research & Innovation) Office > Centre for Research in Biotechnology for Agriculture
Depositing User: Ms Zaharah Ramly
Date Deposited: 13 Jun 2022 08:59
Last Modified: 13 Jun 2022 08:59
URI: http://eprints.um.edu.my/id/eprint/34106

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