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The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato.
Nat Plants. 2021 05; 7(5):655-666.NP

Abstract

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.

Authors+Show Affiliations

Department of Plant Sciences, University of Oxford, Oxford, UK. National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China. CAS-JIC Center of Excellence for Plant and Microbial Sciences (CEPAMS), Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China.Department of Plant Sciences, University of Oxford, Oxford, UK. Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, Kuala Lumpur, Malaysia.Department of Plant Sciences, University of Oxford, Oxford, UK.Department of Plant Sciences, University of Oxford, Oxford, UK. National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China.Department of Plant Sciences, University of Oxford, Oxford, UK. School of Agriculture, Yunnan University, Kunming, China.Department of Plant Sciences, University of Oxford, Oxford, UK. Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan, China.Instituto de Biología Molecular y Celular de Plantas (IBMCP), CSIC-Universitat Politècnica de València, Valencia, Spain.Department of Plant Sciences, University of Oxford, Oxford, UK. paul.jarvis@plants.ox.ac.uk.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

34007040

Citation

Ling, Qihua, et al. "The Chloroplast-associated Protein Degradation Pathway Controls Chromoplast Development and Fruit Ripening in Tomato." Nature Plants, vol. 7, no. 5, 2021, pp. 655-666.
Ling Q, Sadali NM, Soufi Z, et al. The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato. Nat Plants. 2021;7(5):655-666.
Ling, Q., Sadali, N. M., Soufi, Z., Zhou, Y., Huang, B., Zeng, Y., Rodriguez-Concepcion, M., & Jarvis, R. P. (2021). The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato. Nature Plants, 7(5), 655-666. https://doi.org/10.1038/s41477-021-00916-y
Ling Q, et al. The Chloroplast-associated Protein Degradation Pathway Controls Chromoplast Development and Fruit Ripening in Tomato. Nat Plants. 2021;7(5):655-666. PubMed PMID: 34007040.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato. AU - Ling,Qihua, AU - Sadali,Najiah Mohd, AU - Soufi,Ziad, AU - Zhou,Yuan, AU - Huang,Binquan, AU - Zeng,Yunliu, AU - Rodriguez-Concepcion,Manuel, AU - Jarvis,R Paul, Y1 - 2021/05/18/ PY - 2020/08/18/received PY - 2021/04/06/accepted PY - 2021/5/19/entrez PY - 2021/5/20/pubmed PY - 2021/8/5/medline SP - 655 EP - 666 JF - Nature plants JO - Nat Plants VL - 7 IS - 5 N2 - 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. SN - 2055-0278 UR - https://www.unboundmedicine.com/medline/citation/34007040/The_chloroplast_associated_protein_degradation_pathway_controls_chromoplast_development_and_fruit_ripening_in_tomato_ L2 - https://doi.org/10.1038/s41477-021-00916-y DB - PRIME DP - Unbound Medicine ER -