The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato
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DOI：
10.1038/s41477-021-00916-y
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发表时间：
2021-05-01
期刊：
影响因子：
18
通讯作者：
Jarvis, R. Paul
中科院分区：
文献类型：
--
作者：
Ling, Qihua;Sadali, Najiah Mohd;Jarvis, R. Paul
水果成熟是一个微调过程，涉及水果结构和新陈代谢的大规模变化。现在，CHLORAD蛋白水解途径被证明可以调节有色体发育，从而改变番茄果实的成熟过程。绿色肉质果实的成熟变得色彩缤纷、味道鲜美，是植物繁殖和传播的重要策略。在番茄（Solanum lycopersicum）和许多其他物种中，果实成熟与有色体的生物发生密切相关，有色体在成熟果实中含量丰富，专门用于类胡萝卜素色素的积累。有色体是从水果中预先存在的叶绿体发展而来的，但人们对这种转变背后的机制知之甚少。在这里，我们揭示了叶绿体相关蛋白降解（CHLORAD）蛋白水解途径在有色体分化中的作用。质体泛素 E3 连接酶 SP1 或其同源物 SPL2 的敲低会延迟番茄果实的成熟，而 SP1 的过度表达会加速成熟（从颜色变化来看）。我们证明，SP1 通过促进叶绿体到有色体的转变，对果实成熟产生更广泛的影响，包括果实软化、基因表达和代谢变化。此外，我们还发现番茄 SP1 和 SPL2 调节叶片衰老，揭示了 CHLORAD 在植物中的保守功能。我们得出的结论是，SP1 同源物通过重新配置质体蛋白输入机制来影响蛋白质组重组，从而控制果实成熟和叶片衰老过程中的质体转变。该工作强调了有色体在果实成熟中的关键作用，并为工程作物改良提供了理论基础。
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.