A non-photosynthetic green alga illuminates the reductive evolution of plastid electron transport systems
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RESEARCH ARTICLE
Open Access
A non-photosynthetic green alga illuminates the reductive evolution of plastid electron transport systems Motoki Kayama1, Jun-Feng Chen1, Takashi Nakada2, Yoshiki Nishimura3, Toshiharu Shikanai3, Tomonori Azuma1, Hideaki Miyashita1, Shinichi Takaichi4, Yuichiro Kashiyama5 and Ryoma Kamikawa1,6*
Abstract Background: Plastid electron transport systems are essential not only for photosynthesis but also for dissipating excess reducing power and sinking excess electrons generated by various redox reactions. Although numerous organisms with plastids have lost their photoautotrophic lifestyles, there is a spectrum of known functions of remnant plastids in non-photosynthetic algal/plant lineages; some of non-photosynthetic plastids still retain diverse metabolic pathways involving redox reactions while others, such as apicoplasts of apicomplexan parasites, possess highly reduced sets of functions. However, little is known about underlying mechanisms for redox homeostasis in functionally versatile non-photosynthetic plastids and thus about the reductive evolution of plastid electron transport systems. Results: Here we demonstrated that the central component for plastid electron transport systems, plastoquinone/ plastoquinol pool, is still retained in a novel strain of an obligate heterotrophic green alga lacking the photosynthesis-related thylakoid membrane complexes. Microscopic and genome analyses revealed that the Volvocales green alga, chlamydomonad sp. strain NrCl902, has non-photosynthetic plastids and a plastid DNA that carries no genes for the photosynthetic electron transport system. Transcriptome-based in silico prediction of the metabolic map followed by liquid chromatography analyses demonstrated carotenoid and plastoquinol synthesis, but no trace of chlorophyll pigments in the non-photosynthetic green alga. Transient RNA interference knockdown leads to suppression of plastoquinone/plastoquinol synthesis. The alga appears to possess genes for an electron sink system mediated by plastid terminal oxidase, plastoquinone/plastoquinol, and type II NADH dehydrogenase. Other non-photosynthetic algae/land plants also possess key genes for this system, suggesting a broad distribution of an electron sink system in non-photosynthetic plastids. (Continued on next page)
* Correspondence: [email protected] 1 Graduate School of Human and Environmental Studies, Kyoto University, Yoshida nihonmatsu cho, Sakyo ku, Kyoto, Kyoto 606-8501, Japan 6 Graduate School of Agriculture, Kyoto University, Kitashirakawa oiwake cho, Sakyo ku, Kyoto, Kyoto 606-8502, Japan Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if
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