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. 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. The plastoquinone/plastoquinol pool and thus the involved electron transport systems reported herein might be retained for redox homeostasis and might represent an intermediate step towards a more reduced set of the electron transport system in many non-photosynthetic plastids. Our findings illuminate a broadly distributed but previously hidden step of reductive evolution of plastid electron transport systems after the loss of photosynthesis.

中文翻译：

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非光合作用的绿藻阐明了质体电子传输系统的还原演化。

质子电子传输系统不仅对于光合作用至关重要，而且对于耗散过量的还原能力和吸收由各种氧化还原反应产生的过量电子也是必不可少的。尽管许多具有质体的生物丧失了光合自养的生活方式，但在非光合藻类/植物谱系中，残留质体的功能范围广。一些非光合作用的质体仍保留着涉及氧化还原反应的多种代谢途径，而其他一些，例如apicomplexan寄生虫的apicoplasts则具有高度减少的功能。然而，对于功能上通用的非光合质体中氧化还原稳态的基本机制，以及质体电子传输系统的还原进化，知之甚少。在这里，我们证明了质体电子传输系统的中心成分，质体醌/质体喹诺酮池，仍保留在一种新型的专性异养绿藻中，其缺乏与光合作用相关的类囊体膜复合物。显微镜和基因组分析表明，Volvocales绿藻，衣藻。菌株NrCl902具有非光合作用的质体和质体DNA，其不携带光合电子传输系统的基因。基于转录组的代谢谱计算机模拟预测，然后进行液相色谱分析，证明了类胡萝卜素和质体喹诺醇的合成，但在非光合绿藻中未发现叶绿素色素。瞬态RNA干扰敲低导致抑制塑料醌/塑料喹啉合成。藻类似乎具有由质体末端氧化酶，质体醌/质体喹诺醇和II型NADH脱氢酶介导的电子吸收系统的基因。其他非光合作用的藻类/陆地植物也拥有该系统的关键基因，这表明在非光合作用的质体中电子吸收系统的广泛分布。质体醌/质体喹诺醇池以及因此本文报道的所涉及的电子传输系统可能被保留用于氧化还原稳态，并且可能代表迈向许多非光合成质体中电子传输系统集减少的中间步骤。我们的发现阐明了光合作用丧失后质体电子传输系统还原性进化的广泛分布但先前隐藏的步骤。质体醌/质体醌和II型NADH脱氢酶。其他非光合作用的藻类/陆地植物也拥有该系统的关键基因，这表明在非光合作用的质体中电子吸收系统的广泛分布。质体醌/质体喹诺醇池以及因此本文报道的所涉及的电子传输系统可能被保留用于氧化还原稳态，并且可能代表迈向许多非光合成质体中电子传输系统集减少的中间步骤。我们的发现阐明了光合作用丧失后质体电子传输系统还原性进化的广泛分布但先前隐藏的步骤。质体醌/质体醌和II型NADH脱氢酶。其他非光合作用的藻类/陆地植物也拥有该系统的关键基因，这表明在非光合作用的质体中电子吸收系统的广泛分布。质体醌/质体喹诺醇池以及因此本文报道的所涉及的电子传输系统可能被保留用于氧化还原稳态，并且可能代表迈向许多非光合成质体中电子传输系统集减少的中间步骤。我们的发现阐明了光合作用丧失后质体电子传输系统还原性进化的广泛分布但先前隐藏的步骤。这表明在非光合质体中电子吸收系统的广泛分布。质体醌/质体喹诺醇池以及因此本文报道的所涉及的电子传输系统可能被保留用于氧化还原稳态，并且可能代表迈向许多非光合成质体中电子传输系统集减少的中间步骤。我们的发现阐明了光合作用丧失后质体电子传输系统还原性进化的广泛分布但先前隐藏的步骤。这表明在非光合质体中电子吸收系统的广泛分布。质体醌/质体喹诺醇池以及因此本文报道的所涉及的电子传输系统可能被保留用于氧化还原稳态，并且可能代表迈向许多非光合成质体中电子传输系统集减少的中间步骤。我们的发现阐明了光合作用丧失后质体电子传输系统还原性进化的广泛分布但先前隐藏的步骤。