Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes.
Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes.
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DOI：
10.7554/elife.06369
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发表时间：
2015-03-13
期刊：
影响因子：
7.7
通讯作者：
Smirnoff N
中科院分区：
文献类型：
--
作者：
Wheeler G;Ishikawa T;Pornsaksit V;Smirnoff N
抗坏血酸(维生素C)是真核生物体内的一种酶辅助因子，在保护光合作用真核生物免受叶绿体产生的活性氧的破坏方面也起着关键作用。许多动物，包括灵长类，已经成为抗坏血酸营养缺乏症，因为它们的生物合成途径中的末端酶-L-古龙内酯氧化酶(GULO)的丢失。在陆地植物和裸藻中发现的替代途径使用一种不同的末端酶，L-半乳内酯脱氢酶(GLDH)。导致这些不同途径的进化过程及其对抗坏血酸细胞角色的贡献尚不清楚。在这里，我们提出了分子和生化证据，证明在真核光合体获得后，GULO在功能上被GLDH取代。因此，在真核生物进化过程中，GULO反复丢失。在光合作用真核生物中，从过氧化氢的产生中解偶联合成抗坏血酸的替代生物合成途径的形成，可能有助于抗坏血酸作为一种主要的光保护抗氧化剂的兴起。DOI：http://dx.doi.org/10.7554/eLife.06369.001动物、植物、藻类和其他真核生物都需要维生素C来使它们的许多酶正常工作。维生素C还保护植物和藻类细胞免受被称为活性氧物种(ROS)的分子的损害，ROS是这些细胞在光合作用过程中从阳光中获取能量时产生的。光合作用发生在被称为叶绿体的结构中，在真核生物中，当非光合作用的生物从其他藻类获得叶绿体，然后不得不提高对ROS的防御能力时，光合作用已经多次进化。维生素C的产生有几个步骤，在许多动物中，一种名为GULO的酶通过将一种名为醛内酯的分子转化为维生素C来执行最后一步；这一反应还会产生ROS作为废物。GULO酶在人类、灵长类动物和其他一些动物群体中缺失，因此这些生物必须从饮食中获得它们所需的所有维生素C。植物和藻类使用一种不同的酶--称为GLDH--从醛内酯中制造维生素C。GLDH与GULO非常相似，但它不会产生ROS作为废物。目前尚不清楚不同的途径是如何进化的，也不清楚为什么一些动物失去了制造自己的维生素C的能力。使用遗传学和生物化学来研究各种真核生物中维生素C产生的进化起源。这项调查显示，虽然GULO在昆虫和其他几类动物中缺失，但在海绵和许多其他真核生物中存在。这表明GULO在早期的真核生物中进化，后来被不同的动物群体所丢失。另一方面，GLDH只存在于植物和其他能进行光合作用的真核生物中。S等人的发现表明，在所有植物和藻类获得叶绿体后，GULO已经丢失，并被GLDH取代。GDLH允许植物和藻类在不产生ROS的情况下制造维生素C，这可以解释为什么维生素C能够在这些生物体中扮演额外的角色。这一结果使我们能够更好地理解维生素C在光合作用生物体中的功能以及与进化过程中获得叶绿体相关的过程。DOI：http://dx.doi.org/10.7554/eLife.06369.002
Ascorbic acid (vitamin C) is an enzyme co-factor in eukaryotes that also plays a critical role in protecting photosynthetic eukaryotes against damaging reactive oxygen species derived from the chloroplast. Many animal lineages, including primates, have become ascorbate auxotrophs due to the loss of the terminal enzyme in their biosynthetic pathway, l-gulonolactone oxidase (GULO). The alternative pathways found in land plants and Euglena use a different terminal enzyme, l-galactonolactone dehydrogenase (GLDH). The evolutionary processes leading to these differing pathways and their contribution to the cellular roles of ascorbate remain unclear. Here we present molecular and biochemical evidence demonstrating that GULO was functionally replaced with GLDH in photosynthetic eukaryote lineages following plastid acquisition. GULO has therefore been lost repeatedly throughout eukaryote evolution. The formation of the alternative biosynthetic pathways in photosynthetic eukaryotes uncoupled ascorbate synthesis from hydrogen peroxide production and likely contributed to the rise of ascorbate as a major photoprotective antioxidant. DOI: http://dx.doi.org/10.7554/eLife.06369.001 Animals, plants, algae and other eukaryotic organisms all need vitamin C to enable many of their enzymes to work properly. Vitamin C also protects plant and algal cells from damage by molecules called reactive oxygen species (ROS), which can be produced when these cells harvest energy from sunlight in a process called photosynthesis. Photosynthesis occurs inside structures called chloroplasts, and has evolved on multiple occasions in eukaryotes when non-photosynthetic organisms acquired chloroplasts from other algae and then had to develop improved defences against ROS. There are several steps involved in the production of vitamin C. In many animals, an enzyme called GULO carries out the final step by converting a molecule known as an aldonolactone into vitamin C; this reaction also produces ROS as a waste product. The GULO enzyme is missing in humans, primates and some other groups of animals, so these organisms must get all the vitamin C they need from their diet. Plants and algae use a different enzyme—called GLDH—to make vitamin C from aldonolactone. GLDH is very similar to GULO, but it does not produce ROS as a waste product. It is not clear how the different pathways have evolved, or why some animals have lost the ability to make their own vitamin C. Here, Wheeler et al. used genetics and biochemistry to investigate the evolutionary origins of vitamin C production in a variety of eukaryotic organisms. This investigation revealed that although GULO is missing from the insects and several other groups of animals, it is present in the sponges and many other eukaryotes. This suggests that GULO evolved in early eukaryotic organisms and has since been lost by the different groups of animals. On the other hand, GLDH is only found in plants and the other eukaryotes that can photosynthesize. Wheeler et al.'s findings suggest that GULO has been lost and replaced by GLDH in all plants and algae following their acquisition of chloroplasts. GDLH allows plants and algae to make vitamin C without also producing ROS, which could explain why vitamin C has been able to take on an extra role in these organisms. The results allow us to better understand the functions of vitamin C in photosynthetic organisms and the processes associated with the acquisition of chloroplasts during evolution. DOI: http://dx.doi.org/10.7554/eLife.06369.002