Kern Ramona, Facchinelli Fabio, Delwiche Charles, Weber Andreas P M, Bauwe Hermann, Hagemann Martin
Plant Physiology, Institute of Biological Sciences, University of Rostock, Albert-Einstein-Str. 3, D-18051 Rostock, Germany.
Institute of Plant Biochemistry, Cluster of Excellence on Plant Science (CEPLAS), Heinrich-Heine-University Düsseldorf, 40225 Düsseldorf, Germany.
Plants (Basel). 2020 Jan 15;9(1):106. doi: 10.3390/plants9010106.
Photorespiration has been shown to be essential for all oxygenic phototrophs in the present-day oxygen-containing atmosphere. The strong similarity of the photorespiratory cycle in cyanobacteria and plants led to the hypothesis that oxygenic photosynthesis and photorespiration co-evolved in cyanobacteria, and then entered the eukaryotic algal lineages up to land plants via endosymbiosis. However, the evolutionary origin of the photorespiratory enzyme glycolate oxidase (GOX) is controversial, which challenges the common origin hypothesis. Here, we tested this hypothesis using phylogenetic and biochemical approaches with broad taxon sampling. Phylogenetic analysis supported the view that a cyanobacterial GOX-like protein of the 2-hydroxy-acid oxidase family most likely served as an ancestor for GOX in all eukaryotes. Furthermore, our results strongly indicate that GOX was recruited to the photorespiratory metabolism at the origin of Archaeplastida, because we verified that Glaucophyta, Rhodophyta, and Streptophyta all express GOX enzymes with preference for the substrate glycolate. Moreover, an "ancestral" protein synthetically derived from the node separating all prokaryotic from eukaryotic GOX-like proteins also preferred glycolate over l-lactate. These results support the notion that a cyanobacterial ancestral protein laid the foundation for the evolution of photorespiratory GOX enzymes in modern eukaryotic phototrophs.
在当今含氧的大气环境中，光呼吸作用已被证明对所有产氧光合生物来说都是必不可少的。蓝细菌和植物中光呼吸循环的高度相似性，引发了这样一种假说：产氧光合作用和光呼吸作用在蓝细菌中共同进化，然后通过内共生作用进入真核藻类谱系，直至陆地植物。然而，光呼吸酶乙醇酸氧化酶（GOX）的进化起源存在争议，这对共同起源假说提出了挑战。在此，我们运用系统发育和生化方法，并进行广泛的分类群取样，对这一假说进行了验证。系统发育分析支持了这样一种观点：2-羟基酸氧化酶家族中一种类似蓝细菌GOX的蛋白质很可能是所有真核生物中GOX的祖先。此外，我们的结果有力地表明，GOX在古质体起源时就被纳入了光呼吸代谢，因为我们证实了灰胞藻、红藻和链形植物都表达对底物乙醇酸有偏好的GOX酶。此外，一种通过合成得到的“祖先”蛋白质，来源于将所有原核生物与真核生物中类似GOX的蛋白质分隔开来的节点，它对乙醇酸的偏好也高于L-乳酸。这些结果支持了这样一种观点：一种蓝细菌的祖先蛋白质为现代真核光合生物中光呼吸GOX酶的进化奠定了基础。
