Abstract

The adaptation of proteins for novel functions often requires changes in their kinetics via amino acid replacement. This process can require multiple mutations, and therefore extended periods of selection. The transfer of genes among distinct species might speed up the process, by providing proteins already adapted for the novel function. However, this hypothesis remains untested in multicellular eukaryotes. The grass Alloteropsis is an ideal system to test this hypothesis due to its diversity of genes encoding phosphoenolpyruvate carboxylase, an enzyme that catalyzes one of the key reactions in the C₄ pathway. Different accessions of Alloteropsis either use native isoforms relatively recently co-opted from other functions or isoforms that were laterally acquired from distantly related species that evolved the C₄ trait much earlier. By comparing the enzyme kinetics, we show that native isoforms with few amino acid replacements have substrate K_M values similar to the non-C₄ ancestral form, but exhibit marked increases in catalytic efficiency. The co-option of native isoforms was therefore followed by rapid catalytic improvements, which appear to rely on standing genetic variation observed within one species. Native C₄ isoforms with more amino acid replacements exhibit additional changes in affinities, suggesting that the initial catalytic improvements are followed by gradual modifications. Finally, laterally acquired genes show both strong increases in catalytic efficiency and important changes in substrate handling. We conclude that the transfer of genes among distant species sharing the same physiological novelty creates an evolutionary shortcut toward more efficient enzymes, effectively accelerating evolution.

中文翻译：

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横向基因转移是高效C4生物化学的进化捷径。

摘要

使蛋白质适应新功能通常需要通过氨基酸置换改变其动力学。此过程可能需要多个突变，因此需要延长选择时间。通过提供已经适应新功能的蛋白质，不同物种之间的基因转移可能会加快这一过程。但是，这种假说在多细胞真核生物中仍然未经检验。由于其编码磷酸烯醇丙酮酸羧化酶（一种催化C ₄途径中关键反应之一的酶）的基因多样性，草配种异位症是测试该假设的理想系统。同种异体症的不同加入要么使用相对较新的其他功能的天然同工型，要么使用从较早进化出C ₄性状的远缘物种获得的同工型。通过比较酶动力学，我们显示具有很少氨基酸替代的天然同工型具有与非C ₄祖先形式相似的底物K _M值，但显示出催化效率的显着提高。因此，在选择天然同工型之后，迅速进行了催化改进，这似乎依赖于在一个物种中观察到的常规遗传变异。原生C ₄具有更多氨基酸替代物的同工型在亲和力上显示出其他变化，表明最初的催化改进之后是逐渐的修饰。最后，横向获得的基因既显示出催化效率的大幅提高，又显示了底物处理的重要变化。我们得出的结论是，在具有相同生理新奇的遥远物种之间进行基因转移，可为更高效的酶创造一条进化捷径，从而有效地促进进化。