Urano Daisuke, Maruta Natsumi, Trusov Yuri, Stoian Richard, Wu Qingyu, Liang Ying, Jaiswal Dinesh Kumar, Thung Leena, Jackson David, Botella José Ramón, Jones Alan M
Department of Biology, University of North Carolina, Chapel Hill, NC 27599, USA. Temasek Life Sciences Laboratory, 1 Research Link, National University of Singapore, Singapore 117604, Singapore.
Plant Genetic Engineering Laboratory, School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland 4072, Australia.
Sci Signal. 2016 Sep 20;9(446):ra93. doi: 10.1126/scisignal.aaf9558.
Signaling proteins evolved diverse interactions to provide specificity for distinct stimuli. Signaling complexity in the G protein (heterotrimeric guanosine triphosphate-binding protein) network was achieved in animals through subunit duplication and incremental evolution. By combining comprehensive and quantitative phenotypic profiles of Arabidopsis thaliana with protein evolution informatics, we found that plant heterotrimeric G protein machinery evolved by a saltational (jumping) process. Sequence similarity scores mapped onto tertiary structures, and biochemical validation showed that the extra-large Gα (XLG) subunit evolved extensively in the charophycean algae (an aquatic green plant) by gene duplication and gene fusion. In terrestrial plants, further evolution uncoupled XLG from its negative regulator, regulator of G protein signaling, but preserved an α-helix region that enables interaction with its partner Gβγ. The ancestral gene evolved slowly due to the molecular constraints imposed by the need for the protein to maintain interactions with various partners, whereas the genes encoding XLG proteins evolved rapidly to produce three highly divergent members. Analysis of A. thaliana mutants indicated that these Gα and XLG proteins all function with Gβγ and evolved to operate both independently and cooperatively. The XLG-Gβγ machinery specialized in environmental stress responses, whereas the canonical Gα-Gβγ retained developmental roles. Some developmental processes, such as shoot development, involve both Gα and XLG acting cooperatively or antagonistically. These extensive and rapid evolutionary changes in XLG structure compared to those of the canonical Gα subunit contrast with the accepted notion of how pathway diversification occurs through gene duplication with subsequent incremental coevolution of residues among interacting proteins.
信号蛋白进化出多样的相互作用，以便对不同刺激产生特异性。动物通过亚基重复和渐进式进化，实现了G蛋白（异三聚体鸟苷三磷酸结合蛋白）网络中的信号复杂性。通过将拟南芥全面且定量的表型谱与蛋白质进化信息学相结合，我们发现植物异三聚体G蛋白机制是通过一种跳跃式过程进化而来的。映射到三级结构上的序列相似性得分以及生化验证表明，超大Gα（XLG）亚基在轮藻（一种水生绿色植物）中通过基因重复和基因融合发生了广泛进化。在陆生植物中，进一步的进化使XLG与其负调控因子——G蛋白信号调节因子解偶联，但保留了一个能使其与伴侣Gβγ相互作用的α螺旋区域。由于蛋白质需要与各种伴侣保持相互作用所带来的分子限制，祖先基因进化缓慢，而编码XLG蛋白的基因则快速进化，产生了三个高度不同的成员。对拟南芥突变体的分析表明，这些Gα和XLG蛋白均与Gβγ共同发挥作用，并且进化为既能独立运作也能协同运作。XLG - Gβγ机制专门负责环境应激反应，而经典的Gα - Gβγ则保留了发育方面的作用。一些发育过程，如茎的发育，涉及Gα和XLG协同或拮抗作用。与经典Gα亚基相比，XLG结构中这些广泛而快速的进化变化，与通过基因重复以及随后相互作用蛋白之间残基的渐进式共同进化来实现通路多样化的公认概念形成了对比。
