Towards resolution of a paradox in plant G-protein signaling

Towards resolution of a paradox in plant G-protein signaling
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DOI:
10.1093/plphys/kiab534
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发表时间:
2022-02-04
期刊:
影响因子:
7.4
通讯作者:
Jones, Alan M.
Jones, Alan M.
中科院分区:
生物学1区
文献类型:
--
作者:
Ghusinga, Khem Raj;Elston, Timothy C.;Jones, Alan M.

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G蛋白是分子开关,参与将各种细胞外信号传递到其细胞内靶点。在动物和酵母系统中,开关属性是通过核苷酸编码的:GDP结合状态是“关闭状态”,而GTP结合状态是“开启状态”。G蛋白循环由通过由G蛋白偶联受体促进的核苷酸交换打开的开关和通过由G信号调节因子1(RGS)促进的GTP水解回到GDP关闭的开关组成。在植物中,G蛋白信号与动物和酵母中的G蛋白信号截然不同。尽管在16亿年的时间里,核苷酸结合和催化结构严格保守,将植物和动物的进化分开,但遗传和生物化学数据表明,核苷酸交换对于这种开关在植物中的运作并不那么重要。此外,在拟南芥(Arabidopsis thaliana)的单一RGS蛋白的损失赋予意想不到的较弱的表型与G循环的作用减弱一致,至少在静态条件下。然而,在动态条件下,拟南芥中RGS的遗传消除导致强表型。我们探索这个难题的解释,制定一个数学模型,考虑到越来越多的证据磷酸化在植物中的G-蛋白信号的不可或缺的作用,G-蛋白循环需要处理动态信号输入。我们推测,植物G蛋白循环及其伴随的组件演变过程中的动态信号通过信号调制,而不是通过开关,开关样调节信号。这种所谓的变化检测可能赋予植物更大的适应性,因为它们在动态光、温度和害虫环境中的无感性。植物G信号开关的数学模型与最近的数据一致,并表明G信号的7-跨膜调节器在处理动态信号中的作用。
G-proteins are molecular on-off switches that are involved in transmitting a variety of extracellular signals to their intracellular targets. In animal and yeast systems, the switch property is encoded through nucleotides: a GDP-bound state is the "off-state" and the GTP-bound state is the "on-state". The G-protein cycle consists of the switch turning on through nucleotide exchange facilitated by a G-protein coupled receptor and the switch turning off through hydrolysis of GTP back to GDP, facilitated by a protein designated REGULATOR OF G SIGNALING 1 (RGS). In plants, G-protein signaling dramatically differs from that in animals and yeast. Despite stringent conservation of the nucleotide binding and catalytic structures over the 1.6 billion years that separate the evolution of plants and animals, genetic and biochemical data indicate that nucleotide exchange is less critical for this switch to operate in plants. Also, the loss of the single RGS protein in Arabidopsis (Arabidopsis thaliana) confers unexpectedly weaker phenotypes consistent with a diminished role for the G cycle, at least under static conditions. However, under dynamic conditions, genetic ablation of RGS in Arabidopsis results in a strong phenotype. We explore explanations to this conundrum by formulating a mathematical model that takes into account the accruing evidence for the indispensable role of phosphorylation in G-protein signaling in plants and that the G-protein cycle is needed to process dynamic signal inputs. We speculate that the plant G-protein cycle and its attendant components evolved to process dynamic signals through signaling modulation rather than through on-off, switch-like regulation of signaling. This so-called change detection may impart greater fitness for plants due to their sessility in a dynamic light, temperature, and pest environment.A mathematical model of the plant G-signaling switch agrees with recent data and suggests a role of 7-transmembrane regulator of G signaling in processing dynamical signals.