The Molecular Evolutionary Patterns of the Insulin/FOXO Signaling Pathway

Wang, Minghui; Wang, Qishan; Wang, Zhen; Wang, Qingping; Zhang, Xiangzhe; Pan, Yuchun

doi:10.4137/ebo.s10539

Cited by 13 publications

(23 citation statements)

References 60 publications

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“…However, no differentially expressed genes were associated directly with these pathways. This can possibly be attributed to their high degree of conservation [ 39 , 70 ], given that many of these genes are selectively constrained [ 71 , 72 ]. However, our analyses did reveal differential expression of genes involved in metabolism ( bgm , CG2469 , CG10116 , CG10962 , CG33958 , Cyp4d1 , GstD2 , HIP , Ipk1 , phr , SP1029 , tej , tld ).…”

Section: Discussionmentioning

confidence: 99%

Artificial selection for odor-guided behavior in Drosophila reveals changes in food consumption

et al. 2017

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BackgroundThe olfactory system enables organisms to detect chemical cues in the environment and can signal the availability of food or the presence of a predator. Appropriate behavioral responses to these chemical cues are therefore important for organismal survival and can influence traits such as organismal life span and food consumption. However, understanding the genetic mechanisms underlying odor-guided behavior, correlated responses in other traits, and how these constrain or promote their evolution, remain an important challenge. Here, we performed artificial selection for attractive and aversive behavioral responses to four chemical compounds, two aromatics (4-ethylguaiacol and 4-methylphenol) and two esters (methyl hexanoate and ethyl acetate), for thirty generations.ResultsArtificial selection for odor-guided behavior revealed symmetrical responses to selection for each of the four chemical compounds. We then investigated whether selection for odor-guided behavior resulted in correlated responses in life history traits and/or food consumption. We found changes in food consumption upon selection for behavioral responses to aromatics. In many cases, lines selected for increased attraction to aromatics showed an increase in food consumption. We then performed RNA sequencing of lines selected for responses to 4-ethylguaiacol to identify candidate genes associated with odor-guided behavior and its impact on food consumption. We identified 91 genes that were differentially expressed among lines, many of which were associated with metabolic processes. RNAi-mediated knockdown of select candidate genes further supports their role in odor-guided behavior and/or food consumption.ConclusionsThis study identifies novel genes underlying variation in odor-guided behavior and further elucidates the genetic mechanisms underlying the interrelationship between olfaction and feeding.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4233-1) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Artificial selection for odor-guided behavior in Drosophila reveals changes in food consumption

et al. 2017

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“…However, our findings of elevated ωs agree with those of ref. 28 and supply further support that extracellular components are among the fastest evolving genes in the IIS/TOR network (22), as is likely true in other networks. Overall, our data are in agreement with reports that receptors and other extracellular components of signal transduction pathways appear to be under less purifying selection than intracellular components (51)(52)(53).…”

Section: Members Of Iis/tor Network Are Outliers In Evolutionary Ratementioning

confidence: 99%

“…S1) often experienced positive selection, whereas intracellular genes often experienced purifying selection (22)(23)(24)(25)(26)(27)(28), especially farther downstream in the intracellular network. These previous findings have supported the prediction that upstream extracellular factors (e.g., the initial components that interact with environmental stimuli in signal transduction pathways) may have larger impacts on signaling through the network than downstream components.…”

Section: Significancementioning

confidence: 99%

Rapid molecular evolution across amniotes of the IIS/TOR network

McGaugh

Bronikowski

Kuo

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The insulin/insulin-like signaling and target of rapamycin (IIS/TOR) network regulates lifespan and reproduction, as well as metabolic diseases, cancer, and aging. Despite its vital role in health, comparative analyses of IIS/TOR have been limited to invertebrates and mammals. We conducted an extensive evolutionary analysis of the IIS/TOR network across 66 amniotes with 18 newly generated transcriptomes from nonavian reptiles and additional available genomes/transcriptomes. We uncovered rapid and extensive molecular evolution between reptiles (including birds) and mammals: (i) the IIS/TOR network, including the critical nodes insulin receptor substrate (IRS) and phosphatidylinositol 3-kinase (PI3K), exhibit divergent evolutionary rates between reptiles and mammals; (ii) compared with a proxy for the rest of the genome, genes of the IIS/TOR extracellular network exhibit exceptionally fast evolutionary rates; and (iii) signatures of positive selection and coevolution of the extracellular network suggest reptile-and mammal-specific interactions between members of the network. In reptiles, positively selected sites cluster on the binding surfaces of insulin-like growth factor 1 (IGF1), IGF1 receptor (IGF1R), and insulin receptor (INSR); whereas in mammals, positively selected sites clustered on the IGF2 binding surface, suggesting that these hormone-receptor binding affinities are targets of positive selection. Further, contrary to reports that IGF2R binds IGF2 only in marsupial and placental mammals, we found positively selected sites clustered on the hormone binding surface of reptile IGF2R that suggest that IGF2R binds to IGF hormones in diverse taxa and may have evolved in reptiles. These data suggest that key IIS/TOR paralogs have sub-or neofunctionalized between mammals and reptiles and that this network may underlie fundamental life history and physiological differences between these amniote sister clades.insulin signaling | insulin growth factor | molecular evolution | rapamycin T he last 20 y has provided overwhelming support that the insulin-and insulin-like signaling/target of rapamycin (IIS/TOR) molecular network responds to stress and nutrients and underlies a wide range of physiological functions (1); cancer, metabolic syndrome, and diabetes (2); and the timing of life events (e.g., growth, maturation, reproduction, and aging) (3). The vertebrate IIS/TOR network consists of peptide hormones, binding proteins that regulate hormone bioavailability, and cell membrane receptors (hereafter, extracellular proteins of the IIS/TOR network) that induce an intracellular signaling cascade (hereafter, intracellular proteins of the IIS/TOR network) to stimulate cell proliferation, survival, and metabolism (Fig. S1). The core intracellular signal transduction genes in this network are largely conserved across deep phylogenetic time (4, 5). In contrast, genes encoding the IIS/TOR extracellular network have diverged in the vertebrate lineage (6-8) and may have variable roles among taxa (9, 10). Despite its central rol...

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“…Studies have indicated that many factors affect the evolutionary rate of genes within gene pathways and networks. For example, gene position [ 3 , 4 ], protein length [ 5 ], the number of protein-protein interactions [ 6 , 7 ] and codon bias [ 8 , 9 ] have influence on gene evolution. Signaling pathways mediate the sensing and processing of both extracellular and intracellular stimuli.…”

Section: Introductionmentioning

confidence: 99%

“…This observation is consistent with trends reported for the yeast HOG-signaling pathway [ 11 ] and the Caenorhabditis elegans and Drosophila insulin/TOR pathway [ 12 , 13 ]. In contrast, evolutionary patterns of the Insulin/FOXO signaling pathway across metazoan species genomes indicated that components within the middle of the pathway were rather under stronger purifying selection [ 9 ]. Moreover, within the Drosophila Ras signaling pathway, upstream genes have lower evolutionary rate, suggesting more constraints, than downstream genes [ 14 ].…”

Section: Introductionmentioning

confidence: 99%

Evolutionary patterns of Toll-like receptor signaling pathway genes in the Suidae

et al. 2016

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BackgroundThe Toll-like receptor (TLR) signaling pathway constitutes an essential component of the innate immune system. Highly conserved proteins, indicative of their critical roles in host survival, characterize this pathway. Selective constraints could vary depending on the gene’s position within the pathway as TLR signaling is a sequential process and that genes downstream of the TLRs may be more selectively constrained to ensure efficient immune responses given the important role of downstream genes in the signaling process. Thus, we investigated whether gene position influenced protein evolution in the TLR signaling pathway of the Suidae. The members of the Suidae examined included the European Sus scrofa (wild boar), Asian Sus scrofa (wild boar), Sus verrucosus, Sus celebensis, Sus scebifrons, Sus barbatus, Babyrousa babyrussa, Potamochoerus larvatus, Potamochoerus porcus and Phacochoerus africanus.ResultsA total of 33 TLR signaling pathway genes in the Suidae were retrieved from resequencing data. The evolutionary parameter ω (dn/ds) had an overall mean of 0.1668 across genes, indicating high functional conservation within the TLR signaling pathway. A significant relationship was inferred for the network parameters gene position, number of protein-protein interactions, protein length and the evolutionary parameter dn (nonsynonymous substitutions) such that downstream genes had lower nonsynonymous substitution rates, more interactors and shorter protein length than upstream genes. Gene position was significantly correlated with the number of protein-protein interactions and protein length. Thus, the polarity in the selective constraint along the TLR signaling pathway was due to the number of molecules a protein interacted with and the protein’s length.ConclusionResults indicate that the level of selective constraints on genes within the TLR signaling pathway of the Suidae is dependent on the gene’s position and network parameters. In particular, downstream genes evolve more slowly as a result of being highly connected and having shorter protein lengths. These findings highlight the critical role of gene network parameters in gene evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0602-7) contains supplementary material, which is available to authorized users.

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The Molecular Evolutionary Patterns of the Insulin/FOXO Signaling Pathway

Cited by 13 publications

References 60 publications

Artificial selection for odor-guided behavior in Drosophila reveals changes in food consumption

Artificial selection for odor-guided behavior in Drosophila reveals changes in food consumption

Rapid molecular evolution across amniotes of the IIS/TOR network

Evolutionary patterns of Toll-like receptor signaling pathway genes in the Suidae

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