Evolutionary rate patterns of genes involved in the Drosophila Toll and Imd signaling pathway

Han, Min; Qin, Sheng; Song, Xiaojun; Li, Yafang; Park, Jin; Chen, Liming; Ma, Fei

doi:10.1186/1471-2148-13-245

Cited by 26 publications

(30 citation statements)

References 67 publications

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“…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). Indeed, our data indicate that one potential driver of differences in evolutionary rates among genes in the network may be the number of interactions that a gene has with other genes or proteins (i.e., connectivity; SI Results) similar to what has been seen in other systems (54-56, but see refs.…”

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

confidence: 83%

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

confidence: 83%

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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“…Finally, it is well-known that immune related genes evolve faster than non-immune genes due to constant evolutionarily pressures on hosts to neutralize pathogen novelties. Interestingly, when analysing 50 genes involved in the Drosophila Toll and Imd signalling pathways, Han et al realized a strong negative correlation between the rate of evolution of the immune proteins and the number of their regulatory miRNAs, suggesting that genes regulated by more miRNAs evolve slower due to stronger functional constraints (Han et al, 2013). This suggests the role of miRNAs in the evolution of immune related genes in insects.…”

Section: Role Of Mirnas In Regulation Of Insect Immunitymentioning

confidence: 99%

MicroRNAs as mediators of insect host–pathogen interactions and immunity

Hussain

Asgari

2014

Journal of Insect Physiology

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“…Thus, one possible explanation is that the more downstream components may be under stronger purifying selection because of this dual function in the OXPHOS pathway. As inferred here, several other studies conducted on various biological pathways have also reported a negative correlation between selective constraints and gene position within a pathway, such as the yeast HOG signal transduction pathway (Wu et al ., ), the primate N‐glycosylation metabolic pathway (Montanucci et al ., ), the vertebrate insulin and TOR signal transduction pathway (Alvarez‐Ponce et al ., ), the Drosophila Toll and Imd signalling pathways (Han et al ., ) and the plant isoprene biosynthetic pathway (Sharkey et al ., ). Furthermore, in the Suidae Toll‐like receptor (TLR) signalling pathway, downstream genes also evolved under higher levels of selective constraint than did upstream genes (Darfour‐Oduro et al ., ).…”

Section: Discussionmentioning

confidence: 99%

“…In other cases, genes occupying central positions tended to be more constrained than peripheral genes (Lavagnino et al ., ; Invergo et al ., ). Additionally, network parameters including protein length (Darfour‐Oduro et al ., ), the number of PPIs (Lemos et al ., ), codon bias (Montanucci et al ., ), microRNAs (miRNAs) (Han et al ., ) and the length of the 3′‐untranslated region (Darfour‐Oduro et al ., ) were also found to affect the evolutionary rate of genes within gene pathways and networks.…”

Section: Introductionmentioning

confidence: 99%

Stronger selective constraint on downstream genes in the oxidative phosphorylation pathway of cetaceans

Tian

Chai

et al. 2017

J of Evolutionary Biology

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The oxidative phosphorylation (OXPHOS) pathway is an efficient way to produce energy via adenosine triphosphate (ATP), which is critical for sustaining an energy supply for cetaceans in a hypoxic environment. Several studies have shown that natural selection may shape the evolution of the genes involved in OXPHOS. However, how network architecture drives OXPHOS protein sequence evolution remains poorly explored. Here, we investigated the evolutionary patterns of genes in the OXPHOS pathway across six cetacean genomes within the framework of a functional network. Our results show a negative correlation between the strength of purifying selection and pathway position. This result indicates that downstream genes were subjected to stronger evolutionary constraints than upstream genes, which may be due to the dual function of ATP synthase in the OXPHOS pathway. Additionally, there was a positive correlation between codon usage bias and omega (ω = dN/dS) and a negative correlation with synonymous substitution rate (dS), indicating that the stronger selective constraint on genes (with less biased codon usage) along the OXPHOS pathway is attributable to an increase in the rate of synonymous substitution. Surprisingly, there was no significant correlation between protein-protein interactions and the evolutionary estimates, implying that highly connected enzymes may not always show greater evolutionary constraints. Compared with that observed for terrestrial mammals, we found that the signature of positive selection detected in five genes (ATP5J, LHPP, PPA1, UQCRC1 and UQCRQ) was cetacean-specific, reflecting the importance of OXPHOS for survival in hypoxic, aquatic environments.

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Evolutionary rate patterns of genes involved in the Drosophila Toll and Imd signaling pathway

Cited by 26 publications

References 67 publications

Rapid molecular evolution across amniotes of the IIS/TOR network

Rapid molecular evolution across amniotes of the IIS/TOR network

MicroRNAs as mediators of insect host–pathogen interactions and immunity

Stronger selective constraint on downstream genes in the oxidative phosphorylation pathway of cetaceans

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