How do regulatory networks evolve and expand throughout evolution?

Voordeckers, Karin; Pougach, Ksenia; Verstrepen, Kevin J.

doi:10.1016/j.copbio.2015.02.001

Cited by 94 publications

(94 citation statements)

References 68 publications

(87 reference statements)

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“…This functional diversification was not driven by divergent gene expression (Hughes and Friedman, 2005), nor different cellular localization (Marques et al, 2008) or biochemical mode of action. Rather, it is likely the consequence of altered substrate recognition through mutations in the recognition domains, reminiscent of alterations recently described in transcription factors (Singh and Hannenhalli, 2008; Voordeckers et al, 2015). …”

Section: Discussionmentioning

confidence: 96%

CLIPB8 is part of the prophenoloxidase activation system in Anopheles gambiae mosquitoes

Zhang

Sprigg

et al. 2016

Insect Biochemistry and Molecular Biology

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In insects and other arthropods the formation of eumelanin (melanization) is a broad spectrum and potent immune response that is used to encapsulate and kill invading pathogens. This immune response is regulated by the activation of prophenoxidase (proPO), which is controlled by proteinase cascades and its serpin inhibitors, together forming the proPO activation system. While the molecular composition of these protease cascades are well understood in insect model systems, major knowledge gaps remain in mosquitoes. Recently, a regulatory unit of melanization in Anopheles gambiae was documented, comprised of the inhibitory serpin-clip-serine proteinase, CLIPB9 and its inhibitor serpin-2 (SRPN2). Partial reversion of SRPN2 phenotypes in melanotic tumor formation and adult survival by SRPN2/CLIPB9 double knockdown suggested other target proteinases of SRPN2 in regulating melanization. Here we report that CLIPB8 supplements the SRPN2/CLIPB9 regulatory unit in controlling melanization in An. gambiae. As with CLIPB9, knockdown of CLIPB8 partially reversed the pleiotropic phenotype induced by SRPN2 silencing with regards to adult survival and melanotic tumor formation. Recombinant SRPN2 protein formed an SDS-stable protein complex with activated recombinant CLIPB8, however did not efficiently inhibit CLIPB8 activity in vitro. CLIPB8 did not directly activate proPO in vitro nor was it able to cleave and activate proCLIPB9. Nevertheless, epistasis analysis using RNAi placed CLIPB8 and CLIPB9 in the same pathway leading to melanization, suggesting that CLIPB8 either acts further upstream of CLIPB9 or is required for activation of a yet to be identified serine proteinase homolog. Taken together, this study identifies CLIPB8 as an additional player in proPO activation cascade and highlights the complexity of the proteinase network that regulates melanization in An. gambiae.

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Section: Discussionmentioning

confidence: 96%

CLIPB8 is part of the prophenoloxidase activation system in Anopheles gambiae mosquitoes

Zhang

Sprigg

et al. 2016

Insect Biochemistry and Molecular Biology

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“…Here, the promiscuous form is the duplicated phr and not a single Phr peptide, which interacts with both Rap variants. Second, duplications are typically only considered important if both diverged duplicates survive over evolutionary timescales [3]. In contrast, Phr duplication and divergence are evolutionarily crucial for a specificity shift, but to complete the shift it has to be transient—with either divergence or duplication itself being lost.…”

Section: Discussionmentioning

confidence: 99%

Transient Duplication-Dependent Divergence and Horizontal Transfer Underlie the Evolutionary Dynamics of Bacterial Cell–Cell Signaling

et al. 2016

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Evolutionary expansion of signaling pathway families often underlies the evolution of regulatory complexity. Expansion requires the acquisition of a novel homologous pathway and the diversification of pathway specificity. Acquisition can occur either vertically, by duplication, or through horizontal transfer, while divergence of specificity is thought to occur through a promiscuous protein intermediate. The way by which these mechanisms shape the evolution of rapidly diverging signaling families is unclear. Here, we examine this question using the highly diversified Rap-Phr cell–cell signaling system, which has undergone massive expansion in the genus Bacillus. To this end, genomic sequence analysis of >300 Bacilli genomes was combined with experimental analysis of the interaction of Rap receptors with Phr autoinducers and downstream targets. Rap-Phr expansion is shown to have occurred independently in multiple Bacillus lineages, with >80 different putative rap-phr alleles evolving in the Bacillius subtilis group alone. The specificity of many rap-phr alleles and the rapid gain and loss of Rap targets are experimentally demonstrated. Strikingly, both horizontal and vertical processes were shown to participate in this expansion, each with a distinct role. Horizontal gene transfer governs the acquisition of already diverged rap-phr alleles, while intralocus duplication and divergence of the phr gene create the promiscuous intermediate required for the divergence of Rap-Phr specificity. Our results suggest a novel role for transient gene duplication and divergence during evolutionary shifts in specificity.

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“…Duplicate gene differentiation has heavily impacted the evolution of regulatory and metabolic networks (Reece-Hoyes et al, 2013; Voordeckers et al, 2015). Paralogs have contributed to the expansion of regulatory networks (Teichmann and Babu, 2004), the derivation of novel networks (Conant and Wolfe, 2006; Wapinski et al, 2010; Pérez et al, 2014; Pougach et al, 2014), the specialization of network regulation (Lin and Li, 2011), and the robustness of networks to perturbation (Papp et al, 2004; Deutscher et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network

Kuang

Hutchins

Russell

et al. 2016

eLife

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The evolutionary mechanisms leading to duplicate gene retention are well understood, but the long-term impacts of paralog differentiation on the regulation of metabolism remain underappreciated. Here we experimentally dissect the functions of two pairs of ancient paralogs of the GALactose sugar utilization network in two yeast species. We show that the Saccharomyces uvarum network is more active, even as over-induction is prevented by a second co-repressor that the model yeast Saccharomyces cerevisiae lacks. Surprisingly, removal of this repression system leads to a strong growth arrest, likely due to overly rapid galactose catabolism and metabolic overload. Alternative sugars, such as fructose, circumvent metabolic control systems and exacerbate this phenotype. We further show that S. cerevisiae experiences homologous metabolic constraints that are subtler due to how the paralogs have diversified. These results show how the functional differentiation of paralogs continues to shape regulatory network architectures and metabolic strategies long after initial preservation.DOI: http://dx.doi.org/10.7554/eLife.19027.001

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How do regulatory networks evolve and expand throughout evolution?

Cited by 94 publications

References 68 publications

CLIPB8 is part of the prophenoloxidase activation system in Anopheles gambiae mosquitoes

CLIPB8 is part of the prophenoloxidase activation system in Anopheles gambiae mosquitoes

Transient Duplication-Dependent Divergence and Horizontal Transfer Underlie the Evolutionary Dynamics of Bacterial Cell–Cell Signaling

Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network

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