Evolutionary history expands the range of signaling interactions in hybrid multikinase networks

Abstract Two-component systems (TCSs) are ubiquitous signaling pathways, typically comprising a sensory histidine kinase (HK) and a response regulator, which communicate via intermolecular kinase-to-receiver domain phosphotransfer. Hybrid HKs constitute non-canonical TCS signaling pathways, with tra...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Philippe Ortet, Sylvain Fochesato, Anne-Florence Bitbol, David E. Whitworth, David Lalaouna, Catherine Santaella, Thierry Heulin, Wafa Achouak, Mohamed Barakat
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/555b259ad1ec4d8982e71b4c4ea18d7f
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:555b259ad1ec4d8982e71b4c4ea18d7f
record_format	dspace
spelling	oai:doaj.org-article:555b259ad1ec4d8982e71b4c4ea18d7f2021-12-02T18:25:05ZEvolutionary history expands the range of signaling interactions in hybrid multikinase networks10.1038/s41598-021-91260-w2045-2322https://doaj.org/article/555b259ad1ec4d8982e71b4c4ea18d7f2021-06-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-91260-whttps://doaj.org/toc/2045-2322Abstract Two-component systems (TCSs) are ubiquitous signaling pathways, typically comprising a sensory histidine kinase (HK) and a response regulator, which communicate via intermolecular kinase-to-receiver domain phosphotransfer. Hybrid HKs constitute non-canonical TCS signaling pathways, with transmitter and receiver domains within a single protein communicating via intramolecular phosphotransfer. Here, we report how evolutionary relationships between hybrid HKs can be used as predictors of potential intermolecular and intramolecular interactions (‘phylogenetic promiscuity’). We used domain-swap genes chimeras to investigate the specificity of phosphotransfer within hybrid HKs of the GacS–GacA multikinase network of Pseudomonas brassicacearum. The receiver domain of GacS was replaced with those from nine donor hybrid HKs. Three chimeras with receivers from other hybrid HKs demonstrated correct functioning through complementation of a gacS mutant, which was dependent on strains having a functional gacA. Formation of functional chimeras was predictable on the basis of evolutionary heritage, and raises the possibility that HKs sharing a common ancestor with GacS might remain components of the contemporary GacS network. The results also demonstrate that understanding the evolutionary heritage of signaling domains in sophisticated networks allows their rational rewiring by simple domain transplantation, with implications for the creation of designer networks and inference of functional interactions.Philippe OrtetSylvain FochesatoAnne-Florence BitbolDavid E. WhitworthDavid LalaounaCatherine SantaellaThierry HeulinWafa AchouakMohamed BarakatNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Philippe Ortet Sylvain Fochesato Anne-Florence Bitbol David E. Whitworth David Lalaouna Catherine Santaella Thierry Heulin Wafa Achouak Mohamed Barakat Evolutionary history expands the range of signaling interactions in hybrid multikinase networks
description	Abstract Two-component systems (TCSs) are ubiquitous signaling pathways, typically comprising a sensory histidine kinase (HK) and a response regulator, which communicate via intermolecular kinase-to-receiver domain phosphotransfer. Hybrid HKs constitute non-canonical TCS signaling pathways, with transmitter and receiver domains within a single protein communicating via intramolecular phosphotransfer. Here, we report how evolutionary relationships between hybrid HKs can be used as predictors of potential intermolecular and intramolecular interactions (‘phylogenetic promiscuity’). We used domain-swap genes chimeras to investigate the specificity of phosphotransfer within hybrid HKs of the GacS–GacA multikinase network of Pseudomonas brassicacearum. The receiver domain of GacS was replaced with those from nine donor hybrid HKs. Three chimeras with receivers from other hybrid HKs demonstrated correct functioning through complementation of a gacS mutant, which was dependent on strains having a functional gacA. Formation of functional chimeras was predictable on the basis of evolutionary heritage, and raises the possibility that HKs sharing a common ancestor with GacS might remain components of the contemporary GacS network. The results also demonstrate that understanding the evolutionary heritage of signaling domains in sophisticated networks allows their rational rewiring by simple domain transplantation, with implications for the creation of designer networks and inference of functional interactions.
format	article
author	Philippe Ortet Sylvain Fochesato Anne-Florence Bitbol David E. Whitworth David Lalaouna Catherine Santaella Thierry Heulin Wafa Achouak Mohamed Barakat
author_facet	Philippe Ortet Sylvain Fochesato Anne-Florence Bitbol David E. Whitworth David Lalaouna Catherine Santaella Thierry Heulin Wafa Achouak Mohamed Barakat
author_sort	Philippe Ortet
title	Evolutionary history expands the range of signaling interactions in hybrid multikinase networks
title_short	Evolutionary history expands the range of signaling interactions in hybrid multikinase networks
title_full	Evolutionary history expands the range of signaling interactions in hybrid multikinase networks
title_fullStr	Evolutionary history expands the range of signaling interactions in hybrid multikinase networks
title_full_unstemmed	Evolutionary history expands the range of signaling interactions in hybrid multikinase networks
title_sort	evolutionary history expands the range of signaling interactions in hybrid multikinase networks
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/555b259ad1ec4d8982e71b4c4ea18d7f
work_keys_str_mv	AT philippeortet evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks AT sylvainfochesato evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks AT anneflorencebitbol evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks AT davidewhitworth evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks AT davidlalaouna evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks AT catherinesantaella evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks AT thierryheulin evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks AT wafaachouak evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks AT mohamedbarakat evolutionaryhistoryexpandstherangeofsignalinginteractionsinhybridmultikinasenetworks
_version_	1718378040534237184

Evolutionary history expands the range of signaling interactions in hybrid multikinase networks

Ejemplares similares