Dissection of MAPK signaling specificity through protein engineering in a developmental context

Autores
Wengier, Diego Leonardo; Lampard, Gregory R.; Bergmann, Dominique C.
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Background: Mitogen-activated protein kinases (MAPK) signaling affects many processes, some of which have different outcomes in the same cell. In Arabidopsis, activation of a MAPK cascade consisting of YODA, MKK4/5 and MPK3/6 inhibits early stages of stomatal developmental, but the ability to halt stomatal progression is lost at the later stage when guard mother cells (GMCs) transition to guard cells (GCs). Rather than downregulating cascade components, stomatal precursors must have a mechanism to prevent late stage inhibition because the same MKKs and MPKs mediate other physiological responses. Results: We artificially activated the MAPK cascade using MKK7, another MKK that can modulate stomatal development, and found that inhibition of stomatal development is still possible in GMCs. This suggests that MKK4/5, but not MKK7, are specifically prevented from inhibiting stomatal development. To identify regions of MKKs responsible for cell-type specific regulation, we used a domain swap approach with MKK7 and a battery of in vitro and in vivo kinase assays. We found that N-terminal regions of MKK5 and MKK7 establish specific signal-to-output connections like they do in other organisms, but they do so in combination with previously undescribed modules in the C-terminus. One of these modules encoding the GMC-specific regulation of MKK5, when swapped with sequences from the equivalent region of MKK7, allows MKK5 to mediate robust inhibition of late stomatal development. Conclusions: Because MKK structure is conserved across species, the identification of new MKK specificity modules and signaling rules furthers our understanding of how eukaryotes create specificity in complex biological systems.
Fil: Wengier, Diego Leonardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina. Howard Hughes Medical Institute; Estados Unidos
Fil: Lampard, Gregory R.. Howard Hughes Medical Institute; Estados Unidos
Fil: Bergmann, Dominique C.. Howard Hughes Medical Institute; Estados Unidos. Stanford University; Estados Unidos
Materia
MAPK SPECIFICITY
NETWORK REWIRING
SIGNAL TRANSDUCTION
STOMATAL DEVELOPMENT
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/79851

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network_name_str CONICET Digital (CONICET)
spelling Dissection of MAPK signaling specificity through protein engineering in a developmental contextWengier, Diego LeonardoLampard, Gregory R.Bergmann, Dominique C.MAPK SPECIFICITYNETWORK REWIRINGSIGNAL TRANSDUCTIONSTOMATAL DEVELOPMENThttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Background: Mitogen-activated protein kinases (MAPK) signaling affects many processes, some of which have different outcomes in the same cell. In Arabidopsis, activation of a MAPK cascade consisting of YODA, MKK4/5 and MPK3/6 inhibits early stages of stomatal developmental, but the ability to halt stomatal progression is lost at the later stage when guard mother cells (GMCs) transition to guard cells (GCs). Rather than downregulating cascade components, stomatal precursors must have a mechanism to prevent late stage inhibition because the same MKKs and MPKs mediate other physiological responses. Results: We artificially activated the MAPK cascade using MKK7, another MKK that can modulate stomatal development, and found that inhibition of stomatal development is still possible in GMCs. This suggests that MKK4/5, but not MKK7, are specifically prevented from inhibiting stomatal development. To identify regions of MKKs responsible for cell-type specific regulation, we used a domain swap approach with MKK7 and a battery of in vitro and in vivo kinase assays. We found that N-terminal regions of MKK5 and MKK7 establish specific signal-to-output connections like they do in other organisms, but they do so in combination with previously undescribed modules in the C-terminus. One of these modules encoding the GMC-specific regulation of MKK5, when swapped with sequences from the equivalent region of MKK7, allows MKK5 to mediate robust inhibition of late stomatal development. Conclusions: Because MKK structure is conserved across species, the identification of new MKK specificity modules and signaling rules furthers our understanding of how eukaryotes create specificity in complex biological systems.Fil: Wengier, Diego Leonardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina. Howard Hughes Medical Institute; Estados UnidosFil: Lampard, Gregory R.. Howard Hughes Medical Institute; Estados UnidosFil: Bergmann, Dominique C.. Howard Hughes Medical Institute; Estados Unidos. Stanford University; Estados UnidosBioMed Central2018-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/79851Wengier, Diego Leonardo; Lampard, Gregory R.; Bergmann, Dominique C.; Dissection of MAPK signaling specificity through protein engineering in a developmental context; BioMed Central; BMC Plant Biology; 18; 1; 4-2018; 1-171471-2229CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1186/s12870-018-1274-9info:eu-repo/semantics/altIdentifier/url/https://bmcplantbiol.biomedcentral.com/articles/10.1186/s12870-018-1274-9info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:50:14Zoai:ri.conicet.gov.ar:11336/79851instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:50:14.821CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Dissection of MAPK signaling specificity through protein engineering in a developmental context
title Dissection of MAPK signaling specificity through protein engineering in a developmental context
spellingShingle Dissection of MAPK signaling specificity through protein engineering in a developmental context
Wengier, Diego Leonardo
MAPK SPECIFICITY
NETWORK REWIRING
SIGNAL TRANSDUCTION
STOMATAL DEVELOPMENT
title_short Dissection of MAPK signaling specificity through protein engineering in a developmental context
title_full Dissection of MAPK signaling specificity through protein engineering in a developmental context
title_fullStr Dissection of MAPK signaling specificity through protein engineering in a developmental context
title_full_unstemmed Dissection of MAPK signaling specificity through protein engineering in a developmental context
title_sort Dissection of MAPK signaling specificity through protein engineering in a developmental context
dc.creator.none.fl_str_mv Wengier, Diego Leonardo
Lampard, Gregory R.
Bergmann, Dominique C.
author Wengier, Diego Leonardo
author_facet Wengier, Diego Leonardo
Lampard, Gregory R.
Bergmann, Dominique C.
author_role author
author2 Lampard, Gregory R.
Bergmann, Dominique C.
author2_role author
author
dc.subject.none.fl_str_mv MAPK SPECIFICITY
NETWORK REWIRING
SIGNAL TRANSDUCTION
STOMATAL DEVELOPMENT
topic MAPK SPECIFICITY
NETWORK REWIRING
SIGNAL TRANSDUCTION
STOMATAL DEVELOPMENT
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Background: Mitogen-activated protein kinases (MAPK) signaling affects many processes, some of which have different outcomes in the same cell. In Arabidopsis, activation of a MAPK cascade consisting of YODA, MKK4/5 and MPK3/6 inhibits early stages of stomatal developmental, but the ability to halt stomatal progression is lost at the later stage when guard mother cells (GMCs) transition to guard cells (GCs). Rather than downregulating cascade components, stomatal precursors must have a mechanism to prevent late stage inhibition because the same MKKs and MPKs mediate other physiological responses. Results: We artificially activated the MAPK cascade using MKK7, another MKK that can modulate stomatal development, and found that inhibition of stomatal development is still possible in GMCs. This suggests that MKK4/5, but not MKK7, are specifically prevented from inhibiting stomatal development. To identify regions of MKKs responsible for cell-type specific regulation, we used a domain swap approach with MKK7 and a battery of in vitro and in vivo kinase assays. We found that N-terminal regions of MKK5 and MKK7 establish specific signal-to-output connections like they do in other organisms, but they do so in combination with previously undescribed modules in the C-terminus. One of these modules encoding the GMC-specific regulation of MKK5, when swapped with sequences from the equivalent region of MKK7, allows MKK5 to mediate robust inhibition of late stomatal development. Conclusions: Because MKK structure is conserved across species, the identification of new MKK specificity modules and signaling rules furthers our understanding of how eukaryotes create specificity in complex biological systems.
Fil: Wengier, Diego Leonardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina. Howard Hughes Medical Institute; Estados Unidos
Fil: Lampard, Gregory R.. Howard Hughes Medical Institute; Estados Unidos
Fil: Bergmann, Dominique C.. Howard Hughes Medical Institute; Estados Unidos. Stanford University; Estados Unidos
description Background: Mitogen-activated protein kinases (MAPK) signaling affects many processes, some of which have different outcomes in the same cell. In Arabidopsis, activation of a MAPK cascade consisting of YODA, MKK4/5 and MPK3/6 inhibits early stages of stomatal developmental, but the ability to halt stomatal progression is lost at the later stage when guard mother cells (GMCs) transition to guard cells (GCs). Rather than downregulating cascade components, stomatal precursors must have a mechanism to prevent late stage inhibition because the same MKKs and MPKs mediate other physiological responses. Results: We artificially activated the MAPK cascade using MKK7, another MKK that can modulate stomatal development, and found that inhibition of stomatal development is still possible in GMCs. This suggests that MKK4/5, but not MKK7, are specifically prevented from inhibiting stomatal development. To identify regions of MKKs responsible for cell-type specific regulation, we used a domain swap approach with MKK7 and a battery of in vitro and in vivo kinase assays. We found that N-terminal regions of MKK5 and MKK7 establish specific signal-to-output connections like they do in other organisms, but they do so in combination with previously undescribed modules in the C-terminus. One of these modules encoding the GMC-specific regulation of MKK5, when swapped with sequences from the equivalent region of MKK7, allows MKK5 to mediate robust inhibition of late stomatal development. Conclusions: Because MKK structure is conserved across species, the identification of new MKK specificity modules and signaling rules furthers our understanding of how eukaryotes create specificity in complex biological systems.
publishDate 2018
dc.date.none.fl_str_mv 2018-04
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/79851
Wengier, Diego Leonardo; Lampard, Gregory R.; Bergmann, Dominique C.; Dissection of MAPK signaling specificity through protein engineering in a developmental context; BioMed Central; BMC Plant Biology; 18; 1; 4-2018; 1-17
1471-2229
CONICET Digital
CONICET
url http://hdl.handle.net/11336/79851
identifier_str_mv Wengier, Diego Leonardo; Lampard, Gregory R.; Bergmann, Dominique C.; Dissection of MAPK signaling specificity through protein engineering in a developmental context; BioMed Central; BMC Plant Biology; 18; 1; 4-2018; 1-17
1471-2229
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1186/s12870-018-1274-9
info:eu-repo/semantics/altIdentifier/url/https://bmcplantbiol.biomedcentral.com/articles/10.1186/s12870-018-1274-9
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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