Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode

Autores
Gui, Cai Ping; Dong, Xin; Liu, Hai Kuan; Huang, Wei Jie; Zhang, Dong; Wang, Shu Jie; Barberini, María Laura; Gao, Xiao Yan; Muschietti, Jorge Prometeo; McCormick, Sheila; Tang, Wei Hua
Año de publicación
2014
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The tubular growth of a pollen tube cell is crucial for the sexual reproduction of flowering plants. LePRK1 is a pollen-specific and plasma membrane–localized receptor-like kinase from tomato (Solanum lycopersicum). LePRK1 interacts with another receptor, LePRK2, and with KINASE PARTNER PROTEIN (KPP), a Rop guanine nucleotide exchange factor. Here, we show that pollen tubes overexpressing LePRK1 or a truncated LePRK1 lacking its extracellular domain (LePRK1ΔECD) have enlarged tips but also extend their leading edges by producing “blebs.” Coexpression of LePRK1 and tomato PLIM2a, an actin bundling protein that interacts with KPP in a Ca2+-responsive manner, suppressed these LePRK1 overexpression phenotypes, whereas pollen tubes coexpressing KPP, LePRK1, and PLIM2a resumed the blebbing growth mode. We conclude that overexpression of LePRK1 or LePRK1ΔECD rewires pollen tube growth to a blebbing mode, through KPP- and PLIM2a-mediated bundling of actin filaments from tip plasma membranes. Arabidopsis thaliana pollen tubes expressing LePRK1ΔECD also grew by blebbing. Our results exposed a hidden capability of the pollen tube cell: upon overexpression of a single membrane-localized molecule, LePRK1 or LePRK1ΔECD, it can switch to an alternative mechanism for extension of the leading edge that is analogous to the blebbing growth mode reported for Dictyostelium and for Drosophila melanogaster stem cells.
Fil: Gui, Cai Ping. Chinese Academy of Sciences; República de China
Fil: Dong, Xin. Chinese Academy of Sciences; República de China
Fil: Liu, Hai Kuan. Chinese Academy of Sciences; República de China
Fil: Huang, Wei Jie. Chinese Academy of Sciences; República de China
Fil: Zhang, Dong. Chinese Academy of Sciences; República de China
Fil: Wang, Shu Jie. Chinese Academy of Sciences; República de China
Fil: Barberini, María Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Gao, Xiao Yan. Chinese Academy of Sciences; República de China
Fil: Muschietti, Jorge Prometeo. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Biodiversidad y Biología Experimental; Argentina
Fil: McCormick, Sheila. University of California at Berkeley; Estados Unidos
Fil: Tang, Wei Hua. Chinese Academy of Sciences; República de China. University of California at Berkeley; Estados Unidos
Materia
TOMATO
POLLEN TUBE
RECEPTOR KINASE
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:11336/36139
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/36139
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing ModeGui, Cai PingDong, XinLiu, Hai KuanHuang, Wei JieZhang, DongWang, Shu JieBarberini, María LauraGao, Xiao YanMuschietti, Jorge PrometeoMcCormick, SheilaTang, Wei HuaTOMATOPOLLEN TUBERECEPTOR KINASEhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The tubular growth of a pollen tube cell is crucial for the sexual reproduction of flowering plants. LePRK1 is a pollen-specific and plasma membrane–localized receptor-like kinase from tomato (Solanum lycopersicum). LePRK1 interacts with another receptor, LePRK2, and with KINASE PARTNER PROTEIN (KPP), a Rop guanine nucleotide exchange factor. Here, we show that pollen tubes overexpressing LePRK1 or a truncated LePRK1 lacking its extracellular domain (LePRK1ΔECD) have enlarged tips but also extend their leading edges by producing “blebs.” Coexpression of LePRK1 and tomato PLIM2a, an actin bundling protein that interacts with KPP in a Ca2+-responsive manner, suppressed these LePRK1 overexpression phenotypes, whereas pollen tubes coexpressing KPP, LePRK1, and PLIM2a resumed the blebbing growth mode. We conclude that overexpression of LePRK1 or LePRK1ΔECD rewires pollen tube growth to a blebbing mode, through KPP- and PLIM2a-mediated bundling of actin filaments from tip plasma membranes. Arabidopsis thaliana pollen tubes expressing LePRK1ΔECD also grew by blebbing. Our results exposed a hidden capability of the pollen tube cell: upon overexpression of a single membrane-localized molecule, LePRK1 or LePRK1ΔECD, it can switch to an alternative mechanism for extension of the leading edge that is analogous to the blebbing growth mode reported for Dictyostelium and for Drosophila melanogaster stem cells.Fil: Gui, Cai Ping. Chinese Academy of Sciences; República de ChinaFil: Dong, Xin. Chinese Academy of Sciences; República de ChinaFil: Liu, Hai Kuan. Chinese Academy of Sciences; República de ChinaFil: Huang, Wei Jie. Chinese Academy of Sciences; República de ChinaFil: Zhang, Dong. Chinese Academy of Sciences; República de ChinaFil: Wang, Shu Jie. Chinese Academy of Sciences; República de ChinaFil: Barberini, María Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; ArgentinaFil: Gao, Xiao Yan. Chinese Academy of Sciences; República de ChinaFil: Muschietti, Jorge Prometeo. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Biodiversidad y Biología Experimental; ArgentinaFil: McCormick, Sheila. University of California at Berkeley; Estados UnidosFil: Tang, Wei Hua. Chinese Academy of Sciences; República de China. University of California at Berkeley; Estados UnidosAmerican Society of Plant Biologist2014-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/36139Gui, Cai Ping; Dong, Xin; Liu, Hai Kuan; Huang, Wei Jie; Zhang, Dong; et al.; Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode; American Society of Plant Biologist; Plant Cell; 26; 9; 9-2014; 3538-35551040-4651CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1105/tpc.114.127381info:eu-repo/semantics/altIdentifier/url/http://www.plantcell.org/content/26/9/3538info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:46:51Zoai:ri.conicet.gov.ar:11336/36139instacron: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:34982025-09-03 09:46:52.005CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode
title Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode
spellingShingle Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode
Gui, Cai Ping
TOMATO
POLLEN TUBE
RECEPTOR KINASE
title_short Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode
title_full Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode
title_fullStr Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode
title_full_unstemmed Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode
title_sort Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode
dc.creator.none.fl_str_mv Gui, Cai Ping
Dong, Xin
Liu, Hai Kuan
Huang, Wei Jie
Zhang, Dong
Wang, Shu Jie
Barberini, María Laura
Gao, Xiao Yan
Muschietti, Jorge Prometeo
McCormick, Sheila
Tang, Wei Hua
author Gui, Cai Ping
author_facet Gui, Cai Ping
Dong, Xin
Liu, Hai Kuan
Huang, Wei Jie
Zhang, Dong
Wang, Shu Jie
Barberini, María Laura
Gao, Xiao Yan
Muschietti, Jorge Prometeo
McCormick, Sheila
Tang, Wei Hua
author_role author
author2 Dong, Xin
Liu, Hai Kuan
Huang, Wei Jie
Zhang, Dong
Wang, Shu Jie
Barberini, María Laura
Gao, Xiao Yan
Muschietti, Jorge Prometeo
McCormick, Sheila
Tang, Wei Hua
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv TOMATO
POLLEN TUBE
RECEPTOR KINASE
topic TOMATO
POLLEN TUBE
RECEPTOR KINASE
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The tubular growth of a pollen tube cell is crucial for the sexual reproduction of flowering plants. LePRK1 is a pollen-specific and plasma membrane–localized receptor-like kinase from tomato (Solanum lycopersicum). LePRK1 interacts with another receptor, LePRK2, and with KINASE PARTNER PROTEIN (KPP), a Rop guanine nucleotide exchange factor. Here, we show that pollen tubes overexpressing LePRK1 or a truncated LePRK1 lacking its extracellular domain (LePRK1ΔECD) have enlarged tips but also extend their leading edges by producing “blebs.” Coexpression of LePRK1 and tomato PLIM2a, an actin bundling protein that interacts with KPP in a Ca2+-responsive manner, suppressed these LePRK1 overexpression phenotypes, whereas pollen tubes coexpressing KPP, LePRK1, and PLIM2a resumed the blebbing growth mode. We conclude that overexpression of LePRK1 or LePRK1ΔECD rewires pollen tube growth to a blebbing mode, through KPP- and PLIM2a-mediated bundling of actin filaments from tip plasma membranes. Arabidopsis thaliana pollen tubes expressing LePRK1ΔECD also grew by blebbing. Our results exposed a hidden capability of the pollen tube cell: upon overexpression of a single membrane-localized molecule, LePRK1 or LePRK1ΔECD, it can switch to an alternative mechanism for extension of the leading edge that is analogous to the blebbing growth mode reported for Dictyostelium and for Drosophila melanogaster stem cells.
Fil: Gui, Cai Ping. Chinese Academy of Sciences; República de China
Fil: Dong, Xin. Chinese Academy of Sciences; República de China
Fil: Liu, Hai Kuan. Chinese Academy of Sciences; República de China
Fil: Huang, Wei Jie. Chinese Academy of Sciences; República de China
Fil: Zhang, Dong. Chinese Academy of Sciences; República de China
Fil: Wang, Shu Jie. Chinese Academy of Sciences; República de China
Fil: Barberini, María Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina
Fil: Gao, Xiao Yan. Chinese Academy of Sciences; República de China
Fil: Muschietti, Jorge Prometeo. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular "Dr. Héctor N. Torres"; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Biodiversidad y Biología Experimental; Argentina
Fil: McCormick, Sheila. University of California at Berkeley; Estados Unidos
Fil: Tang, Wei Hua. Chinese Academy of Sciences; República de China. University of California at Berkeley; Estados Unidos
description The tubular growth of a pollen tube cell is crucial for the sexual reproduction of flowering plants. LePRK1 is a pollen-specific and plasma membrane–localized receptor-like kinase from tomato (Solanum lycopersicum). LePRK1 interacts with another receptor, LePRK2, and with KINASE PARTNER PROTEIN (KPP), a Rop guanine nucleotide exchange factor. Here, we show that pollen tubes overexpressing LePRK1 or a truncated LePRK1 lacking its extracellular domain (LePRK1ΔECD) have enlarged tips but also extend their leading edges by producing “blebs.” Coexpression of LePRK1 and tomato PLIM2a, an actin bundling protein that interacts with KPP in a Ca2+-responsive manner, suppressed these LePRK1 overexpression phenotypes, whereas pollen tubes coexpressing KPP, LePRK1, and PLIM2a resumed the blebbing growth mode. We conclude that overexpression of LePRK1 or LePRK1ΔECD rewires pollen tube growth to a blebbing mode, through KPP- and PLIM2a-mediated bundling of actin filaments from tip plasma membranes. Arabidopsis thaliana pollen tubes expressing LePRK1ΔECD also grew by blebbing. Our results exposed a hidden capability of the pollen tube cell: upon overexpression of a single membrane-localized molecule, LePRK1 or LePRK1ΔECD, it can switch to an alternative mechanism for extension of the leading edge that is analogous to the blebbing growth mode reported for Dictyostelium and for Drosophila melanogaster stem cells.
publishDate 2014
dc.date.none.fl_str_mv 2014-09
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/11336/36139
Gui, Cai Ping; Dong, Xin; Liu, Hai Kuan; Huang, Wei Jie; Zhang, Dong; et al.; Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode; American Society of Plant Biologist; Plant Cell; 26; 9; 9-2014; 3538-3555
1040-4651
CONICET Digital
CONICET
url http://hdl.handle.net/11336/36139
identifier_str_mv Gui, Cai Ping; Dong, Xin; Liu, Hai Kuan; Huang, Wei Jie; Zhang, Dong; et al.; Overexpression of the Tomato Pollen Receptor Kinase LePRK1 Rewires Pollen Tube Growth to a Blebbing Mode; American Society of Plant Biologist; Plant Cell; 26; 9; 9-2014; 3538-3555
1040-4651
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1105/tpc.114.127381
info:eu-repo/semantics/altIdentifier/url/http://www.plantcell.org/content/26/9/3538
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 American Society of Plant Biologist
publisher.none.fl_str_mv American Society of Plant Biologist
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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score 13.13397

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