Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens

Autores
Saavedra Borelli, Laura Lucía; Catarino, Rita; Heinz, Tobias; Heilmann, Ingo; Bezanilla, Magdalena; Malho, Rui
Año de publicación
2015
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Phosphatase and tensin homolog deleted on chromosome 10 (PTEN) is a lipid phosphatase implicated in cellular proliferation and survival. In animal cells, loss of PTEN leads to increased levels of phosphatidylinositol (3,4,5)-trisphosphate, stimulation of glucose and lipid metabolism, cellular growth, and morphological changes (related to adaptation and survival). Intriguingly, in plants, phosphatidylinositol (3,4,5)-trisphosphate has not been detected, and the enzymes that synthesize it were never reported. In this study we performed a genetic, biochemical, and functional characterization of the moss Physcomitrella patens PTEN gene family. P. patens has four PTENs,which areubiquitously expressed during the entire moss life cycle. Using a knock-in approach, we show that all four genes are expressed in growing tissues, namely caulonemal and rhizoid cells. At the subcellular level, PpPTEN-green fluorescent protein fusions localized to the cytosol and the nucleus. Analysis of single and double knockouts revealed no significant phenotypes at different developmental stages, indicative of functional redundancy. However, compared with wild-type triple and quadruple pten knockouts, caulonemal cells grew faster, switched from the juvenile protonemal stage to adult gametophores earlier, and produced more rhizoids. Furthermore, analysis of lipid content and quantitative real-time polymerase chain reaction data performed in quadruple mutants revealed altered phosphoinositide levels [increase in phosphatidylinositol (3,5)-bisphosphate and decrease in phosphatidylinositol 3-phosphate] and up-regulation of marker genes from the synthesis phase of the cell cycle (e.g. P. patens proliferating cell nuclear antigen, ribonucleotide reductase,andminichromosome maintenance) and of the retinoblastoma-related protein gene P. patens retinoblastoma-related protein1. Together, these results suggest that PpPTEN is a suppressor of cell growth and morphogenic development in plants.
Fil: Saavedra Borelli, Laura Lucía. Universidade de Lisboa; Portugal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas, Físicas y Naturales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Catarino, Rita. Universidade de Lisboa; Portugal
Fil: Heinz, Tobias. Martin Luther University Halle Wittenberg; Alemania
Fil: Heilmann, Ingo. Martin Luther University Halle Wittenberg; Alemania
Fil: Bezanilla, Magdalena. University of Massachusetts; Estados Unidos
Fil: Malho, Rui. Universidade de Lisboa; Portugal
Materia
Pten
Physcomitrella Patens
Phosphoinositides
Cell Cycle
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:11336/69873
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/69873
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patensSaavedra Borelli, Laura LucíaCatarino, RitaHeinz, TobiasHeilmann, IngoBezanilla, MagdalenaMalho, RuiPtenPhyscomitrella PatensPhosphoinositidesCell Cyclehttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Phosphatase and tensin homolog deleted on chromosome 10 (PTEN) is a lipid phosphatase implicated in cellular proliferation and survival. In animal cells, loss of PTEN leads to increased levels of phosphatidylinositol (3,4,5)-trisphosphate, stimulation of glucose and lipid metabolism, cellular growth, and morphological changes (related to adaptation and survival). Intriguingly, in plants, phosphatidylinositol (3,4,5)-trisphosphate has not been detected, and the enzymes that synthesize it were never reported. In this study we performed a genetic, biochemical, and functional characterization of the moss Physcomitrella patens PTEN gene family. P. patens has four PTENs,which areubiquitously expressed during the entire moss life cycle. Using a knock-in approach, we show that all four genes are expressed in growing tissues, namely caulonemal and rhizoid cells. At the subcellular level, PpPTEN-green fluorescent protein fusions localized to the cytosol and the nucleus. Analysis of single and double knockouts revealed no significant phenotypes at different developmental stages, indicative of functional redundancy. However, compared with wild-type triple and quadruple pten knockouts, caulonemal cells grew faster, switched from the juvenile protonemal stage to adult gametophores earlier, and produced more rhizoids. Furthermore, analysis of lipid content and quantitative real-time polymerase chain reaction data performed in quadruple mutants revealed altered phosphoinositide levels [increase in phosphatidylinositol (3,5)-bisphosphate and decrease in phosphatidylinositol 3-phosphate] and up-regulation of marker genes from the synthesis phase of the cell cycle (e.g. P. patens proliferating cell nuclear antigen, ribonucleotide reductase,andminichromosome maintenance) and of the retinoblastoma-related protein gene P. patens retinoblastoma-related protein1. Together, these results suggest that PpPTEN is a suppressor of cell growth and morphogenic development in plants.Fil: Saavedra Borelli, Laura Lucía. Universidade de Lisboa; Portugal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas, Físicas y Naturales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Catarino, Rita. Universidade de Lisboa; PortugalFil: Heinz, Tobias. Martin Luther University Halle Wittenberg; AlemaniaFil: Heilmann, Ingo. Martin Luther University Halle Wittenberg; AlemaniaFil: Bezanilla, Magdalena. University of Massachusetts; Estados UnidosFil: Malho, Rui. Universidade de Lisboa; PortugalAmerican Society of Plant Biologist2015-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/69873Saavedra Borelli, Laura Lucía; Catarino, Rita; Heinz, Tobias; Heilmann, Ingo; Bezanilla, Magdalena; et al.; Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens; American Society of Plant Biologist; Plant Physiology; 169; 4; 12-2015; 2572-25860032-0889CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1104/pp.15.01197info:eu-repo/semantics/altIdentifier/url/http://www.plantphysiol.org/content/169/4/2572info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:14:15Zoai:ri.conicet.gov.ar:11336/69873instacron: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 10:14:15.759CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens
title Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens
spellingShingle Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens
Saavedra Borelli, Laura Lucía
Pten
Physcomitrella Patens
Phosphoinositides
Cell Cycle
title_short Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens
title_full Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens
title_fullStr Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens
title_full_unstemmed Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens
title_sort Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens
dc.creator.none.fl_str_mv Saavedra Borelli, Laura Lucía
Catarino, Rita
Heinz, Tobias
Heilmann, Ingo
Bezanilla, Magdalena
Malho, Rui
author Saavedra Borelli, Laura Lucía
author_facet Saavedra Borelli, Laura Lucía
Catarino, Rita
Heinz, Tobias
Heilmann, Ingo
Bezanilla, Magdalena
Malho, Rui
author_role author
author2 Catarino, Rita
Heinz, Tobias
Heilmann, Ingo
Bezanilla, Magdalena
Malho, Rui
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv Pten
Physcomitrella Patens
Phosphoinositides
Cell Cycle
topic Pten
Physcomitrella Patens
Phosphoinositides
Cell Cycle
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Phosphatase and tensin homolog deleted on chromosome 10 (PTEN) is a lipid phosphatase implicated in cellular proliferation and survival. In animal cells, loss of PTEN leads to increased levels of phosphatidylinositol (3,4,5)-trisphosphate, stimulation of glucose and lipid metabolism, cellular growth, and morphological changes (related to adaptation and survival). Intriguingly, in plants, phosphatidylinositol (3,4,5)-trisphosphate has not been detected, and the enzymes that synthesize it were never reported. In this study we performed a genetic, biochemical, and functional characterization of the moss Physcomitrella patens PTEN gene family. P. patens has four PTENs,which areubiquitously expressed during the entire moss life cycle. Using a knock-in approach, we show that all four genes are expressed in growing tissues, namely caulonemal and rhizoid cells. At the subcellular level, PpPTEN-green fluorescent protein fusions localized to the cytosol and the nucleus. Analysis of single and double knockouts revealed no significant phenotypes at different developmental stages, indicative of functional redundancy. However, compared with wild-type triple and quadruple pten knockouts, caulonemal cells grew faster, switched from the juvenile protonemal stage to adult gametophores earlier, and produced more rhizoids. Furthermore, analysis of lipid content and quantitative real-time polymerase chain reaction data performed in quadruple mutants revealed altered phosphoinositide levels [increase in phosphatidylinositol (3,5)-bisphosphate and decrease in phosphatidylinositol 3-phosphate] and up-regulation of marker genes from the synthesis phase of the cell cycle (e.g. P. patens proliferating cell nuclear antigen, ribonucleotide reductase,andminichromosome maintenance) and of the retinoblastoma-related protein gene P. patens retinoblastoma-related protein1. Together, these results suggest that PpPTEN is a suppressor of cell growth and morphogenic development in plants.
Fil: Saavedra Borelli, Laura Lucía. Universidade de Lisboa; Portugal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas, Físicas y Naturales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Catarino, Rita. Universidade de Lisboa; Portugal
Fil: Heinz, Tobias. Martin Luther University Halle Wittenberg; Alemania
Fil: Heilmann, Ingo. Martin Luther University Halle Wittenberg; Alemania
Fil: Bezanilla, Magdalena. University of Massachusetts; Estados Unidos
Fil: Malho, Rui. Universidade de Lisboa; Portugal
description Phosphatase and tensin homolog deleted on chromosome 10 (PTEN) is a lipid phosphatase implicated in cellular proliferation and survival. In animal cells, loss of PTEN leads to increased levels of phosphatidylinositol (3,4,5)-trisphosphate, stimulation of glucose and lipid metabolism, cellular growth, and morphological changes (related to adaptation and survival). Intriguingly, in plants, phosphatidylinositol (3,4,5)-trisphosphate has not been detected, and the enzymes that synthesize it were never reported. In this study we performed a genetic, biochemical, and functional characterization of the moss Physcomitrella patens PTEN gene family. P. patens has four PTENs,which areubiquitously expressed during the entire moss life cycle. Using a knock-in approach, we show that all four genes are expressed in growing tissues, namely caulonemal and rhizoid cells. At the subcellular level, PpPTEN-green fluorescent protein fusions localized to the cytosol and the nucleus. Analysis of single and double knockouts revealed no significant phenotypes at different developmental stages, indicative of functional redundancy. However, compared with wild-type triple and quadruple pten knockouts, caulonemal cells grew faster, switched from the juvenile protonemal stage to adult gametophores earlier, and produced more rhizoids. Furthermore, analysis of lipid content and quantitative real-time polymerase chain reaction data performed in quadruple mutants revealed altered phosphoinositide levels [increase in phosphatidylinositol (3,5)-bisphosphate and decrease in phosphatidylinositol 3-phosphate] and up-regulation of marker genes from the synthesis phase of the cell cycle (e.g. P. patens proliferating cell nuclear antigen, ribonucleotide reductase,andminichromosome maintenance) and of the retinoblastoma-related protein gene P. patens retinoblastoma-related protein1. Together, these results suggest that PpPTEN is a suppressor of cell growth and morphogenic development in plants.
publishDate 2015
dc.date.none.fl_str_mv 2015-12
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/11336/69873
Saavedra Borelli, Laura Lucía; Catarino, Rita; Heinz, Tobias; Heilmann, Ingo; Bezanilla, Magdalena; et al.; Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens; American Society of Plant Biologist; Plant Physiology; 169; 4; 12-2015; 2572-2586
0032-0889
CONICET Digital
CONICET
url http://hdl.handle.net/11336/69873
identifier_str_mv Saavedra Borelli, Laura Lucía; Catarino, Rita; Heinz, Tobias; Heilmann, Ingo; Bezanilla, Magdalena; et al.; Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens; American Society of Plant Biologist; Plant Physiology; 169; 4; 12-2015; 2572-2586
0032-0889
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1104/pp.15.01197
info:eu-repo/semantics/altIdentifier/url/http://www.plantphysiol.org/content/169/4/2572
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
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 13.070432

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