Targeting of plasmodesmal proteins requires unconventional signals

Autores
Robles Luna, Gabriel; Li, Jiefu; Wang, Xu; Liao, Li; Jung-Youn Lee
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Effective cellular signaling relies on precise spatial localization and dynamic interactions among proteins in specific subcellular compartments or niches, such as cell-to-cell contact sites and junctions. In plants, endogenous and pathogenic proteins gained the ability to target plasmodesmata, membrane-lined cytoplasmic connections, through evolution to regulate or exploit cellular signaling across cell wall boundaries. For example, the receptor-like membrane protein PLASMODESMATA-LOCATED PROTEIN 5 (PDLP5), a potent regulator of plasmodesmal permeability, generates feed-forward or feed-back signals important for plant immunity and root development. However, the molecular features that determine the plasmodesmal association of PDLP5 or other proteins remain largely unknown, and no protein motifs have been identified as plasmodesmal targeting signals. Here, we developed an approach combining custom-built machine-learning algorithms and targeted mutagenesis to examine PDLP5 in Arabidopsis thaliana and Nicotiana benthamiana. We report that PDLP5 and its closely related proteins carry unconventional targeting signals consisting of short stretches of amino acids. PDLP5 contains two divergent, tandemly arranged signals, either of which is sufficient for localization and biological function in regulating viral movement through plasmodesmata. Notably, plasmodesmal targeting signals exhibit little sequence conservation but are located similarly proximal to the membrane. These features appear to be a common theme in plasmodesmal targeting.
Fil: Robles Luna, Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; Argentina
Fil: Li, Jiefu. University of Delaware; Estados Unidos
Fil: Wang, Xu. University of Delaware; Estados Unidos
Fil: Liao, Li. University of Delaware; Estados Unidos
Fil: Jung-Youn Lee. University of Delaware; Estados Unidos
Materia
Plasmodesmata
Targeting signal
virus movement
Machine learning
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:11336/250443

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spelling Targeting of plasmodesmal proteins requires unconventional signalsRobles Luna, GabrielLi, JiefuWang, XuLiao, LiJung-Youn LeePlasmodesmataTargeting signalvirus movementMachine learninghttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Effective cellular signaling relies on precise spatial localization and dynamic interactions among proteins in specific subcellular compartments or niches, such as cell-to-cell contact sites and junctions. In plants, endogenous and pathogenic proteins gained the ability to target plasmodesmata, membrane-lined cytoplasmic connections, through evolution to regulate or exploit cellular signaling across cell wall boundaries. For example, the receptor-like membrane protein PLASMODESMATA-LOCATED PROTEIN 5 (PDLP5), a potent regulator of plasmodesmal permeability, generates feed-forward or feed-back signals important for plant immunity and root development. However, the molecular features that determine the plasmodesmal association of PDLP5 or other proteins remain largely unknown, and no protein motifs have been identified as plasmodesmal targeting signals. Here, we developed an approach combining custom-built machine-learning algorithms and targeted mutagenesis to examine PDLP5 in Arabidopsis thaliana and Nicotiana benthamiana. We report that PDLP5 and its closely related proteins carry unconventional targeting signals consisting of short stretches of amino acids. PDLP5 contains two divergent, tandemly arranged signals, either of which is sufficient for localization and biological function in regulating viral movement through plasmodesmata. Notably, plasmodesmal targeting signals exhibit little sequence conservation but are located similarly proximal to the membrane. These features appear to be a common theme in plasmodesmal targeting.Fil: Robles Luna, Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; ArgentinaFil: Li, Jiefu. University of Delaware; Estados UnidosFil: Wang, Xu. University of Delaware; Estados UnidosFil: Liao, Li. University of Delaware; Estados UnidosFil: Jung-Youn Lee. University of Delaware; Estados UnidosAmerican Society of Plant Biologist2023-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/250443Robles Luna, Gabriel; Li, Jiefu; Wang, Xu; Liao, Li; Jung-Youn Lee; Targeting of plasmodesmal proteins requires unconventional signals; American Society of Plant Biologist; Plant Cell; 35; 8; 5-2023; 3035-30521040-4651CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/plcell/advance-article/doi/10.1093/plcell/koad152/7178006?utm_source=authortollfreelink&utm_campaign=plcell&utm_medium=email&guestAccessKey=5044d9bd-2522-4a48-a918-8d5c6141418binfo:eu-repo/semantics/altIdentifier/doi/10.1093/plcell/koad152info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:53:52Zoai:ri.conicet.gov.ar:11336/250443instacron: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 09:53:53.225CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Targeting of plasmodesmal proteins requires unconventional signals
title Targeting of plasmodesmal proteins requires unconventional signals
spellingShingle Targeting of plasmodesmal proteins requires unconventional signals
Robles Luna, Gabriel
Plasmodesmata
Targeting signal
virus movement
Machine learning
title_short Targeting of plasmodesmal proteins requires unconventional signals
title_full Targeting of plasmodesmal proteins requires unconventional signals
title_fullStr Targeting of plasmodesmal proteins requires unconventional signals
title_full_unstemmed Targeting of plasmodesmal proteins requires unconventional signals
title_sort Targeting of plasmodesmal proteins requires unconventional signals
dc.creator.none.fl_str_mv Robles Luna, Gabriel
Li, Jiefu
Wang, Xu
Liao, Li
Jung-Youn Lee
author Robles Luna, Gabriel
author_facet Robles Luna, Gabriel
Li, Jiefu
Wang, Xu
Liao, Li
Jung-Youn Lee
author_role author
author2 Li, Jiefu
Wang, Xu
Liao, Li
Jung-Youn Lee
author2_role author
author
author
author
dc.subject.none.fl_str_mv Plasmodesmata
Targeting signal
virus movement
Machine learning
topic Plasmodesmata
Targeting signal
virus movement
Machine learning
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Effective cellular signaling relies on precise spatial localization and dynamic interactions among proteins in specific subcellular compartments or niches, such as cell-to-cell contact sites and junctions. In plants, endogenous and pathogenic proteins gained the ability to target plasmodesmata, membrane-lined cytoplasmic connections, through evolution to regulate or exploit cellular signaling across cell wall boundaries. For example, the receptor-like membrane protein PLASMODESMATA-LOCATED PROTEIN 5 (PDLP5), a potent regulator of plasmodesmal permeability, generates feed-forward or feed-back signals important for plant immunity and root development. However, the molecular features that determine the plasmodesmal association of PDLP5 or other proteins remain largely unknown, and no protein motifs have been identified as plasmodesmal targeting signals. Here, we developed an approach combining custom-built machine-learning algorithms and targeted mutagenesis to examine PDLP5 in Arabidopsis thaliana and Nicotiana benthamiana. We report that PDLP5 and its closely related proteins carry unconventional targeting signals consisting of short stretches of amino acids. PDLP5 contains two divergent, tandemly arranged signals, either of which is sufficient for localization and biological function in regulating viral movement through plasmodesmata. Notably, plasmodesmal targeting signals exhibit little sequence conservation but are located similarly proximal to the membrane. These features appear to be a common theme in plasmodesmal targeting.
Fil: Robles Luna, Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Biotecnología y Biología Molecular. Universidad Nacional de La Plata. Facultad de Ciencias Exactas. Instituto de Biotecnología y Biología Molecular; Argentina
Fil: Li, Jiefu. University of Delaware; Estados Unidos
Fil: Wang, Xu. University of Delaware; Estados Unidos
Fil: Liao, Li. University of Delaware; Estados Unidos
Fil: Jung-Youn Lee. University of Delaware; Estados Unidos
description Effective cellular signaling relies on precise spatial localization and dynamic interactions among proteins in specific subcellular compartments or niches, such as cell-to-cell contact sites and junctions. In plants, endogenous and pathogenic proteins gained the ability to target plasmodesmata, membrane-lined cytoplasmic connections, through evolution to regulate or exploit cellular signaling across cell wall boundaries. For example, the receptor-like membrane protein PLASMODESMATA-LOCATED PROTEIN 5 (PDLP5), a potent regulator of plasmodesmal permeability, generates feed-forward or feed-back signals important for plant immunity and root development. However, the molecular features that determine the plasmodesmal association of PDLP5 or other proteins remain largely unknown, and no protein motifs have been identified as plasmodesmal targeting signals. Here, we developed an approach combining custom-built machine-learning algorithms and targeted mutagenesis to examine PDLP5 in Arabidopsis thaliana and Nicotiana benthamiana. We report that PDLP5 and its closely related proteins carry unconventional targeting signals consisting of short stretches of amino acids. PDLP5 contains two divergent, tandemly arranged signals, either of which is sufficient for localization and biological function in regulating viral movement through plasmodesmata. Notably, plasmodesmal targeting signals exhibit little sequence conservation but are located similarly proximal to the membrane. These features appear to be a common theme in plasmodesmal targeting.
publishDate 2023
dc.date.none.fl_str_mv 2023-05
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/11336/250443
Robles Luna, Gabriel; Li, Jiefu; Wang, Xu; Liao, Li; Jung-Youn Lee; Targeting of plasmodesmal proteins requires unconventional signals; American Society of Plant Biologist; Plant Cell; 35; 8; 5-2023; 3035-3052
1040-4651
CONICET Digital
CONICET
url http://hdl.handle.net/11336/250443
identifier_str_mv Robles Luna, Gabriel; Li, Jiefu; Wang, Xu; Liao, Li; Jung-Youn Lee; Targeting of plasmodesmal proteins requires unconventional signals; American Society of Plant Biologist; Plant Cell; 35; 8; 5-2023; 3035-3052
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/url/https://academic.oup.com/plcell/advance-article/doi/10.1093/plcell/koad152/7178006?utm_source=authortollfreelink&utm_campaign=plcell&utm_medium=email&guestAccessKey=5044d9bd-2522-4a48-a918-8d5c6141418b
info:eu-repo/semantics/altIdentifier/doi/10.1093/plcell/koad152
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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