Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation

Pollen development is a crucial biological process indispensable for seed set in flowering plants and for successful crop breeding. However, little is known about the molecular mechanisms regulating pollen development in crop species. This study reports a novel male-sterile tomato mutant, pollen def...

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Autores: Micol-Ponce, R., García-Alcázar, Manuel, Lebrón, Ricardo, Capel, Carmen, Pineda, Benito, García-Sogo, Begoña, Alché Ramírez, Juan de Dios, Ortíz-Atienza, Ana, Bretones, Sandra, Yuste-Lisbona, Fernando J., Moreno, Vicente, Capel, Juan, Lozano, Rafael
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/342544
Acceso en línea:http://hdl.handle.net/10261/342544
Access Level:acceso abierto
Palabra clave:Male sterility
Mapping-by-sequencing
Mcrogametogenesis
Microsporogenesis
Parthenocarpic fruits
Pollen formation
Receptor kinases
RNA interference
Tapetum development
Tomato
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spelling Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formationMicol-Ponce, R.García-Alcázar, ManuelLebrón, RicardoCapel, CarmenPineda, BenitoGarcía-Sogo, BegoñaAlché Ramírez, Juan de DiosOrtíz-Atienza, AnaBretones, SandraYuste-Lisbona, Fernando J.Moreno, VicenteCapel, JuanLozano, RafaelMale sterilityMapping-by-sequencingMcrogametogenesisMicrosporogenesisParthenocarpic fruitsPollen formationReceptor kinasesRNA interferenceTapetum developmentTomatoPollen development is a crucial biological process indispensable for seed set in flowering plants and for successful crop breeding. However, little is known about the molecular mechanisms regulating pollen development in crop species. This study reports a novel male-sterile tomato mutant, pollen deficient 2 (pod2), characterized by the production of non-viable pollen grains and resulting in the development of small parthenocarpic fruits. A combined strategy of mapping-by-sequencing and RNA interference-mediated gene silencing was used to prove that the pod2 phenotype is caused by the loss of Solanum lycopersicum G-Type lectin receptor kinase II.9 (SlG-LecRK-II.9) activity. In situ hybridization of floral buds showed that POD2/SlG-LecRK-II.9 is specifically expressed in tapetal cells and microspores at the late tetrad stage. Accordingly, abnormalities in meiosis and tapetum programmed cell death in pod2 occurred during microsporogenesis, resulting in the formation of four dysfunctional microspores leading to an aberrant microgametogenesis process. RNA-seq analyses supported the existence of alterations at the final stage of microsporogenesis, since we found tomato deregulated genes whose counterparts in Arabidopsis are essential for the normal progression of male meiosis and cytokinesis. Collectively, our results revealed the essential role of POD2/SlG-LecRK-II.9 in regulating tomato pollen development.This work was supported by research grants PID2019-110833RB-C31, PID2019-110833RB-C32, and PID2020-113324GB-100 funded by the Spanish Ministry of Science and Innovation (MCIN/AEI/10.13039/501100011033), and the Research and Innovation Programme of the European Union Horizon 2020 (BRESOV Project, ID 774244). A PhD fellowship to MGA was funded by the FPU Programme of the Spanish Ministry of Education and Culture (ref. AP2010-4528). RLe was supported by a Junta de Andalucía and FEDER research contract (DOC_01129).Oxford University PressEuropean CommissionMinisterio de Ciencia e Innovación (España)Junta de AndalucíaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2024202420232024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/342544reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110833RB-C31info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110833RB-C32info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-113324GB-I00info:eu-repo/grantAgreement/EC/H2020/774244http://dx.doi.org/10.1093/jxb/erac419Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3425442026-05-22T06:33:51Z
dc.title.none.fl_str_mv Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation
title Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation
spellingShingle Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation
Micol-Ponce, R.
Male sterility
Mapping-by-sequencing
Mcrogametogenesis
Microsporogenesis
Parthenocarpic fruits
Pollen formation
Receptor kinases
RNA interference
Tapetum development
Tomato
title_short Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation
title_full Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation
title_fullStr Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation
title_full_unstemmed Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation
title_sort Tomato POLLEN DEFICIENT 2 encodes a G-Type lectin receptor kinase required for viable pollen grain formation
dc.creator.none.fl_str_mv Micol-Ponce, R.
García-Alcázar, Manuel
Lebrón, Ricardo
Capel, Carmen
Pineda, Benito
García-Sogo, Begoña
Alché Ramírez, Juan de Dios
Ortíz-Atienza, Ana
Bretones, Sandra
Yuste-Lisbona, Fernando J.
Moreno, Vicente
Capel, Juan
Lozano, Rafael
author Micol-Ponce, R.
author_facet Micol-Ponce, R.
García-Alcázar, Manuel
Lebrón, Ricardo
Capel, Carmen
Pineda, Benito
García-Sogo, Begoña
Alché Ramírez, Juan de Dios
Ortíz-Atienza, Ana
Bretones, Sandra
Yuste-Lisbona, Fernando J.
Moreno, Vicente
Capel, Juan
Lozano, Rafael
author_role author
author2 García-Alcázar, Manuel
Lebrón, Ricardo
Capel, Carmen
Pineda, Benito
García-Sogo, Begoña
Alché Ramírez, Juan de Dios
Ortíz-Atienza, Ana
Bretones, Sandra
Yuste-Lisbona, Fernando J.
Moreno, Vicente
Capel, Juan
Lozano, Rafael
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv European Commission
Ministerio de Ciencia e Innovación (España)
Junta de Andalucía
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Male sterility
Mapping-by-sequencing
Mcrogametogenesis
Microsporogenesis
Parthenocarpic fruits
Pollen formation
Receptor kinases
RNA interference
Tapetum development
Tomato
topic Male sterility
Mapping-by-sequencing
Mcrogametogenesis
Microsporogenesis
Parthenocarpic fruits
Pollen formation
Receptor kinases
RNA interference
Tapetum development
Tomato
description Pollen development is a crucial biological process indispensable for seed set in flowering plants and for successful crop breeding. However, little is known about the molecular mechanisms regulating pollen development in crop species. This study reports a novel male-sterile tomato mutant, pollen deficient 2 (pod2), characterized by the production of non-viable pollen grains and resulting in the development of small parthenocarpic fruits. A combined strategy of mapping-by-sequencing and RNA interference-mediated gene silencing was used to prove that the pod2 phenotype is caused by the loss of Solanum lycopersicum G-Type lectin receptor kinase II.9 (SlG-LecRK-II.9) activity. In situ hybridization of floral buds showed that POD2/SlG-LecRK-II.9 is specifically expressed in tapetal cells and microspores at the late tetrad stage. Accordingly, abnormalities in meiosis and tapetum programmed cell death in pod2 occurred during microsporogenesis, resulting in the formation of four dysfunctional microspores leading to an aberrant microgametogenesis process. RNA-seq analyses supported the existence of alterations at the final stage of microsporogenesis, since we found tomato deregulated genes whose counterparts in Arabidopsis are essential for the normal progression of male meiosis and cytokinesis. Collectively, our results revealed the essential role of POD2/SlG-LecRK-II.9 in regulating tomato pollen development.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/342544
url http://hdl.handle.net/10261/342544
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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#PLACEHOLDER_PARENT_METADATA_VALUE#
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110833RB-C31
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110833RB-C32
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-113324GB-I00
info:eu-repo/grantAgreement/EC/H2020/774244
http://dx.doi.org/10.1093/jxb/erac419
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
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