Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses

Iron is an essential nutrient required for plant growth and development. The availability of iron might also influence disease resistance in plants. However, the molecular mechanisms involved in the plant response to iron availability and immunity have been investigated separately from each other. I...

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Autores: Sánchez-Sanuy, Ferran, Mateluna-Cuadra, Roberto, Tomita, Keisuke, Okada, Kazunori, Sacchi, Gian Attilio, Campo, Sonia, San Segundo, Blanca
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/296722
Acceso en línea:http://hdl.handle.net/10261/296722
Access Level:acceso abierto
Palabra clave:Blast
Ferroptosis
Immune response
Iron
Magnaporthe oryzae
Oryza sativa
Phytoalexins
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dc.title.none.fl_str_mv Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses
title Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses
spellingShingle Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses
Sánchez-Sanuy, Ferran
Blast
Ferroptosis
Immune response
Iron
Magnaporthe oryzae
Oryza sativa
Phytoalexins
title_short Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses
title_full Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses
title_fullStr Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses
title_full_unstemmed Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses
title_sort Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses
dc.creator.none.fl_str_mv Sánchez-Sanuy, Ferran
Mateluna-Cuadra, Roberto
Tomita, Keisuke
Okada, Kazunori
Sacchi, Gian Attilio
Campo, Sonia
San Segundo, Blanca
author Sánchez-Sanuy, Ferran
author_facet Sánchez-Sanuy, Ferran
Mateluna-Cuadra, Roberto
Tomita, Keisuke
Okada, Kazunori
Sacchi, Gian Attilio
Campo, Sonia
San Segundo, Blanca
author_role author
author2 Mateluna-Cuadra, Roberto
Tomita, Keisuke
Okada, Kazunori
Sacchi, Gian Attilio
Campo, Sonia
San Segundo, Blanca
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Conferencia de Rectores de las Universidades Españolas
Consejo Superior de Investigaciones Científicas (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
European Commission
Ministerio de Ciencia e Innovación (España)
Ministerio de Economía y Competitividad (España)
Generalitat de Catalunya
Ministerio de Ciencia, Tecnología, Conocimiento e Innovación (Chile)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Blast
Ferroptosis
Immune response
Iron
Magnaporthe oryzae
Oryza sativa
Phytoalexins
topic Blast
Ferroptosis
Immune response
Iron
Magnaporthe oryzae
Oryza sativa
Phytoalexins
description Iron is an essential nutrient required for plant growth and development. The availability of iron might also influence disease resistance in plants. However, the molecular mechanisms involved in the plant response to iron availability and immunity have been investigated separately from each other. In this work, we found that exposure of rice plants to high iron enhances resistance to infection by the fungal pathogen Magnaporthe oryzae, the causal agent of blast disease. RNA-Seq analysis revealed that blast resistance in iron-treated rice plants was associated with superinduction of defense-related genes during pathogen infection, including Pathogenesis-Related genes. The expression level of genes involved in the biosynthesis of phytoalexins, both diterpene phytoalexins and the flavonoid phytoalexin sakuranetin, was also higher in iron-treated plants compared with control plants, which correlated well with increased levels of phytoalexins in these plants during M. oryzae infection. Upon pathogen infection, lipid peroxidation was also higher in iron-treated plants compared with non-treated plants. We also show that M. oryzae infection modulates the expression of genes that play a pivotal role in the maintenance of iron homeostasis. Histochemical analysis of M. oryzae-infected leaves revealed colocalization of iron and reactive oxygen species in cells located in the vicinity of fungal penetration sites (e.g. appressoria) in rice plants that have been exposed to iron. Together these findings support that ferroptosis plays a role in the response of iron-treated rice plants to infection by virulent M. oryzae. Understanding interconnected regulations between iron signaling and immune signaling in rice holds great potential for developing novel strategies to improve blast resistance in rice.
publishDate 2022
dc.date.none.fl_str_mv 2022
2023
2023
2023
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/10261/296722
url http://hdl.handle.net/10261/296722
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-101275-B-I00
info:eu-repo/grantAgreement/AEI//PID2021-128825OB-I00
info:eu-repo/grantAgreement/MINECO//SEV-2015-0533
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Iron treatment induces resistance against the rice blast fungus Magnaporthe oryzae through potentiation of immune responses [Dataset]; Gene Expression Omnibus; GSE202997
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 1 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600705.v1
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 2 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600708.v1
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 3 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600711.v1
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 4 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600714.v1
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 5 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600717.v1
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 6 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600720.v1
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 7 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600723.v1
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 8 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600726.v1
Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 9 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600729.v1
http://dx.doi.org/10.1186/s12284-022-00609-w
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dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
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spelling Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune ResponsesSánchez-Sanuy, FerranMateluna-Cuadra, RobertoTomita, KeisukeOkada, KazunoriSacchi, Gian AttilioCampo, SoniaSan Segundo, BlancaBlastFerroptosisImmune responseIronMagnaporthe oryzaeOryza sativaPhytoalexinsIron is an essential nutrient required for plant growth and development. The availability of iron might also influence disease resistance in plants. However, the molecular mechanisms involved in the plant response to iron availability and immunity have been investigated separately from each other. In this work, we found that exposure of rice plants to high iron enhances resistance to infection by the fungal pathogen Magnaporthe oryzae, the causal agent of blast disease. RNA-Seq analysis revealed that blast resistance in iron-treated rice plants was associated with superinduction of defense-related genes during pathogen infection, including Pathogenesis-Related genes. The expression level of genes involved in the biosynthesis of phytoalexins, both diterpene phytoalexins and the flavonoid phytoalexin sakuranetin, was also higher in iron-treated plants compared with control plants, which correlated well with increased levels of phytoalexins in these plants during M. oryzae infection. Upon pathogen infection, lipid peroxidation was also higher in iron-treated plants compared with non-treated plants. We also show that M. oryzae infection modulates the expression of genes that play a pivotal role in the maintenance of iron homeostasis. Histochemical analysis of M. oryzae-infected leaves revealed colocalization of iron and reactive oxygen species in cells located in the vicinity of fungal penetration sites (e.g. appressoria) in rice plants that have been exposed to iron. Together these findings support that ferroptosis plays a role in the response of iron-treated rice plants to infection by virulent M. oryzae. Understanding interconnected regulations between iron signaling and immune signaling in rice holds great potential for developing novel strategies to improve blast resistance in rice.Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This research was supported by Projects RTI2018-101275-B-I00 and PID2021-128825OB-I00 funded by MCIN/AEI/and by “ERDF A way of making Europe” to BSS. We acknowledge financial support from the MCIN/AEI/10.13039/501100011033 through the “Severo Ochoa Programme for Centres of Excellence in R&D” (SEV-2015-0533 and CEX2019-000902-S) and the CERCA Programme/“Generalitat de Catalunya”. R. M-C is a recipient of a Ph.D. Grant from the “Ministerio de Ciencia, Tecnología, Conocimiento e Innovación del Gobierno de Chile (ref. 72210076).With funding from the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000902-S)SpringerConferencia de Rectores de las Universidades EspañolasConsejo Superior de Investigaciones Científicas (España)Ministerio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)European CommissionMinisterio de Ciencia e Innovación (España)Ministerio de Economía y Competitividad (España)Generalitat de CatalunyaMinisterio de Ciencia, Tecnología, Conocimiento e Innovación (Chile)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2023202320222023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/296722reponame: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#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-101275-B-I00info:eu-repo/grantAgreement/AEI//PID2021-128825OB-I00info:eu-repo/grantAgreement/MINECO//SEV-2015-0533Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Iron treatment induces resistance against the rice blast fungus Magnaporthe oryzae through potentiation of immune responses [Dataset]; Gene Expression Omnibus; GSE202997Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 1 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600705.v1Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 2 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600708.v1Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 3 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600711.v1Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 4 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600714.v1Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 5 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600717.v1Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 6 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600720.v1Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 7 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600723.v1Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 8 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600726.v1Sánchez-Sanuy, Ferran; Mateluna-Cuadra, Roberto; Tomita, Keisuke; Okada, Kazunori; Sacchi, Gian Attilio; Campo, Sonia; San Segundo, Blanca; 2023; Additional file 9 of Iron Induces Resistance Against the Rice Blast Fungus Magnaporthe oryzae Through Potentiation of Immune Responses [Dataset]; Figshare; Version 1; https://doi.org/10.6084/m9.figshare.22600729.v1http://dx.doi.org/10.1186/s12284-022-00609-wSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2967222026-05-22T06:33:51Z
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