Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) Nirenberg infection

IntroductionThe fungal pathogen Fusarium verticillioides (Sacc.) Nirenberg (Fv) causes considerable agricultural and economic losses and is harmful to animal and human health. Fv can infect maize throughout its long agricultural cycle, and root infection drastically affects maize growth and yield.Me...

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Main Authors: Francisco Roberto Quiroz-Figueroa, Abraham Cruz-Mendívil, Enrique Ibarra-Laclette, Luz María García-Pérez, Rosa Luz Gómez-Peraza, Greta Hanako-Rosas, Eliel Ruíz-May, Apolinar Santamaría-Miranda, Rupesh Kumar Singh, Gerardo Campos-Rivero, Elpidio García-Ramírez, José Alberto Narváez-Zapata
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1195794/full
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author Francisco Roberto Quiroz-Figueroa
Abraham Cruz-Mendívil
Enrique Ibarra-Laclette
Luz María García-Pérez
Rosa Luz Gómez-Peraza
Greta Hanako-Rosas
Eliel Ruíz-May
Apolinar Santamaría-Miranda
Rupesh Kumar Singh
Gerardo Campos-Rivero
Elpidio García-Ramírez
José Alberto Narváez-Zapata
author_facet Francisco Roberto Quiroz-Figueroa
Abraham Cruz-Mendívil
Enrique Ibarra-Laclette
Luz María García-Pérez
Rosa Luz Gómez-Peraza
Greta Hanako-Rosas
Eliel Ruíz-May
Apolinar Santamaría-Miranda
Rupesh Kumar Singh
Gerardo Campos-Rivero
Elpidio García-Ramírez
José Alberto Narváez-Zapata
author_sort Francisco Roberto Quiroz-Figueroa
collection DOAJ
description IntroductionThe fungal pathogen Fusarium verticillioides (Sacc.) Nirenberg (Fv) causes considerable agricultural and economic losses and is harmful to animal and human health. Fv can infect maize throughout its long agricultural cycle, and root infection drastically affects maize growth and yield.MethodsThe root cell wall is the first physical and defensive barrier against soilborne pathogens such as Fv. This study compares two contrasting genotypes of maize (Zea mays L.) roots that are resistant (RES) or susceptible (SUS) to Fv infection by using transcriptomics, fluorescence, scanning electron microscopy analyses, and ddPCR.ResultsSeeds were infected with a highly virulent local Fv isolate. Although Fv infected both the RES and SUS genotypes, infection occurred faster in SUS, notably showing a difference of three to four days. In addition, root infections in RES were less severe in comparison to SUS infections. Comparative transcriptomics (rate +Fv/control) were performed seven days after inoculation (DAI). The analysis of differentially expressed genes (DEGs) in each rate revealed 733 and 559 unique transcripts that were significantly (P ≤0.05) up and downregulated in RES (+Fv/C) and SUS (+Fv/C), respectively. KEGG pathway enrichment analysis identified coumarin and furanocoumarin biosynthesis, phenylpropanoid biosynthesis, and plant-pathogen interaction pathways as being highly enriched with specific genes involved in cell wall modifications in the RES genotype, whereas the SUS genotype mainly displayed a repressed plant–pathogen interaction pathway and did not show any enriched cell wall genes. In particular, cell wall-related gene expression showed a higher level in RES than in SUS under Fv infection. Analysis of DEG abundance made it possible to identify transcripts involved in response to abiotic and biotic stresses, biosynthetic and catabolic processes, pectin biosynthesis, phenylpropanoid metabolism, and cell wall biosynthesis and organization. Root histological analysis in RES showed an increase in lignified cells in the sclerenchymatous hypodermis zone during Fv infection.DiscussionThese differences in the cell wall and lignification could be related to an enhanced degradation of the root hairs and the epidermis cell wall in SUS, as was visualized by SEM. These findings reveal that components of the root cell wall are important against Fv infection and possibly other soilborne phytopathogens.
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spelling doaj.art-c6563ab9ccbc478fa0cc3818845d7b2a2023-06-27T10:36:40ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-06-011410.3389/fpls.2023.11957941195794Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) Nirenberg infectionFrancisco Roberto Quiroz-Figueroa0Abraham Cruz-Mendívil1Enrique Ibarra-Laclette2Luz María García-Pérez3Rosa Luz Gómez-Peraza4Greta Hanako-Rosas5Eliel Ruíz-May6Apolinar Santamaría-Miranda7Rupesh Kumar Singh8Gerardo Campos-Rivero9Elpidio García-Ramírez10José Alberto Narváez-Zapata11Instituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR)—Unidad Sinaloa, Guasave, MexicoConsejo Nacional de Ciencia y Tecnología (CONACYT)-Instituto Politécnico Nacional, (CIIDIR) Unidad Sinaloa, Guasave, MexicoRed de Estudios Moleculares Avanzados, Instituto de Ecología A. C., Cluster BioMimic®, Xalapa, MexicoInstituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR)—Unidad Sinaloa, Guasave, MexicoInstituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR)—Unidad Sinaloa, Guasave, MexicoRed de Estudios Moleculares Avanzados, Instituto de Ecología A. C., Cluster BioMimic®, Xalapa, MexicoRed de Estudios Moleculares Avanzados, Instituto de Ecología A. C., Cluster BioMimic®, Xalapa, MexicoInstituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR)—Unidad Sinaloa, Guasave, MexicoCentre of Molecular and Environmental Biology, Department of Biology, University of Minho, Braga, PortugalInstituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR)—Unidad Sinaloa, Guasave, MexicoFacultad de Química, Departamento de Bioquímica, Universidad Nacional Autónoma de México, Ciudad de México, MexicoInstituto Politécnico Nacional, Centro de Biotecnología Genómica, Reynosa, MexicoIntroductionThe fungal pathogen Fusarium verticillioides (Sacc.) Nirenberg (Fv) causes considerable agricultural and economic losses and is harmful to animal and human health. Fv can infect maize throughout its long agricultural cycle, and root infection drastically affects maize growth and yield.MethodsThe root cell wall is the first physical and defensive barrier against soilborne pathogens such as Fv. This study compares two contrasting genotypes of maize (Zea mays L.) roots that are resistant (RES) or susceptible (SUS) to Fv infection by using transcriptomics, fluorescence, scanning electron microscopy analyses, and ddPCR.ResultsSeeds were infected with a highly virulent local Fv isolate. Although Fv infected both the RES and SUS genotypes, infection occurred faster in SUS, notably showing a difference of three to four days. In addition, root infections in RES were less severe in comparison to SUS infections. Comparative transcriptomics (rate +Fv/control) were performed seven days after inoculation (DAI). The analysis of differentially expressed genes (DEGs) in each rate revealed 733 and 559 unique transcripts that were significantly (P ≤0.05) up and downregulated in RES (+Fv/C) and SUS (+Fv/C), respectively. KEGG pathway enrichment analysis identified coumarin and furanocoumarin biosynthesis, phenylpropanoid biosynthesis, and plant-pathogen interaction pathways as being highly enriched with specific genes involved in cell wall modifications in the RES genotype, whereas the SUS genotype mainly displayed a repressed plant–pathogen interaction pathway and did not show any enriched cell wall genes. In particular, cell wall-related gene expression showed a higher level in RES than in SUS under Fv infection. Analysis of DEG abundance made it possible to identify transcripts involved in response to abiotic and biotic stresses, biosynthetic and catabolic processes, pectin biosynthesis, phenylpropanoid metabolism, and cell wall biosynthesis and organization. Root histological analysis in RES showed an increase in lignified cells in the sclerenchymatous hypodermis zone during Fv infection.DiscussionThese differences in the cell wall and lignification could be related to an enhanced degradation of the root hairs and the epidermis cell wall in SUS, as was visualized by SEM. These findings reveal that components of the root cell wall are important against Fv infection and possibly other soilborne phytopathogens.https://www.frontiersin.org/articles/10.3389/fpls.2023.1195794/fulltranscriptomicfusariosishistologySEMligninddPCR
spellingShingle Francisco Roberto Quiroz-Figueroa
Abraham Cruz-Mendívil
Enrique Ibarra-Laclette
Luz María García-Pérez
Rosa Luz Gómez-Peraza
Greta Hanako-Rosas
Eliel Ruíz-May
Apolinar Santamaría-Miranda
Rupesh Kumar Singh
Gerardo Campos-Rivero
Elpidio García-Ramírez
José Alberto Narváez-Zapata
Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) Nirenberg infection
Frontiers in Plant Science
transcriptomic
fusariosis
histology
SEM
lignin
ddPCR
title Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) Nirenberg infection
title_full Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) Nirenberg infection
title_fullStr Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) Nirenberg infection
title_full_unstemmed Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) Nirenberg infection
title_short Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) Nirenberg infection
title_sort cell wall related genes and lignin accumulation contribute to the root resistance in different maize zea mays l genotypes to fusarium verticillioides sacc nirenberg infection
topic transcriptomic
fusariosis
histology
SEM
lignin
ddPCR
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1195794/full
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