Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB

Detalhes bibliográficos
Autor(a) principal: Baatsen, Jeroen
Data de Publicação: 2024
Tipo de documento: Tese
Idioma: eng
Título da fonte: Biblioteca Digital de Teses e Dissertações da USP
Texto Completo: https://www.teses.usp.br/teses/disponiveis/11/11137/tde-06062024-083116/
Resumo: Benzoxazinoids (BXs) form a group of secondary metabolites produced by many plants of the grass family (Poaceae). Release and activation of BXs upon pathogen attack strongly suppresses disease of pest species and foraging of herbivorous insects in areal parts of the plant. At the same time, BXs are constitutively produced and set free in the rhizosphere predominantly during early plant development, where they affect microbial interaction. Hydroxamic acid BX derivatives such as 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA), 2,4- dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and 2-hydroxy-4,7-dimethoxy-1,4- benzoxazin-3-one (HDMBOA) in general are more reactive but have a shorter half-life than the lactam derivatives 2-benzoxazolinone (BOA) and 6-methoxy-2-benzoxazolinone (MBOA). Regardless, MBOA is more efficient at suppressing several fungal pathogens and influences microbial rhizospheric interactions over generations of plants. Key to understanding plant-microbe symbiosis is knowledge about the means of chemical communication between symbionts, and the physiological changes those signaling molecules evoke on each symbiont. Therefore, we aimed to study the mechanisms by which an interspecies exchange of information precedes the initiation of symbiosis establishment. In order to gain more insight into these processes, we investigated how MBOA mediate root colonization by the plant growth promoting bacteria (PGPB) Azospirillum brasilense Ab-V5, Bacillus thuringiensis RZ2MS9, Pantoea agglomerans 33.1 and Pseudomonas protegens Pf-5, and the adverse effect on several fungal species of the pathogenic Fusarium. We found that bacterial response to exogenic MBOA was specific for each PGPB and dose dependent. Curiously, Fusarium strains isolated from non-BX-producing hosts were susceptible to MBOA at low doses, while maize isolated Fusarium (from a BX-producing host) was tolerant. Root colonization patterns by Ab-V5 and Pf-5 were studied in more detail, showing preference for crevices and root hairs as primary colonization sites. MBOA did not influence Pf-5 biofilm formation on Arabidopsis roots but Ab-V5 biofilm was improved. Finally, results from in vitro experiments were cross validated by transcriptomic assays on Ab-V5 where a chemotaxis regulatory protein showed a relative upregulation in 0.05 mM MBOA treatment and we could correlated the amount of differential expressed genes related to biofilm production with MBOA concentration. The Pf-5 transcriptome however, was little affected, which was consistent with previously obtained results. We conclude that MBOA in intermediate concentrations stimulates the motile form Ab-V5, while high concentrations of MBOA evoke a metabolic switch in preparation of root colonization.
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spelling Benzoxazinoids influence rhizosphere establishment and root colonization by PGPBOs benzoxazinóides influenciam o estabelecimento na rizosfera e a colonização radicular pelo BPCPFusariumFusariumBenzoxazinoidesBenzoxazinoidsBiofilmBiofilmeBPCPChemotaxisColonização radicularPGPBQuimoitaxiaRoot colonizationTransciptomaTransciptomeBenzoxazinoids (BXs) form a group of secondary metabolites produced by many plants of the grass family (Poaceae). Release and activation of BXs upon pathogen attack strongly suppresses disease of pest species and foraging of herbivorous insects in areal parts of the plant. At the same time, BXs are constitutively produced and set free in the rhizosphere predominantly during early plant development, where they affect microbial interaction. Hydroxamic acid BX derivatives such as 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA), 2,4- dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and 2-hydroxy-4,7-dimethoxy-1,4- benzoxazin-3-one (HDMBOA) in general are more reactive but have a shorter half-life than the lactam derivatives 2-benzoxazolinone (BOA) and 6-methoxy-2-benzoxazolinone (MBOA). Regardless, MBOA is more efficient at suppressing several fungal pathogens and influences microbial rhizospheric interactions over generations of plants. Key to understanding plant-microbe symbiosis is knowledge about the means of chemical communication between symbionts, and the physiological changes those signaling molecules evoke on each symbiont. Therefore, we aimed to study the mechanisms by which an interspecies exchange of information precedes the initiation of symbiosis establishment. In order to gain more insight into these processes, we investigated how MBOA mediate root colonization by the plant growth promoting bacteria (PGPB) Azospirillum brasilense Ab-V5, Bacillus thuringiensis RZ2MS9, Pantoea agglomerans 33.1 and Pseudomonas protegens Pf-5, and the adverse effect on several fungal species of the pathogenic Fusarium. We found that bacterial response to exogenic MBOA was specific for each PGPB and dose dependent. Curiously, Fusarium strains isolated from non-BX-producing hosts were susceptible to MBOA at low doses, while maize isolated Fusarium (from a BX-producing host) was tolerant. Root colonization patterns by Ab-V5 and Pf-5 were studied in more detail, showing preference for crevices and root hairs as primary colonization sites. MBOA did not influence Pf-5 biofilm formation on Arabidopsis roots but Ab-V5 biofilm was improved. Finally, results from in vitro experiments were cross validated by transcriptomic assays on Ab-V5 where a chemotaxis regulatory protein showed a relative upregulation in 0.05 mM MBOA treatment and we could correlated the amount of differential expressed genes related to biofilm production with MBOA concentration. The Pf-5 transcriptome however, was little affected, which was consistent with previously obtained results. We conclude that MBOA in intermediate concentrations stimulates the motile form Ab-V5, while high concentrations of MBOA evoke a metabolic switch in preparation of root colonization.Benzoxazinoides (BXs) formam um grupo de metabólitos secundários produzidos por muitas plantas da família das gramíneas (Poaceae). A liberação e ativação dos BXs durante o ataque de patógenos suprimem fortemente doenças de espécies de pragas e a forragem de insetos herbívoros em partes aéreas da planta. Ao mesmo tempo, os BXs são produzidos constitutivamente e liberados na rizosfera predominantemente durante o desenvolvimento inicial da planta, onde eles afetam a diversidade microbiana. Os derivados de ácido hidroxâmico dos BXs, como 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA), 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) e 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3- one (HDMBOA), em geral, são mais reativos, mas têm meia-vida mais curta do que os derivados de lactama 2-benzoxazolinone (BOA) e 6-methoxy-2-benzoxazolinone (MBOA). Independentemente, o MBOA é mais eficiente na supressão de vários patógenos fúngicos e influência a interação da rizosfera com microrganismos ao longo das gerações de plantas. A chave para entender a simbiose planta-microrganismo é o conhecimento sobre os meios de comunicação química entre os simbiontes e as mudanças fisiológicas que essas moléculas sinalizadoras provocam em cada simbionte. Portanto, nosso objetivo foi estudar os mecanismos pelos quais uma troca interespecífica de informações precede o estabelecimento da simbiose. Para obter mais informações sobre esses processos, investigamos como o MBOA medeia a colonização das raízes pelas bactérias promotoras do crescimento das plantas (BPCP) Azospirillum brasilense Ab-V5, Bacillus thuringiensis RZ2MS9, Pantoea agglomerans 33.1 e Pseudomonas protegens Pf-5, e o efeito adverso em várias espécies fúngicas do gênero Fusarium. A resposta bacteriana ao MBOA exógeno é específica para cada BPCP e dependente da dose. Curiosamente, linhagens de Fusarium isoladas de hospedeiros que não produzem BX foram suscetíveis ao MBOA em baixas doses, enquanto Fusarium isolado do milho (hospedeiro produtor de BX) é tolerante. Padrões de colonização radicular por Ab-V5 e Pf-5 foram estudados mais detalhadamente, revelando uma preferência por fendas e pelos pelos radiculares como locais primários de colonização. MBOA não influenciou a formação de biofilme por Pf-5 nas raízes de Arabidopsis, mas o biofilme de Ab-V5 foi aprimorado. Por fim, os resultados de experimentos in vitro foram validados cruzadamente por ensaios transcriptômicos em Ab-V5, nos quais uma proteína reguladora de quimiotaxia mostrou uma upregulação relativa no tratamento com 0,05 mM de MBOA, e pudemos correlacionar a quantidade de genes diferencialmente expressos relacionados à produção de biofilme com a concentração de MBOA. O transcriptoma de Pf-5, no entanto, foi pouco afetado, o que foi consistente com resultados previamente obtidos. Concluímos que MBOA em concentrações intermediárias estimula a forma móvel de Ab-V5, enquanto concentrações elevadas de MBOA provocam uma mudança metabólica em preparação para a colonização radicular.Biblioteca Digitais de Teses e Dissertações da USPVerdi, Maria Carolina QuecineBaatsen, Jeroen2024-03-26info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/doctoralThesisapplication/pdfhttps://www.teses.usp.br/teses/disponiveis/11/11137/tde-06062024-083116/reponame:Biblioteca Digital de Teses e Dissertações da USPinstname:Universidade de São Paulo (USP)instacron:USPLiberar o conteúdo para acesso público.info:eu-repo/semantics/openAccesseng2024-06-06T19:03:02Zoai:teses.usp.br:tde-06062024-083116Biblioteca Digital de Teses e Dissertaçõeshttp://www.teses.usp.br/PUBhttp://www.teses.usp.br/cgi-bin/mtd2br.plvirginia@if.usp.br|| atendimento@aguia.usp.br||virginia@if.usp.bropendoar:27212024-06-06T19:03:02Biblioteca Digital de Teses e Dissertações da USP - Universidade de São Paulo (USP)false
dc.title.none.fl_str_mv Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB
Os benzoxazinóides influenciam o estabelecimento na rizosfera e a colonização radicular pelo BPCP
title Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB
spellingShingle Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB
Baatsen, Jeroen
Fusarium
Fusarium
Benzoxazinoides
Benzoxazinoids
Biofilm
Biofilme
BPCP
Chemotaxis
Colonização radicular
PGPB
Quimoitaxia
Root colonization
Transciptoma
Transciptome
title_short Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB
title_full Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB
title_fullStr Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB
title_full_unstemmed Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB
title_sort Benzoxazinoids influence rhizosphere establishment and root colonization by PGPB
author Baatsen, Jeroen
author_facet Baatsen, Jeroen
author_role author
dc.contributor.none.fl_str_mv Verdi, Maria Carolina Quecine
dc.contributor.author.fl_str_mv Baatsen, Jeroen
dc.subject.por.fl_str_mv Fusarium
Fusarium
Benzoxazinoides
Benzoxazinoids
Biofilm
Biofilme
BPCP
Chemotaxis
Colonização radicular
PGPB
Quimoitaxia
Root colonization
Transciptoma
Transciptome
topic Fusarium
Fusarium
Benzoxazinoides
Benzoxazinoids
Biofilm
Biofilme
BPCP
Chemotaxis
Colonização radicular
PGPB
Quimoitaxia
Root colonization
Transciptoma
Transciptome
description Benzoxazinoids (BXs) form a group of secondary metabolites produced by many plants of the grass family (Poaceae). Release and activation of BXs upon pathogen attack strongly suppresses disease of pest species and foraging of herbivorous insects in areal parts of the plant. At the same time, BXs are constitutively produced and set free in the rhizosphere predominantly during early plant development, where they affect microbial interaction. Hydroxamic acid BX derivatives such as 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA), 2,4- dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and 2-hydroxy-4,7-dimethoxy-1,4- benzoxazin-3-one (HDMBOA) in general are more reactive but have a shorter half-life than the lactam derivatives 2-benzoxazolinone (BOA) and 6-methoxy-2-benzoxazolinone (MBOA). Regardless, MBOA is more efficient at suppressing several fungal pathogens and influences microbial rhizospheric interactions over generations of plants. Key to understanding plant-microbe symbiosis is knowledge about the means of chemical communication between symbionts, and the physiological changes those signaling molecules evoke on each symbiont. Therefore, we aimed to study the mechanisms by which an interspecies exchange of information precedes the initiation of symbiosis establishment. In order to gain more insight into these processes, we investigated how MBOA mediate root colonization by the plant growth promoting bacteria (PGPB) Azospirillum brasilense Ab-V5, Bacillus thuringiensis RZ2MS9, Pantoea agglomerans 33.1 and Pseudomonas protegens Pf-5, and the adverse effect on several fungal species of the pathogenic Fusarium. We found that bacterial response to exogenic MBOA was specific for each PGPB and dose dependent. Curiously, Fusarium strains isolated from non-BX-producing hosts were susceptible to MBOA at low doses, while maize isolated Fusarium (from a BX-producing host) was tolerant. Root colonization patterns by Ab-V5 and Pf-5 were studied in more detail, showing preference for crevices and root hairs as primary colonization sites. MBOA did not influence Pf-5 biofilm formation on Arabidopsis roots but Ab-V5 biofilm was improved. Finally, results from in vitro experiments were cross validated by transcriptomic assays on Ab-V5 where a chemotaxis regulatory protein showed a relative upregulation in 0.05 mM MBOA treatment and we could correlated the amount of differential expressed genes related to biofilm production with MBOA concentration. The Pf-5 transcriptome however, was little affected, which was consistent with previously obtained results. We conclude that MBOA in intermediate concentrations stimulates the motile form Ab-V5, while high concentrations of MBOA evoke a metabolic switch in preparation of root colonization.
publishDate 2024
dc.date.none.fl_str_mv 2024-03-26
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/doctoralThesis
format doctoralThesis
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dc.identifier.uri.fl_str_mv https://www.teses.usp.br/teses/disponiveis/11/11137/tde-06062024-083116/
url https://www.teses.usp.br/teses/disponiveis/11/11137/tde-06062024-083116/
dc.language.iso.fl_str_mv eng
language eng
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dc.rights.driver.fl_str_mv Liberar o conteúdo para acesso público.
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Liberar o conteúdo para acesso público.
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
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dc.publisher.none.fl_str_mv Biblioteca Digitais de Teses e Dissertações da USP
publisher.none.fl_str_mv Biblioteca Digitais de Teses e Dissertações da USP
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reponame:Biblioteca Digital de Teses e Dissertações da USP
instname:Universidade de São Paulo (USP)
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instname_str Universidade de São Paulo (USP)
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reponame_str Biblioteca Digital de Teses e Dissertações da USP
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repository.name.fl_str_mv Biblioteca Digital de Teses e Dissertações da USP - Universidade de São Paulo (USP)
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