Transcriptome and Secretome Analyses of Endophyte <i>Methylobacterium mesophilicum</i> and Pathogen <i>Xylella fastidiosa</i> Interacting Show Nutrient Competition

<i>Xylella fastidiosa</i> is the causal agent of several plant diseases affecting fruit and nut crops. <i>Methylobacterium mesophilicum</i> strain SR1.6/6 was isolated from <i>Citrus sinensis</i> and shown to promote plant growth by producing phytohormones, provid...

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Main Authors: Manuella Nobrega Dourado, Paulo Marques Pierry, Oseias Rodrigues Feitosa-Junior, Guillermo Uceda-Campos, Deibs Barbosa, Paulo A. Zaini, Abhaya M. Dandekar, Aline Maria da Silva, Welington Luiz Araújo
Format: Article
Language:English
Published: MDPI AG 2023-11-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/11/11/2755
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author Manuella Nobrega Dourado
Paulo Marques Pierry
Oseias Rodrigues Feitosa-Junior
Guillermo Uceda-Campos
Deibs Barbosa
Paulo A. Zaini
Abhaya M. Dandekar
Aline Maria da Silva
Welington Luiz Araújo
author_facet Manuella Nobrega Dourado
Paulo Marques Pierry
Oseias Rodrigues Feitosa-Junior
Guillermo Uceda-Campos
Deibs Barbosa
Paulo A. Zaini
Abhaya M. Dandekar
Aline Maria da Silva
Welington Luiz Araújo
author_sort Manuella Nobrega Dourado
collection DOAJ
description <i>Xylella fastidiosa</i> is the causal agent of several plant diseases affecting fruit and nut crops. <i>Methylobacterium mesophilicum</i> strain SR1.6/6 was isolated from <i>Citrus sinensis</i> and shown to promote plant growth by producing phytohormones, providing nutrients, inhibiting <i>X. fastidiosa</i>, and preventing Citrus Variegated Chlorosis. However, the molecular mechanisms involved in the interaction among these microbes are still unclear. The present work aimed to analyze physiological and molecular aspects of <i>M. mesophilicum</i> SR1.6/6 and <i>X. fastidiosa</i> 9a5c in co-culture. The transcriptome and secretome analyses indicated that <i>X. fastidiosa</i> down-regulates cell division and transport genes and up-regulates stress via induction of chaperones and pathogenicity-related genes including, the lipase-esterase LesA, a protease, as well as an oligopeptidase in response to <i>M. mesophilicum</i> competition. On the other hand, <i>M. mesophilicum</i> also down-regulated transport genes, except for iron uptake, which was up-regulated. Secretome analysis identified four proteins in <i>M. mesophilicum</i> exclusively produced in co-culture with <i>X. fastidiosa</i>, among these, three are related to phosphorous uptake. These results suggest that <i>M. mesophilicum</i> inhibits <i>X. fastidiosa</i> growth mainly due to nutrient competition for iron and phosphorous, thus promoting <i>X. fastidiosa</i> starvation, besides producing enzymes that degrade <i>X. fastidiosa</i> cell wall, mainly hydrolases. The understanding of these interactions provides a direction for control and management of the phytopathogen <i>X. fastidiosa</i>, and consequently, helps to improve citrus growth and productivity.
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spelling doaj.art-d8f83a1b447d422b8e410ae38fffe9222023-11-24T14:57:09ZengMDPI AGMicroorganisms2076-26072023-11-011111275510.3390/microorganisms11112755Transcriptome and Secretome Analyses of Endophyte <i>Methylobacterium mesophilicum</i> and Pathogen <i>Xylella fastidiosa</i> Interacting Show Nutrient CompetitionManuella Nobrega Dourado0Paulo Marques Pierry1Oseias Rodrigues Feitosa-Junior2Guillermo Uceda-Campos3Deibs Barbosa4Paulo A. Zaini5Abhaya M. Dandekar6Aline Maria da Silva7Welington Luiz Araújo8Microbiology Department, Biomedical Sciences Institute, University of Sao Paulo, Sao Paulo 05508-000, BrazilBiochemistry Department, Chemistry Institute, University of Sao Paulo, Sao Paulo 05508-000, BrazilBiochemistry Department, Chemistry Institute, University of Sao Paulo, Sao Paulo 05508-000, BrazilBiochemistry Department, Chemistry Institute, University of Sao Paulo, Sao Paulo 05508-000, BrazilBiochemistry Department, Chemistry Institute, University of Sao Paulo, Sao Paulo 05508-000, BrazilDepartment of Plant Sciences, College of Agricultural and Environmental Sciences, University of California, Davis, CA 95616, USADepartment of Plant Sciences, College of Agricultural and Environmental Sciences, University of California, Davis, CA 95616, USABiochemistry Department, Chemistry Institute, University of Sao Paulo, Sao Paulo 05508-000, BrazilMicrobiology Department, Biomedical Sciences Institute, University of Sao Paulo, Sao Paulo 05508-000, Brazil<i>Xylella fastidiosa</i> is the causal agent of several plant diseases affecting fruit and nut crops. <i>Methylobacterium mesophilicum</i> strain SR1.6/6 was isolated from <i>Citrus sinensis</i> and shown to promote plant growth by producing phytohormones, providing nutrients, inhibiting <i>X. fastidiosa</i>, and preventing Citrus Variegated Chlorosis. However, the molecular mechanisms involved in the interaction among these microbes are still unclear. The present work aimed to analyze physiological and molecular aspects of <i>M. mesophilicum</i> SR1.6/6 and <i>X. fastidiosa</i> 9a5c in co-culture. The transcriptome and secretome analyses indicated that <i>X. fastidiosa</i> down-regulates cell division and transport genes and up-regulates stress via induction of chaperones and pathogenicity-related genes including, the lipase-esterase LesA, a protease, as well as an oligopeptidase in response to <i>M. mesophilicum</i> competition. On the other hand, <i>M. mesophilicum</i> also down-regulated transport genes, except for iron uptake, which was up-regulated. Secretome analysis identified four proteins in <i>M. mesophilicum</i> exclusively produced in co-culture with <i>X. fastidiosa</i>, among these, three are related to phosphorous uptake. These results suggest that <i>M. mesophilicum</i> inhibits <i>X. fastidiosa</i> growth mainly due to nutrient competition for iron and phosphorous, thus promoting <i>X. fastidiosa</i> starvation, besides producing enzymes that degrade <i>X. fastidiosa</i> cell wall, mainly hydrolases. The understanding of these interactions provides a direction for control and management of the phytopathogen <i>X. fastidiosa</i>, and consequently, helps to improve citrus growth and productivity.https://www.mdpi.com/2076-2607/11/11/2755endophytic bacteriacitrusphytopathogen–endophyte interactiontranscriptomesecretome
spellingShingle Manuella Nobrega Dourado
Paulo Marques Pierry
Oseias Rodrigues Feitosa-Junior
Guillermo Uceda-Campos
Deibs Barbosa
Paulo A. Zaini
Abhaya M. Dandekar
Aline Maria da Silva
Welington Luiz Araújo
Transcriptome and Secretome Analyses of Endophyte <i>Methylobacterium mesophilicum</i> and Pathogen <i>Xylella fastidiosa</i> Interacting Show Nutrient Competition
Microorganisms
endophytic bacteria
citrus
phytopathogen–endophyte interaction
transcriptome
secretome
title Transcriptome and Secretome Analyses of Endophyte <i>Methylobacterium mesophilicum</i> and Pathogen <i>Xylella fastidiosa</i> Interacting Show Nutrient Competition
title_full Transcriptome and Secretome Analyses of Endophyte <i>Methylobacterium mesophilicum</i> and Pathogen <i>Xylella fastidiosa</i> Interacting Show Nutrient Competition
title_fullStr Transcriptome and Secretome Analyses of Endophyte <i>Methylobacterium mesophilicum</i> and Pathogen <i>Xylella fastidiosa</i> Interacting Show Nutrient Competition
title_full_unstemmed Transcriptome and Secretome Analyses of Endophyte <i>Methylobacterium mesophilicum</i> and Pathogen <i>Xylella fastidiosa</i> Interacting Show Nutrient Competition
title_short Transcriptome and Secretome Analyses of Endophyte <i>Methylobacterium mesophilicum</i> and Pathogen <i>Xylella fastidiosa</i> Interacting Show Nutrient Competition
title_sort transcriptome and secretome analyses of endophyte i methylobacterium mesophilicum i and pathogen i xylella fastidiosa i interacting show nutrient competition
topic endophytic bacteria
citrus
phytopathogen–endophyte interaction
transcriptome
secretome
url https://www.mdpi.com/2076-2607/11/11/2755
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