Metschnikowia pulcherrima as an efficient biocontrol agent of Botrytis cinerea infection in apples: Unraveling protection mechanisms through yeast proteomics

[Display omitted] •Metschnikowia pulcherrima Mp-30 prevents Botrytis cinerea infection in apples.•Multiple yeast mechanisms are involved in the gray mold biocontrol ability.•There is a reprogramming of yeast metabolism involved in B. cinerea inactivation.•Membrane trafficking of yeast compounds is e...

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Published inBiological control Vol. 183; p. 105266
Main Authors Fernandez-San Millan, Alicia, Fernandez-Irigoyen, Joaquin, Santamaria, Enrique, Larraya, Luis, Farran, Inmaculada, Veramendi, Jon
Format Journal Article
LanguageEnglish
Published Elsevier Inc 01.08.2023
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Online AccessGet full text
ISSN1049-9644
DOI10.1016/j.biocontrol.2023.105266

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Abstract [Display omitted] •Metschnikowia pulcherrima Mp-30 prevents Botrytis cinerea infection in apples.•Multiple yeast mechanisms are involved in the gray mold biocontrol ability.•There is a reprogramming of yeast metabolism involved in B. cinerea inactivation.•Membrane trafficking of yeast compounds is enhanced in the fungal presence.•Yeast envelope composition has a major role in the antagonistic interaction. The results obtained in this study show that the Mp-30 strain of Metschnikowia pulcherrima is able to completely prevent Botrytis cinerea infection in apples, which is a major postharvest disease of fruits throughout the world. We have observed that although Mp-30 is able to rapidly colonize wounds, sequestrate iron and secrete antifungal compounds, other unknown mechanisms that occur in the early phase of the yeast-fungal interaction must be implicated in the biocontrol response. The main objective of this study was to identify the pathways involved in the mechanism of action of Mp-30 against B. cinerea in apples. Therefore, differentially accumulated yeast proteins in the presence/absence of B. cinerea on wounded apples were studied to elucidate Mp-30 biocontrol mechanisms and regulation at the protein level. A comparative proteomic analysis showed that 114 yeast proteins were increased and 61 were decreased. The Mp-30 antagonistic response mainly showed the increase of (1) gene expression and protein translation related proteins, (2) trafficking and vesicle-mediated transport related proteins, (3) pyruvate metabolism and mitochondrial proteins related to energy and amino acid production, (4) fatty acid synthesis, and (5) cell envelope related proteins. On the other hand, redox homeostasis, and amino acid and carbon metabolism were downregulated. Since there is no yeast growth enhancement associated with the presence of B. cinerea, such regulation mechanisms may be related to the reprogramming of metabolism, synthesis of new compounds and reorganization of yeast cell structure. Indeed, the results show that several pathways cooperate in restructuring the plasma membrane and cell wall composition, highlighting their major role in the antagonistic interactions for apple protection against gray mold proliferation. These results are of great interest since they provide a clear insight into the yeast mechanisms involved in B. cinerea inactivation during the first hours of contact in the wounded fruit. They shed light on the unknown yeast molecular biocontrol mechanisms.
AbstractList The results obtained in this study show that the Mp-30 strain of Metschnikowia pulcherrima is able to completely prevent Botrytis cinerea infection in apples, which is a major postharvest disease of fruits throughout the world. We have observed that although Mp-30 is able to rapidly colonize wounds, sequestrate iron and secrete antifungal compounds, other unknown mechanisms that occur in the early phase of the yeast-fungal interaction must be implicated in the biocontrol response. The main objective of this study was to identify the pathways involved in the mechanism of action of Mp-30 against B. cinerea in apples. Therefore, differentially accumulated yeast proteins in the presence/absence of B. cinerea on wounded apples were studied to elucidate Mp-30 biocontrol mechanisms and regulation at the protein level. A comparative proteomic analysis showed that 114 yeast proteins were increased and 61 were decreased. The Mp-30 antagonistic response mainly showed the increase of (1) gene expression and protein translation related proteins, (2) trafficking and vesicle-mediated transport related proteins, (3) pyruvate metabolism and mitochondrial proteins related to energy and amino acid production, (4) fatty acid synthesis, and (5) cell envelope related proteins. On the other hand, redox homeostasis, and amino acid and carbon metabolism were downregulated. Since there is no yeast growth enhancement associated with the presence of B. cinerea, such regulation mechanisms may be related to the reprogramming of metabolism, synthesis of new compounds and reorganization of yeast cell structure. Indeed, the results show that several pathways cooperate in restructuring the plasma membrane and cell wall composition, highlighting their major role in the antagonistic interactions for apple protection against gray mold proliferation. These results are of great interest since they provide a clear insight into the yeast mechanisms involved in B. cinerea inactivation during the first hours of contact in the wounded fruit. They shed light on the unknown yeast molecular biocontrol mechanisms.
[Display omitted] •Metschnikowia pulcherrima Mp-30 prevents Botrytis cinerea infection in apples.•Multiple yeast mechanisms are involved in the gray mold biocontrol ability.•There is a reprogramming of yeast metabolism involved in B. cinerea inactivation.•Membrane trafficking of yeast compounds is enhanced in the fungal presence.•Yeast envelope composition has a major role in the antagonistic interaction. The results obtained in this study show that the Mp-30 strain of Metschnikowia pulcherrima is able to completely prevent Botrytis cinerea infection in apples, which is a major postharvest disease of fruits throughout the world. We have observed that although Mp-30 is able to rapidly colonize wounds, sequestrate iron and secrete antifungal compounds, other unknown mechanisms that occur in the early phase of the yeast-fungal interaction must be implicated in the biocontrol response. The main objective of this study was to identify the pathways involved in the mechanism of action of Mp-30 against B. cinerea in apples. Therefore, differentially accumulated yeast proteins in the presence/absence of B. cinerea on wounded apples were studied to elucidate Mp-30 biocontrol mechanisms and regulation at the protein level. A comparative proteomic analysis showed that 114 yeast proteins were increased and 61 were decreased. The Mp-30 antagonistic response mainly showed the increase of (1) gene expression and protein translation related proteins, (2) trafficking and vesicle-mediated transport related proteins, (3) pyruvate metabolism and mitochondrial proteins related to energy and amino acid production, (4) fatty acid synthesis, and (5) cell envelope related proteins. On the other hand, redox homeostasis, and amino acid and carbon metabolism were downregulated. Since there is no yeast growth enhancement associated with the presence of B. cinerea, such regulation mechanisms may be related to the reprogramming of metabolism, synthesis of new compounds and reorganization of yeast cell structure. Indeed, the results show that several pathways cooperate in restructuring the plasma membrane and cell wall composition, highlighting their major role in the antagonistic interactions for apple protection against gray mold proliferation. These results are of great interest since they provide a clear insight into the yeast mechanisms involved in B. cinerea inactivation during the first hours of contact in the wounded fruit. They shed light on the unknown yeast molecular biocontrol mechanisms.
ArticleNumber 105266
Author Fernandez-Irigoyen, Joaquin
Farran, Inmaculada
Fernandez-San Millan, Alicia
Veramendi, Jon
Larraya, Luis
Santamaria, Enrique
Author_xml – sequence: 1
  givenname: Alicia
  surname: Fernandez-San Millan
  fullname: Fernandez-San Millan, Alicia
  email: alicia.fernandez@unavarra.es
  organization: Institute for Multidisciplinary Research in Applied Biology (IMAB), Universidad Pública de Navarra (UPNA), Campus Arrosadía, 31006 Pamplona, Spain
– sequence: 2
  givenname: Joaquin
  surname: Fernandez-Irigoyen
  fullname: Fernandez-Irigoyen, Joaquin
  email: jfernani@navarra.es
  organization: Proteored-ISCIII, Proteomics Unit, Navarrabiomed-Departamento de Salud-Universidad Pública de Navarra (UPNA), Campus de Ciencias de la Salud, Avda. de Barañain s/n, 31008 Pamplona, Spain
– sequence: 3
  givenname: Enrique
  surname: Santamaria
  fullname: Santamaria, Enrique
  email: enrique.santamaria.martinez@navarra.es
  organization: Proteored-ISCIII, Proteomics Unit, Navarrabiomed-Departamento de Salud-Universidad Pública de Navarra (UPNA), Campus de Ciencias de la Salud, Avda. de Barañain s/n, 31008 Pamplona, Spain
– sequence: 4
  givenname: Luis
  surname: Larraya
  fullname: Larraya, Luis
  email: luis.larraya@unavarra.es
  organization: Institute for Multidisciplinary Research in Applied Biology (IMAB), Universidad Pública de Navarra (UPNA), Campus Arrosadía, 31006 Pamplona, Spain
– sequence: 5
  givenname: Inmaculada
  surname: Farran
  fullname: Farran, Inmaculada
  email: farran@unavarra.es
  organization: Institute for Multidisciplinary Research in Applied Biology (IMAB), Universidad Pública de Navarra (UPNA), Campus Arrosadía, 31006 Pamplona, Spain
– sequence: 6
  givenname: Jon
  surname: Veramendi
  fullname: Veramendi, Jon
  email: jon@unavarra.es
  organization: Institute for Multidisciplinary Research in Applied Biology (IMAB), Universidad Pública de Navarra (UPNA), Campus Arrosadía, 31006 Pamplona, Spain
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Keywords Botrytis
Apple
Yeast
Metschnikowia
Proteomic
Biocontrol
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Snippet [Display omitted] •Metschnikowia pulcherrima Mp-30 prevents Botrytis cinerea infection in apples.•Multiple yeast mechanisms are involved in the gray mold...
The results obtained in this study show that the Mp-30 strain of Metschnikowia pulcherrima is able to completely prevent Botrytis cinerea infection in apples,...
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SubjectTerms amino acids
Apple
apples
Biocontrol
biological control
biological control agents
Botrytis
Botrytis cinerea
carbon metabolism
cell wall components
energy
fatty acids
fruits
gene expression
gray mold
homeostasis
mechanism of action
Metschnikowia
Metschnikowia pulcherrima
mitochondria
plasma membrane
postharvest diseases
protein content
Proteomic
proteomics
pyruvic acid
Yeast
yeasts
Title Metschnikowia pulcherrima as an efficient biocontrol agent of Botrytis cinerea infection in apples: Unraveling protection mechanisms through yeast proteomics
URI https://dx.doi.org/10.1016/j.biocontrol.2023.105266
https://www.proquest.com/docview/2834271274
Volume 183
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