The Differential Growth Inhibition of Phytophthora spp. Caused by the Rare Sugar Tagatose Is Associated With Species-Specific Metabolic and Transcriptional Changes
Tagatose is a rare sugar with no negative impacts on human health and selective inhibitory effects on plant-associated microorganisms. Tagatose inhibited mycelial growth and negatively affected mitochondrial processes in Phytophthora infestans , but not in Phytophthora cinnamomi . The aim of this st...
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Published in | Frontiers in microbiology Vol. 12; p. 711545 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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07.07.2021
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Abstract | Tagatose is a rare sugar with no negative impacts on human health and selective inhibitory effects on plant-associated microorganisms. Tagatose inhibited mycelial growth and negatively affected mitochondrial processes in
Phytophthora infestans
, but not in
Phytophthora cinnamomi
. The aim of this study was to elucidate metabolic changes and transcriptional reprogramming activated by
P. infestans
and
P. cinnamomi
in response to tagatose, in order to clarify the differential inhibitory mechanisms of tagatose and the species-specific reactions to this rare sugar.
Phytophthora infestans
and
P. cinnamomi
activated distinct metabolic and transcriptional changes in response to the rare sugar. Tagatose negatively affected mycelial growth, sugar content and amino acid content in
P. infestans
with a severe transcriptional reprogramming that included the downregulation of genes involved in transport, sugar metabolism, signal transduction, and growth-related process. Conversely, tagatose incubation upregulated genes related to transport, energy metabolism, sugar metabolism and oxidative stress in
P. cinnamomi
with no negative effects on mycelial growth, sugar content and amino acid content. Differential inhibitory effects of tagatose on
Phytophthora
spp. were associated with an attempted reaction of
P. infestans
, which was not sufficient to attenuate the negative impacts of the rare sugar and with an efficient response of
P. cinnamomi
with the reprogramming of multiple metabolic processes, such as genes related to glucose transport, pentose metabolism, tricarboxylic acid cycle, reactive oxygen species detoxification, mitochondrial and alternative respiration processes. Knowledge on the differential response of
Phytophthora
spp. to tagatose represent a step forward in the understanding functional roles of rare sugars. |
---|---|
AbstractList | Tagatose is a rare sugar with no negative impacts on human health and selective inhibitory effects on plant-associated microorganisms. Tagatose inhibited mycelial growth and negatively affected mitochondrial processes in Phytophthora infestans , but not in Phytophthora cinnamomi . The aim of this study was to elucidate metabolic changes and transcriptional reprogramming activated by P. infestans and P. cinnamomi in response to tagatose, in order to clarify the differential inhibitory mechanisms of tagatose and the species-specific reactions to this rare sugar. Phytophthora infestans and P. cinnamomi activated distinct metabolic and transcriptional changes in response to the rare sugar. Tagatose negatively affected mycelial growth, sugar content and amino acid content in P. infestans with a severe transcriptional reprogramming that included the downregulation of genes involved in transport, sugar metabolism, signal transduction, and growth-related process. Conversely, tagatose incubation upregulated genes related to transport, energy metabolism, sugar metabolism and oxidative stress in P. cinnamomi with no negative effects on mycelial growth, sugar content and amino acid content. Differential inhibitory effects of tagatose on Phytophthora spp. were associated with an attempted reaction of P. infestans , which was not sufficient to attenuate the negative impacts of the rare sugar and with an efficient response of P. cinnamomi with the reprogramming of multiple metabolic processes, such as genes related to glucose transport, pentose metabolism, tricarboxylic acid cycle, reactive oxygen species detoxification, mitochondrial and alternative respiration processes. Knowledge on the differential response of Phytophthora spp. to tagatose represent a step forward in the understanding functional roles of rare sugars. Tagatose is a rare sugar with no negative impacts on human health and selective inhibitory effects on plant-associated microorganisms. Tagatose inhibited mycelial growth and negatively affected mitochondrial processes in Phytophthora infestans , but not in Phytophthora cinnamomi . The aim of this study was to elucidate metabolic changes and transcriptional reprogramming activated by P. infestans and P. cinnamomi in response to tagatose, in order to clarify the differential inhibitory mechanisms of tagatose and the species-specific reactions to this rare sugar. Phytophthora infestans and P. cinnamomi activated distinct metabolic and transcriptional changes in response to the rare sugar. Tagatose negatively affected mycelial growth, sugar content and amino acid content in P. infestans with a severe transcriptional reprogramming that included the downregulation of genes involved in transport, sugar metabolism, signal transduction, and growth-related process. Conversely, tagatose incubation upregulated genes related to transport, energy metabolism, sugar metabolism and oxidative stress in P. cinnamomi with no negative effects on mycelial growth, sugar content and amino acid content. Differential inhibitory effects of tagatose on Phytophthora spp. were associated with an attempted reaction of P. infestans , which was not sufficient to attenuate the negative impacts of the rare sugar and with an efficient response of P. cinnamomi with the reprogramming of multiple metabolic processes, such as genes related to glucose transport, pentose metabolism, tricarboxylic acid cycle, reactive oxygen species detoxification, mitochondrial and alternative respiration processes. Knowledge on the differential response of Phytophthora spp. to tagatose represent a step forward in the understanding functional roles of rare sugars. |
Author | Corneo, Paola Elisa Moretto, Marco Lazazzara, Valentina Perazzolli, Michele Puopolo, Gerardo Barka, Essaid Ait Pertot, Ilaria Nesler, Andrea Chahed, Abdessalem |
AuthorAffiliation | 2 Bi-PA nv , Londerzeel , Belgium 1 Research and Innovation Centre, Fondazione Edmund Mach , San Michele all’Adige , Italy 3 Department of Induced Resistance and Plant Bioprotection, University of Reims , Reims , France 4 Center Agriculture Food Environment (C3A), University of Trento , San Michele all’Adige , Italy |
AuthorAffiliation_xml | – name: 2 Bi-PA nv , Londerzeel , Belgium – name: 3 Department of Induced Resistance and Plant Bioprotection, University of Reims , Reims , France – name: 1 Research and Innovation Centre, Fondazione Edmund Mach , San Michele all’Adige , Italy – name: 4 Center Agriculture Food Environment (C3A), University of Trento , San Michele all’Adige , Italy |
Author_xml | – sequence: 1 givenname: Abdessalem surname: Chahed fullname: Chahed, Abdessalem – sequence: 2 givenname: Valentina surname: Lazazzara fullname: Lazazzara, Valentina – sequence: 3 givenname: Marco surname: Moretto fullname: Moretto, Marco – sequence: 4 givenname: Andrea surname: Nesler fullname: Nesler, Andrea – sequence: 5 givenname: Paola Elisa surname: Corneo fullname: Corneo, Paola Elisa – sequence: 6 givenname: Essaid Ait surname: Barka fullname: Barka, Essaid Ait – sequence: 7 givenname: Ilaria surname: Pertot fullname: Pertot, Ilaria – sequence: 8 givenname: Gerardo surname: Puopolo fullname: Puopolo, Gerardo – sequence: 9 givenname: Michele surname: Perazzolli fullname: Perazzolli, Michele |
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CitedBy_id | crossref_primary_10_1016_j_ijbiomac_2023_125148 crossref_primary_10_1155_2022_9814348 crossref_primary_10_3390_agronomy13092225 crossref_primary_10_3390_plants11030296 crossref_primary_10_3390_agronomy12020498 crossref_primary_10_3390_plants11202781 crossref_primary_10_3389_fcimb_2021_767944 crossref_primary_10_3390_plants11121611 crossref_primary_10_1111_ppa_13440 |
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ContentType | Journal Article |
Copyright | Attribution Copyright © 2021 Chahed, Lazazzara, Moretto, Nesler, Corneo, Barka, Pertot, Puopolo and Perazzolli. 2021 Chahed, Lazazzara, Moretto, Nesler, Corneo, Barka, Pertot, Puopolo and Perazzolli |
Copyright_xml | – notice: Attribution – notice: Copyright © 2021 Chahed, Lazazzara, Moretto, Nesler, Corneo, Barka, Pertot, Puopolo and Perazzolli. 2021 Chahed, Lazazzara, Moretto, Nesler, Corneo, Barka, Pertot, Puopolo and Perazzolli |
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Keywords | transcriptomics targeted metabolomics rare sugar gene expression level transcriptional reprogramming Phytophthora spp |
Language | English |
License | Attribution: http://creativecommons.org/licenses/by This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology Reviewed by: Maria Victoria Aguilar Pontes, Concordia University, Canada; Sergio Adrian Guerrero, National University of the Littoral, Argentina Edited by: Alberto A. Iglesias, CONICET Coastline Agrobiotechnology Institute (IAL), Argentina |
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SubjectTerms | Biochemistry, Molecular Biology gene expression level Genomics Life Sciences Microbiology Microbiology and Parasitology Phytopathology and phytopharmacy Phytophthora spp Protistology rare sugar targeted metabolomics transcriptional reprogramming transcriptomics Vegetal Biology |
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Title | The Differential Growth Inhibition of Phytophthora spp. Caused by the Rare Sugar Tagatose Is Associated With Species-Specific Metabolic and Transcriptional Changes |
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