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Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae

Oomycetes, of the genus Phytophthora, comprise of some of the most devastating plant pathogens. Parasitism of Phytophthora results from evolution from an autotrophic ancestor and adaptation to a wide range of environments, involving metabolic adaptation. Sequence mining showed that Phytophthora spp....

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Autores principales: Kuhn, Marie-Line, Berre, Jo-Yanne Le, Kebdani-Minet, Naima, Panabières, Franck
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8879444/
https://www.ncbi.nlm.nih.gov/pubmed/35208735
http://dx.doi.org/10.3390/microorganisms10020281
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author Kuhn, Marie-Line
Berre, Jo-Yanne Le
Kebdani-Minet, Naima
Panabières, Franck
author_facet Kuhn, Marie-Line
Berre, Jo-Yanne Le
Kebdani-Minet, Naima
Panabières, Franck
author_sort Kuhn, Marie-Line
collection PubMed
description Oomycetes, of the genus Phytophthora, comprise of some of the most devastating plant pathogens. Parasitism of Phytophthora results from evolution from an autotrophic ancestor and adaptation to a wide range of environments, involving metabolic adaptation. Sequence mining showed that Phytophthora spp. display an unusual repertoire of glycolytic enzymes, made of multigene families and enzyme replacements. To investigate the impact of these gene duplications on the biology of Phytophthora and, eventually, identify novel functions associated to gene expansion, we focused our study on the first glycolytic step on P. nicotianae, a broad host range pathogen. We reveal that this step is committed by a set of three glucokinase types that differ by their structure, enzymatic properties, and evolutionary histories. In addition, they are expressed differentially during the P. nicotianae life cycle, including plant infection. Last, we show that there is a strong association between the expression of a glucokinase member in planta and extent of plant infection. Together, these results suggest that metabolic adaptation is a component of the processes underlying evolution of parasitism in Phytophthora, which may possibly involve the neofunctionalization of metabolic enzymes.
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spelling pubmed-88794442022-02-26 Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae Kuhn, Marie-Line Berre, Jo-Yanne Le Kebdani-Minet, Naima Panabières, Franck Microorganisms Article Oomycetes, of the genus Phytophthora, comprise of some of the most devastating plant pathogens. Parasitism of Phytophthora results from evolution from an autotrophic ancestor and adaptation to a wide range of environments, involving metabolic adaptation. Sequence mining showed that Phytophthora spp. display an unusual repertoire of glycolytic enzymes, made of multigene families and enzyme replacements. To investigate the impact of these gene duplications on the biology of Phytophthora and, eventually, identify novel functions associated to gene expansion, we focused our study on the first glycolytic step on P. nicotianae, a broad host range pathogen. We reveal that this step is committed by a set of three glucokinase types that differ by their structure, enzymatic properties, and evolutionary histories. In addition, they are expressed differentially during the P. nicotianae life cycle, including plant infection. Last, we show that there is a strong association between the expression of a glucokinase member in planta and extent of plant infection. Together, these results suggest that metabolic adaptation is a component of the processes underlying evolution of parasitism in Phytophthora, which may possibly involve the neofunctionalization of metabolic enzymes. MDPI 2022-01-25 /pmc/articles/PMC8879444/ /pubmed/35208735 http://dx.doi.org/10.3390/microorganisms10020281 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Kuhn, Marie-Line
Berre, Jo-Yanne Le
Kebdani-Minet, Naima
Panabières, Franck
Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae
title Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae
title_full Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae
title_fullStr Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae
title_full_unstemmed Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae
title_short Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae
title_sort neofunctionalization of glycolytic enzymes: an evolutionary route to plant parasitism in the oomycete phytophthora nicotianae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8879444/
https://www.ncbi.nlm.nih.gov/pubmed/35208735
http://dx.doi.org/10.3390/microorganisms10020281
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