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Insights Into the Genetics of the Zhonghua 11 Resistance to Meloidogyne graminicola and Its Molecular Determinism in Rice

Meloidogyne graminicola is a widely spread nematode pest of rice that reduces crop yield up to 20% on average in Asia, with devastating consequences for local and global rice production. Due to the ban on many chemical nematicides and the recent changes in water management practices in rice agricult...

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Autores principales: Nguyen, Hue Thi, Mantelin, Sophie, Ha, Cuong Viet, Lorieux, Mathias, Jones, John T., Mai, Chung Duc, Bellafiore, Stéphane
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9116194/
https://www.ncbi.nlm.nih.gov/pubmed/35599898
http://dx.doi.org/10.3389/fpls.2022.854961
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author Nguyen, Hue Thi
Mantelin, Sophie
Ha, Cuong Viet
Lorieux, Mathias
Jones, John T.
Mai, Chung Duc
Bellafiore, Stéphane
author_facet Nguyen, Hue Thi
Mantelin, Sophie
Ha, Cuong Viet
Lorieux, Mathias
Jones, John T.
Mai, Chung Duc
Bellafiore, Stéphane
author_sort Nguyen, Hue Thi
collection PubMed
description Meloidogyne graminicola is a widely spread nematode pest of rice that reduces crop yield up to 20% on average in Asia, with devastating consequences for local and global rice production. Due to the ban on many chemical nematicides and the recent changes in water management practices in rice agriculture, an even greater impact of M. graminicola can be expected in the future, stressing the demand for the development of new sustainable nematode management solutions. Recently, a source of resistance to M. graminicola was identified in the Oryza sativa japonica rice variety Zhonghua 11 (Zh11). In the present study, we examine the genetics of the Zh11 resistance to M. graminicola and provide new insights into its cellular and molecular mechanisms. The segregation of the resistance in F(2) hybrid populations indicated that two dominant genes may be contributing to the resistance. The incompatible interaction of M. graminicola in Zh11 was distinguished by a lack of swelling of the root tips normally observed in compatible interactions. At the cellular level, the incompatible interaction was characterised by a rapid accumulation of reactive oxygen species in the vicinity of the nematodes, accompanied by extensive necrosis of neighbouring cells. The expression profiles of several genes involved in plant immunity were analysed at the early stages of infection during compatible (susceptible plant) and incompatible (resistant plant) interactions. Notably, the expression of OsAtg4 and OsAtg7, significantly increased in roots of resistant plants in parallel with the cell death response, suggesting that autophagy is activated and may contribute to the resistance-mediated hypersensitive response. Similarly, transcriptional regulation of genes involved in hormonal pathways in Zh11 indicated that salicylate signalling may be important in the resistance response towards M. graminicola. Finally, the nature of the resistance to M. graminicola and the potential exploitation of the Zh11 resistance for breeding are discussed.
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spelling pubmed-91161942022-05-19 Insights Into the Genetics of the Zhonghua 11 Resistance to Meloidogyne graminicola and Its Molecular Determinism in Rice Nguyen, Hue Thi Mantelin, Sophie Ha, Cuong Viet Lorieux, Mathias Jones, John T. Mai, Chung Duc Bellafiore, Stéphane Front Plant Sci Plant Science Meloidogyne graminicola is a widely spread nematode pest of rice that reduces crop yield up to 20% on average in Asia, with devastating consequences for local and global rice production. Due to the ban on many chemical nematicides and the recent changes in water management practices in rice agriculture, an even greater impact of M. graminicola can be expected in the future, stressing the demand for the development of new sustainable nematode management solutions. Recently, a source of resistance to M. graminicola was identified in the Oryza sativa japonica rice variety Zhonghua 11 (Zh11). In the present study, we examine the genetics of the Zh11 resistance to M. graminicola and provide new insights into its cellular and molecular mechanisms. The segregation of the resistance in F(2) hybrid populations indicated that two dominant genes may be contributing to the resistance. The incompatible interaction of M. graminicola in Zh11 was distinguished by a lack of swelling of the root tips normally observed in compatible interactions. At the cellular level, the incompatible interaction was characterised by a rapid accumulation of reactive oxygen species in the vicinity of the nematodes, accompanied by extensive necrosis of neighbouring cells. The expression profiles of several genes involved in plant immunity were analysed at the early stages of infection during compatible (susceptible plant) and incompatible (resistant plant) interactions. Notably, the expression of OsAtg4 and OsAtg7, significantly increased in roots of resistant plants in parallel with the cell death response, suggesting that autophagy is activated and may contribute to the resistance-mediated hypersensitive response. Similarly, transcriptional regulation of genes involved in hormonal pathways in Zh11 indicated that salicylate signalling may be important in the resistance response towards M. graminicola. Finally, the nature of the resistance to M. graminicola and the potential exploitation of the Zh11 resistance for breeding are discussed. Frontiers Media S.A. 2022-05-04 /pmc/articles/PMC9116194/ /pubmed/35599898 http://dx.doi.org/10.3389/fpls.2022.854961 Text en Copyright © 2022 Nguyen, Mantelin, Ha, Lorieux, Jones, Mai and Bellafiore. https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Plant Science
Nguyen, Hue Thi
Mantelin, Sophie
Ha, Cuong Viet
Lorieux, Mathias
Jones, John T.
Mai, Chung Duc
Bellafiore, Stéphane
Insights Into the Genetics of the Zhonghua 11 Resistance to Meloidogyne graminicola and Its Molecular Determinism in Rice
title Insights Into the Genetics of the Zhonghua 11 Resistance to Meloidogyne graminicola and Its Molecular Determinism in Rice
title_full Insights Into the Genetics of the Zhonghua 11 Resistance to Meloidogyne graminicola and Its Molecular Determinism in Rice
title_fullStr Insights Into the Genetics of the Zhonghua 11 Resistance to Meloidogyne graminicola and Its Molecular Determinism in Rice
title_full_unstemmed Insights Into the Genetics of the Zhonghua 11 Resistance to Meloidogyne graminicola and Its Molecular Determinism in Rice
title_short Insights Into the Genetics of the Zhonghua 11 Resistance to Meloidogyne graminicola and Its Molecular Determinism in Rice
title_sort insights into the genetics of the zhonghua 11 resistance to meloidogyne graminicola and its molecular determinism in rice
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9116194/
https://www.ncbi.nlm.nih.gov/pubmed/35599898
http://dx.doi.org/10.3389/fpls.2022.854961
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