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Integrated Omic Approaches Reveal Molecular Mechanisms of Tolerance during Soybean and Meloidogyne incognita Interactions

The root-knot nematode (RKN), Meloidogyne incognita, is a devastating soybean pathogen worldwide. The use of resistant cultivars is the most effective method to prevent economic losses caused by RKNs. To elucidate the mechanisms involved in resistance to RKN, we determined the proteome and transcrip...

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Autores principales: Arraes, Fabricio B. M., Vasquez, Daniel D. N., Tahir, Muhammed, Pinheiro, Daniele H., Faheem, Muhammed, Freitas-Alves, Nayara S., Moreira-Pinto, Clídia E., Moreira, Valdeir J. V., Paes-de-Melo, Bruno, Lisei-de-Sa, Maria E., Morgante, Carolina V., Mota, Ana P. Z., Lourenço-Tessutti, Isabela T., Togawa, Roberto C., Grynberg, Priscila, Fragoso, Rodrigo R., de Almeida-Engler, Janice, Larsen, Martin R., Grossi-de-Sa, Maria F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9612212/
https://www.ncbi.nlm.nih.gov/pubmed/36297768
http://dx.doi.org/10.3390/plants11202744
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author Arraes, Fabricio B. M.
Vasquez, Daniel D. N.
Tahir, Muhammed
Pinheiro, Daniele H.
Faheem, Muhammed
Freitas-Alves, Nayara S.
Moreira-Pinto, Clídia E.
Moreira, Valdeir J. V.
Paes-de-Melo, Bruno
Lisei-de-Sa, Maria E.
Morgante, Carolina V.
Mota, Ana P. Z.
Lourenço-Tessutti, Isabela T.
Togawa, Roberto C.
Grynberg, Priscila
Fragoso, Rodrigo R.
de Almeida-Engler, Janice
Larsen, Martin R.
Grossi-de-Sa, Maria F.
author_facet Arraes, Fabricio B. M.
Vasquez, Daniel D. N.
Tahir, Muhammed
Pinheiro, Daniele H.
Faheem, Muhammed
Freitas-Alves, Nayara S.
Moreira-Pinto, Clídia E.
Moreira, Valdeir J. V.
Paes-de-Melo, Bruno
Lisei-de-Sa, Maria E.
Morgante, Carolina V.
Mota, Ana P. Z.
Lourenço-Tessutti, Isabela T.
Togawa, Roberto C.
Grynberg, Priscila
Fragoso, Rodrigo R.
de Almeida-Engler, Janice
Larsen, Martin R.
Grossi-de-Sa, Maria F.
author_sort Arraes, Fabricio B. M.
collection PubMed
description The root-knot nematode (RKN), Meloidogyne incognita, is a devastating soybean pathogen worldwide. The use of resistant cultivars is the most effective method to prevent economic losses caused by RKNs. To elucidate the mechanisms involved in resistance to RKN, we determined the proteome and transcriptome profiles from roots of susceptible (BRS133) and highly tolerant (PI 595099) Glycine max genotypes 4, 12, and 30 days after RKN infestation. After in silico analysis, we described major defense molecules and mechanisms considered constitutive responses to nematode infestation, such as mTOR, PI3K-Akt, relaxin, and thermogenesis. The integrated data allowed us to identify protein families and metabolic pathways exclusively regulated in tolerant soybean genotypes. Among them, we highlighted the phenylpropanoid pathway as an early, robust, and systemic defense process capable of controlling M. incognita reproduction. Associated with this metabolic pathway, 29 differentially expressed genes encoding 11 different enzymes were identified, mainly from the flavonoid and derivative pathways. Based on differential expression in transcriptomic and proteomic data, as well as in the expression profile by RT–qPCR, and previous studies, we selected and overexpressed the GmPR10 gene in transgenic tobacco to assess its protective effect against M. incognita. Transgenic plants of the T(2) generation showed up to 58% reduction in the M. incognita reproduction factor. Finally, data suggest that GmPR10 overexpression can be effective against the plant parasitic nematode M. incognita, but its mechanism of action remains unclear. These findings will help develop new engineered soybean genotypes with higher performance in response to RKN infections.
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spelling pubmed-96122122022-10-28 Integrated Omic Approaches Reveal Molecular Mechanisms of Tolerance during Soybean and Meloidogyne incognita Interactions Arraes, Fabricio B. M. Vasquez, Daniel D. N. Tahir, Muhammed Pinheiro, Daniele H. Faheem, Muhammed Freitas-Alves, Nayara S. Moreira-Pinto, Clídia E. Moreira, Valdeir J. V. Paes-de-Melo, Bruno Lisei-de-Sa, Maria E. Morgante, Carolina V. Mota, Ana P. Z. Lourenço-Tessutti, Isabela T. Togawa, Roberto C. Grynberg, Priscila Fragoso, Rodrigo R. de Almeida-Engler, Janice Larsen, Martin R. Grossi-de-Sa, Maria F. Plants (Basel) Article The root-knot nematode (RKN), Meloidogyne incognita, is a devastating soybean pathogen worldwide. The use of resistant cultivars is the most effective method to prevent economic losses caused by RKNs. To elucidate the mechanisms involved in resistance to RKN, we determined the proteome and transcriptome profiles from roots of susceptible (BRS133) and highly tolerant (PI 595099) Glycine max genotypes 4, 12, and 30 days after RKN infestation. After in silico analysis, we described major defense molecules and mechanisms considered constitutive responses to nematode infestation, such as mTOR, PI3K-Akt, relaxin, and thermogenesis. The integrated data allowed us to identify protein families and metabolic pathways exclusively regulated in tolerant soybean genotypes. Among them, we highlighted the phenylpropanoid pathway as an early, robust, and systemic defense process capable of controlling M. incognita reproduction. Associated with this metabolic pathway, 29 differentially expressed genes encoding 11 different enzymes were identified, mainly from the flavonoid and derivative pathways. Based on differential expression in transcriptomic and proteomic data, as well as in the expression profile by RT–qPCR, and previous studies, we selected and overexpressed the GmPR10 gene in transgenic tobacco to assess its protective effect against M. incognita. Transgenic plants of the T(2) generation showed up to 58% reduction in the M. incognita reproduction factor. Finally, data suggest that GmPR10 overexpression can be effective against the plant parasitic nematode M. incognita, but its mechanism of action remains unclear. These findings will help develop new engineered soybean genotypes with higher performance in response to RKN infections. MDPI 2022-10-17 /pmc/articles/PMC9612212/ /pubmed/36297768 http://dx.doi.org/10.3390/plants11202744 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
Arraes, Fabricio B. M.
Vasquez, Daniel D. N.
Tahir, Muhammed
Pinheiro, Daniele H.
Faheem, Muhammed
Freitas-Alves, Nayara S.
Moreira-Pinto, Clídia E.
Moreira, Valdeir J. V.
Paes-de-Melo, Bruno
Lisei-de-Sa, Maria E.
Morgante, Carolina V.
Mota, Ana P. Z.
Lourenço-Tessutti, Isabela T.
Togawa, Roberto C.
Grynberg, Priscila
Fragoso, Rodrigo R.
de Almeida-Engler, Janice
Larsen, Martin R.
Grossi-de-Sa, Maria F.
Integrated Omic Approaches Reveal Molecular Mechanisms of Tolerance during Soybean and Meloidogyne incognita Interactions
title Integrated Omic Approaches Reveal Molecular Mechanisms of Tolerance during Soybean and Meloidogyne incognita Interactions
title_full Integrated Omic Approaches Reveal Molecular Mechanisms of Tolerance during Soybean and Meloidogyne incognita Interactions
title_fullStr Integrated Omic Approaches Reveal Molecular Mechanisms of Tolerance during Soybean and Meloidogyne incognita Interactions
title_full_unstemmed Integrated Omic Approaches Reveal Molecular Mechanisms of Tolerance during Soybean and Meloidogyne incognita Interactions
title_short Integrated Omic Approaches Reveal Molecular Mechanisms of Tolerance during Soybean and Meloidogyne incognita Interactions
title_sort integrated omic approaches reveal molecular mechanisms of tolerance during soybean and meloidogyne incognita interactions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9612212/
https://www.ncbi.nlm.nih.gov/pubmed/36297768
http://dx.doi.org/10.3390/plants11202744
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