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Minimization of energy transduction confers resistance to phosphine in the rice weevil, Sitophilus oryzae

Infestation of phosphine (PH(3)) resistant insects threatens global grain reserves. PH(3) fumigation controls rice weevil (Sitophilus oryzae) but not highly resistant insect pests. Here, we investigated naturally occurring strains of S. oryzae that were moderately resistant (MR), strongly resistant...

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Autores principales: Kim, Kyeongnam, Yang, Jeong Oh, Sung, Jae-Yoon, Lee, Ji-Young, Park, Jeong Sun, Lee, Heung-Sik, Lee, Byung-Ho, Ren, Yonglin, Lee, Dong-Woo, Lee, Sung-Eun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6787191/
https://www.ncbi.nlm.nih.gov/pubmed/31601880
http://dx.doi.org/10.1038/s41598-019-50972-w
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author Kim, Kyeongnam
Yang, Jeong Oh
Sung, Jae-Yoon
Lee, Ji-Young
Park, Jeong Sun
Lee, Heung-Sik
Lee, Byung-Ho
Ren, Yonglin
Lee, Dong-Woo
Lee, Sung-Eun
author_facet Kim, Kyeongnam
Yang, Jeong Oh
Sung, Jae-Yoon
Lee, Ji-Young
Park, Jeong Sun
Lee, Heung-Sik
Lee, Byung-Ho
Ren, Yonglin
Lee, Dong-Woo
Lee, Sung-Eun
author_sort Kim, Kyeongnam
collection PubMed
description Infestation of phosphine (PH(3)) resistant insects threatens global grain reserves. PH(3) fumigation controls rice weevil (Sitophilus oryzae) but not highly resistant insect pests. Here, we investigated naturally occurring strains of S. oryzae that were moderately resistant (MR), strongly resistant (SR), or susceptible (wild-type; WT) to PH(3) using global proteome analysis and mitochondrial DNA sequencing. Both PH(3) resistant (PH(3)–R) strains exhibited higher susceptibility to ethyl formate-mediated inhibition of cytochrome c oxidase than the WT strain, whereas the disinfectant PH(3) concentration time of the SR strain was much longer than that of the MR strain. Unlike the MR strain, which showed altered expression levels of genes encoding metabolic enzymes involved in catabolic pathways that minimize metabolic burden, the SR strain showed changes in the mitochondrial respiratory chain. Our results suggest that the acquisition of strong PH(3) resistance necessitates the avoidance of oxidative phosphorylation through the accumulation of a few non-synonymous mutations in mitochondrial genes encoding complex I subunits as well as nuclear genes encoding dihydrolipoamide dehydrogenase, concomitant with metabolic reprogramming, a recognized hallmark of cancer metabolism. Taken together, our data suggest that reprogrammed metabolism represents a survival strategy of SR insect pests for the compensation of minimized energy transduction under anoxic conditions. Therefore, understanding the resistance mechanism of PH(3)–R strains will support the development of new strategies to control insect pests.
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spelling pubmed-67871912019-10-17 Minimization of energy transduction confers resistance to phosphine in the rice weevil, Sitophilus oryzae Kim, Kyeongnam Yang, Jeong Oh Sung, Jae-Yoon Lee, Ji-Young Park, Jeong Sun Lee, Heung-Sik Lee, Byung-Ho Ren, Yonglin Lee, Dong-Woo Lee, Sung-Eun Sci Rep Article Infestation of phosphine (PH(3)) resistant insects threatens global grain reserves. PH(3) fumigation controls rice weevil (Sitophilus oryzae) but not highly resistant insect pests. Here, we investigated naturally occurring strains of S. oryzae that were moderately resistant (MR), strongly resistant (SR), or susceptible (wild-type; WT) to PH(3) using global proteome analysis and mitochondrial DNA sequencing. Both PH(3) resistant (PH(3)–R) strains exhibited higher susceptibility to ethyl formate-mediated inhibition of cytochrome c oxidase than the WT strain, whereas the disinfectant PH(3) concentration time of the SR strain was much longer than that of the MR strain. Unlike the MR strain, which showed altered expression levels of genes encoding metabolic enzymes involved in catabolic pathways that minimize metabolic burden, the SR strain showed changes in the mitochondrial respiratory chain. Our results suggest that the acquisition of strong PH(3) resistance necessitates the avoidance of oxidative phosphorylation through the accumulation of a few non-synonymous mutations in mitochondrial genes encoding complex I subunits as well as nuclear genes encoding dihydrolipoamide dehydrogenase, concomitant with metabolic reprogramming, a recognized hallmark of cancer metabolism. Taken together, our data suggest that reprogrammed metabolism represents a survival strategy of SR insect pests for the compensation of minimized energy transduction under anoxic conditions. Therefore, understanding the resistance mechanism of PH(3)–R strains will support the development of new strategies to control insect pests. Nature Publishing Group UK 2019-10-10 /pmc/articles/PMC6787191/ /pubmed/31601880 http://dx.doi.org/10.1038/s41598-019-50972-w Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Kim, Kyeongnam
Yang, Jeong Oh
Sung, Jae-Yoon
Lee, Ji-Young
Park, Jeong Sun
Lee, Heung-Sik
Lee, Byung-Ho
Ren, Yonglin
Lee, Dong-Woo
Lee, Sung-Eun
Minimization of energy transduction confers resistance to phosphine in the rice weevil, Sitophilus oryzae
title Minimization of energy transduction confers resistance to phosphine in the rice weevil, Sitophilus oryzae
title_full Minimization of energy transduction confers resistance to phosphine in the rice weevil, Sitophilus oryzae
title_fullStr Minimization of energy transduction confers resistance to phosphine in the rice weevil, Sitophilus oryzae
title_full_unstemmed Minimization of energy transduction confers resistance to phosphine in the rice weevil, Sitophilus oryzae
title_short Minimization of energy transduction confers resistance to phosphine in the rice weevil, Sitophilus oryzae
title_sort minimization of energy transduction confers resistance to phosphine in the rice weevil, sitophilus oryzae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6787191/
https://www.ncbi.nlm.nih.gov/pubmed/31601880
http://dx.doi.org/10.1038/s41598-019-50972-w
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