Transcriptome Analysis and Knockdown of the Juvenile Hormone Esterase Gene Reveal Abnormal Feeding Behavior in the Sugarcane Giant Borer

The sugarcane giant borer (SGB), Telchin licus licus, is a pest that has strong economic relevance for sugarcane producers. Due to the endophytic behavior of the larva, current methods of management are inefficient. A promising biotechnological management option has been proposed based on RNA interf...

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Main Authors: Daniel D. Noriega, Fabricio B. M. Arraes, José Dijair Antonino, Leonardo L. P. Macedo, Fernando C. A. Fonseca, Roberto C. Togawa, Priscila Grynberg, Maria C. M. Silva, Aldomario S. Negrisoli, Maria F. Grossi-de-Sa
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2020.588450/full
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author Daniel D. Noriega
Daniel D. Noriega
Daniel D. Noriega
Fabricio B. M. Arraes
Fabricio B. M. Arraes
José Dijair Antonino
José Dijair Antonino
Leonardo L. P. Macedo
Fernando C. A. Fonseca
Fernando C. A. Fonseca
Roberto C. Togawa
Priscila Grynberg
Maria C. M. Silva
Aldomario S. Negrisoli
Maria F. Grossi-de-Sa
Maria F. Grossi-de-Sa
Maria F. Grossi-de-Sa
spellingShingle Daniel D. Noriega
Daniel D. Noriega
Daniel D. Noriega
Fabricio B. M. Arraes
Fabricio B. M. Arraes
José Dijair Antonino
José Dijair Antonino
Leonardo L. P. Macedo
Fernando C. A. Fonseca
Fernando C. A. Fonseca
Roberto C. Togawa
Priscila Grynberg
Maria C. M. Silva
Aldomario S. Negrisoli
Maria F. Grossi-de-Sa
Maria F. Grossi-de-Sa
Maria F. Grossi-de-Sa
Transcriptome Analysis and Knockdown of the Juvenile Hormone Esterase Gene Reveal Abnormal Feeding Behavior in the Sugarcane Giant Borer
Frontiers in Physiology
Telchin licus licus
RNA interference
Lepidoptera
insect gut
RNA-seq
author_facet Daniel D. Noriega
Daniel D. Noriega
Daniel D. Noriega
Fabricio B. M. Arraes
Fabricio B. M. Arraes
José Dijair Antonino
José Dijair Antonino
Leonardo L. P. Macedo
Fernando C. A. Fonseca
Fernando C. A. Fonseca
Roberto C. Togawa
Priscila Grynberg
Maria C. M. Silva
Aldomario S. Negrisoli
Maria F. Grossi-de-Sa
Maria F. Grossi-de-Sa
Maria F. Grossi-de-Sa
author_sort Daniel D. Noriega
title Transcriptome Analysis and Knockdown of the Juvenile Hormone Esterase Gene Reveal Abnormal Feeding Behavior in the Sugarcane Giant Borer
title_short Transcriptome Analysis and Knockdown of the Juvenile Hormone Esterase Gene Reveal Abnormal Feeding Behavior in the Sugarcane Giant Borer
title_full Transcriptome Analysis and Knockdown of the Juvenile Hormone Esterase Gene Reveal Abnormal Feeding Behavior in the Sugarcane Giant Borer
title_fullStr Transcriptome Analysis and Knockdown of the Juvenile Hormone Esterase Gene Reveal Abnormal Feeding Behavior in the Sugarcane Giant Borer
title_full_unstemmed Transcriptome Analysis and Knockdown of the Juvenile Hormone Esterase Gene Reveal Abnormal Feeding Behavior in the Sugarcane Giant Borer
title_sort transcriptome analysis and knockdown of the juvenile hormone esterase gene reveal abnormal feeding behavior in the sugarcane giant borer
publisher Frontiers Media S.A.
series Frontiers in Physiology
issn 1664-042X
publishDate 2020-10-01
description The sugarcane giant borer (SGB), Telchin licus licus, is a pest that has strong economic relevance for sugarcane producers. Due to the endophytic behavior of the larva, current methods of management are inefficient. A promising biotechnological management option has been proposed based on RNA interference (RNAi), a process that uses molecules of double-stranded RNA (dsRNA) to specifically knock down essential genes and reduce insect survival. The selection of suitable target genes is often supported by omic sciences. Studies have shown that genes related to feeding adaptation processes are good candidates to be targeted by RNAi for pest management. Among those genes, esterases are highlighted because of their impact on insect development. In this study, the objective was to evaluate the transcriptome responses of the SGB’s gut in order to provide curated data of genes that could be used for pest management by RNAi in future studies. Further, we validated the function of an esterase-coding gene and its potential as a target for RNAi-based control. We sequenced the gut transcriptome of SGB larvae by Illumina HiSeq and evaluated its gene expression profiles in response to different diets (sugarcane stalk and artificial diet). We obtained differentially expressed genes (DEGs) involved in detoxification, digestion, and transport, which suggest a generalist mechanism of adaptation in SGB larvae. Among the DEGs, was identified and characterized a candidate juvenile hormone esterase gene (Tljhe). We knocked down the Tljhe gene by oral delivery of dsRNA molecules and evaluated gene expression in the gut. The survival and nutritional parameters of the larvae were measured along the developmental cycle of treated insects. We found that the gene Tljhe acts as a regulator of feeding behavior. The knockdown of Tljhe triggered a forced starvation state in late larval instars that significantly reduced the fitness of the larvae. However, the mechanism of action of this gene remains unclear, and the correlation between the expression of Tljhe and the levels of juvenile hormone (JH) metabolites in the hemolymph of the SGB must be assessed in future research.
topic Telchin licus licus
RNA interference
Lepidoptera
insect gut
RNA-seq
url https://www.frontiersin.org/articles/10.3389/fphys.2020.588450/full
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spelling doaj-f0fb5549743b4e9588f3fd2ea1261c0c2020-11-25T04:06:12ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-10-011110.3389/fphys.2020.588450588450Transcriptome Analysis and Knockdown of the Juvenile Hormone Esterase Gene Reveal Abnormal Feeding Behavior in the Sugarcane Giant BorerDaniel D. Noriega0Daniel D. Noriega1Daniel D. Noriega2Fabricio B. M. Arraes3Fabricio B. M. Arraes4José Dijair Antonino5José Dijair Antonino6Leonardo L. P. Macedo7Fernando C. A. Fonseca8Fernando C. A. Fonseca9Roberto C. Togawa10Priscila Grynberg11Maria C. M. Silva12Aldomario S. Negrisoli13Maria F. Grossi-de-Sa14Maria F. Grossi-de-Sa15Maria F. Grossi-de-Sa16Embrapa Genetic Resources and Biotechnology, Brasília, BrazilDepartment of Cellular Biology, University of Brasília, Brasília, BrazilPPG in Genomic Sciences and Biotechnology, Catholic University of Brasília, Brasília, BrazilEmbrapa Genetic Resources and Biotechnology, Brasília, BrazilBiotechnology Center, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, BrazilEmbrapa Genetic Resources and Biotechnology, Brasília, BrazilDepartment of Agronomy/Entomology, Universidade Federal Rural de Pernambuco (UFRPE), Recife, BrazilEmbrapa Genetic Resources and Biotechnology, Brasília, BrazilEmbrapa Genetic Resources and Biotechnology, Brasília, BrazilDepartment of Cellular Biology, University of Brasília, Brasília, BrazilEmbrapa Genetic Resources and Biotechnology, Brasília, BrazilEmbrapa Genetic Resources and Biotechnology, Brasília, BrazilEmbrapa Genetic Resources and Biotechnology, Brasília, BrazilEmbrapa Coastal Tablelands, Aracaju, BrazilEmbrapa Genetic Resources and Biotechnology, Brasília, BrazilPPG in Genomic Sciences and Biotechnology, Catholic University of Brasília, Brasília, BrazilNational Institute of Science and Technology (INCT) PlantStress Biotech, Brazilian Agricultural Research Corporation (EMBRAPA), Brasília, BrazilThe sugarcane giant borer (SGB), Telchin licus licus, is a pest that has strong economic relevance for sugarcane producers. Due to the endophytic behavior of the larva, current methods of management are inefficient. A promising biotechnological management option has been proposed based on RNA interference (RNAi), a process that uses molecules of double-stranded RNA (dsRNA) to specifically knock down essential genes and reduce insect survival. The selection of suitable target genes is often supported by omic sciences. Studies have shown that genes related to feeding adaptation processes are good candidates to be targeted by RNAi for pest management. Among those genes, esterases are highlighted because of their impact on insect development. In this study, the objective was to evaluate the transcriptome responses of the SGB’s gut in order to provide curated data of genes that could be used for pest management by RNAi in future studies. Further, we validated the function of an esterase-coding gene and its potential as a target for RNAi-based control. We sequenced the gut transcriptome of SGB larvae by Illumina HiSeq and evaluated its gene expression profiles in response to different diets (sugarcane stalk and artificial diet). We obtained differentially expressed genes (DEGs) involved in detoxification, digestion, and transport, which suggest a generalist mechanism of adaptation in SGB larvae. Among the DEGs, was identified and characterized a candidate juvenile hormone esterase gene (Tljhe). We knocked down the Tljhe gene by oral delivery of dsRNA molecules and evaluated gene expression in the gut. The survival and nutritional parameters of the larvae were measured along the developmental cycle of treated insects. We found that the gene Tljhe acts as a regulator of feeding behavior. The knockdown of Tljhe triggered a forced starvation state in late larval instars that significantly reduced the fitness of the larvae. However, the mechanism of action of this gene remains unclear, and the correlation between the expression of Tljhe and the levels of juvenile hormone (JH) metabolites in the hemolymph of the SGB must be assessed in future research.https://www.frontiersin.org/articles/10.3389/fphys.2020.588450/fullTelchin licus licusRNA interferenceLepidopterainsect gutRNA-seq