Understanding the evolution of insecticide resistance in Brazilian crop pests: Towards effective Insecticide Resistance Management (IRM)

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

Insect pests represent a major threat to current and future food security with an average of 20% of crops worldwide lost annually to herbivorous insects. This issue is particularly acute in Brazil where agriculture forms a key component of the economy accounting for 26% of gross domestic product (GDP). Synthetic insecticides are widely used by farmers and growers in Brazil in an attempt to reduce yield loss from insect pests. Unfortunately, the growing reliance on insecticides has resulted in the emergence of insect pest populations that are resistant to many of the chemicals used for control. Two of the most economically important species in this regard are the neotropical brown stink bug, Euschistus heros, and the fall armyworm, Spodoptera frugiperda. E. heros is a major pest of soybean and vegetable crops and causes severe damage to cotton and maize, while S. frugiperda feeds on more than 80 plant species but is particularly destructive on maize. Resistance to several important insecticides has now emerged in these species and threatens their sustainable control. Despite the seriousness of this issue very little research has been carried out to understand the evolution of resistance in E. heros and S. frugiperda and to use this knowledge to develop means to combat its emergence and spread. This is, in part, due to a lack of genomic resources for these key pest species - particularly in the case of E. heros.

This project builds on key 'omic' (genomic and transcriptomic) and biological resources for E. heros and S. frugiperda generated in a stage 1 pump-prime project to understand the molecular basis of resistance in the two pest species. Specifically, we generated a high quality draft genome sequence of E. heros and strains of E. heros and S. frugiperda that share a common genetic background but differ in their susceptibility to several insecticides. These resources will be exploited in the stage 2 project to identify candidate genes and genetic variation associated with resistance and their causal role validated using transgenic approaches. Understanding the role of these genes in resistance will be facilitated by the generation of gene expression atlases for both species which will comprise databases and user-friendly web applications for studying the expression of genes in different tissues of adults or larvae. These resources will be used in the project to identify where candidate resistance genes are expressed in order to understand how they confer resistance. More broadly their publication will accelerate broad functional genomic research in these pest species beyond the scope of this project. Another key output of the stage 1 project was characterisation of the microbial community (the microbiome) present in the gut of both pest species and the identification of gut bacteria that degrade pesticides. The genomic and biological material generated will be used in the stage 2 project to understand how and to what extent these microbes contribute to resistance, and how they might be disrupted in order to overcome resistance.

The data from these experiments will fundamentally advance our understanding of how insects evolve resistance to insecticides. Furthermore, the knowledge generated will be of direct applied importance in relation to the sustainable control of both pest species. To translate the knowledge gained in this project to combat resistance we will develop simple DNA-based diagnostics, and use these to determine the frequency and distribution of resistance in the field in order to inform rational control decisions and develop insecticide resistance management strategies. Furthermore, we will develop screening tools (recombinant enzyme assays or transgenic insect lines) that can be used by academia and industry to develop resistance-breaking chemistry.

Planned Impact

The proposed research will be of direct and indirect benefit to several groups and end-users beyond the academic community. By characterising the mechanisms of insecticide resistance in two highly damaging insect pests of some of the most economically important crops in Brazil, a primary beneficiary will be Brazilian agriculture. An improved understanding of the molecular basis of insecticide resistance (which detoxifying enzymes and target-site mutations confer insecticide resistance and to which chemical classes) will assist with anticipating resistance risks and cross-resistance profiles, and will thereby influence the design and monitoring of strategies for managing these pests while reducing selection pressure for specific resistance mechanisms. Furthermore the translation of the knowledge generated in this project into tools that can be used to rapidly determine the frequency and distribution of resistance will help growers make rational control decisions. Farmers in other countries where these insects have recently emerged will also benefit from this work. For example the emergence of S. frugiperda in Africa represents a serious threat to maize, the most widely grown crop in Africa and a staple for around half the continent's people. The development of resistance management strategies in Brazil will provide a model that, with modification, would also assist stakeholders in affected African countries to prevent or slow the development of resistance.

The goals of this proposal have additional benefits beyond those relating solely to the control of the target insect pests. Ineffective control due to resistance can result in the wasteful over-application of ineffective compounds leading to negative environmental and economic outcomes. The development of diagnostics for specific resistance mechanisms will allow resistance to be detected at an early stage and avoid these off-target effects.

Another key beneficiary of our work is the agrochemical industry who recognise the responsibility of stewardship of current actives and are keen to prolong the life of these insecticides. The knowledge and deliverables derived from our study will inform the policy of IRAC (Insecticide Resistance Action Committee) international that works as a worldwide specialist technical group of the industry association CropLife providing a coordinated industry response to prevent or delay the development of resistance in insect and mite pests, and its national body in Brazil (IRAC-BR).

We envisage that a further impact of our research will be its potential influence on the policy and regulatory environment of insecticide registration and use. The ultimate outcomes of our work will be of direct relevance in defining which chemistry should be used for control of these species and how (i.e. how frequently, when and in combination with which other controls). A robust regulatory framework is extremely important in ensuring compliance with strategies that aim to manage resistance and extend the life-span of insecticides that retain efficacy.

The genomic and transcriptomic data generated as part of this project has significant scope to result in wide ranging impacts beyond managing resistance. Many of the genes identified and annotated in the genome and transcriptomes represent potential targets for novel control strategies and their sequence characterisation is a prerequisite for strategies based on gene knockdown (RNAi) or genetic manipulation (i.e. gene drives). In the same way characterisation of the gut microbiome of these species and understanding the metabolic activity of these herbivore-associated microbes may assist in industrial development of novel pest-management strategies or may have application for biotechnological applications.

Publications

10 25 50
 
Title Genome assembly of the neotropical brown stink bug, Euschistus heros 
Description As part of BBSRC/FAPESP funded projects (Grant Refs: BB/S018719/1 and BB/R022623/1) we have created new genomic resources for the neotropical brown stink bug, Euschistus heros, an economically important pest of agriculture in Brazil (DAC country). These resources will accelerate subsequent investigation of the molecular mechanisms of insecticide resistance in this species. Bioinformatic assessment of the genome sequence revealed it to be high quality with good representation of all of the genes of this species obtained. Annotation of the genes and other genomic features in this sequence assembly has also been completed. The genome sequence has been publicly available (pre-publication) at The National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/bioproject/489772) and a manuscript on the resource is in preparation. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
Impact The genome sequence is currently being used by us and our partners at the University of São Paulo in a project to understand how insecticide resistance evolves in E. heros as part of project BB/R022623/1. 
URL https://www.ncbi.nlm.nih.gov/bioproject/489772
 
Description Insecticide Resistance Action Committee Brazil (IRAC-BR) 
Organisation Insecticide Resistance Action Committee (IRAC)
Department Insecticide Resistance Action Committee Brazil (IRAC-BR)
Country Brazil 
Sector Charity/Non Profit 
PI Contribution We have provided information and knowledge on insecticide resistance in key crop pests of Brazilian Agri-Ecosystems and the development of tools and resources to combat it from two projects funded by the BBSRC/FAPESP (Grant Refs: BB/S018719/1 and BB/R022623/1).
Collaborator Contribution The collaborators have provided a route to disseminate the project results in order to enhance the impact from our projects (Grant Refs: BB/S018719/1 and BB/R022623/1).
Impact The Insecticide Resistance Action Committee Brazil (IRAC-BR) will consider our findings during the creation of recommendations for insecticide use targeted at growers/grower organisations. These will aim to reduce the loss of insecticides due to resistance, with associated economic and environmental benefits.
Start Year 2018
 
Description The Brazilian Cotton Growers Association (ABRAPA) 
Organisation Brazilian Cotton Growers Association (ABRAPA)
Country Brazil 
Sector Charity/Non Profit 
PI Contribution We have provided information and knowledge on insecticide resistance in key crop pests of Brazilian Agri-Ecosystems and the development of tools and resources to combat it from two projects funded by the BBSRC/FAPESP (Grant Refs: BB/S018719/1 and BB/R022623/1).
Collaborator Contribution The collaborators have provided a route to disseminate the project results in order to enhance the impact from our projects (Grant Refs: BB/S018719/1 and BB/R022623/1).
Impact The Brazilian Cotton Growers Association (ABRAPA)will consider our findings during the creation of recommendations for insecticide use targeted at their growers. These will aim to reduce the loss of insecticides due to resistance, with associated economic and environmental benefits.
Start Year 2018
 
Description The Soybean and Maize Growers Association (APROSOJA) 
Organisation Mato Grosso Soy and Corn Producers Association (Aprosoja)
Country Brazil 
Sector Charity/Non Profit 
PI Contribution We have provided information and knowledge on insecticide resistance in key crop pests of Brazilian Agri-Ecosystems and the development of tools and resources to combat it from two projects funded by the BBSRC/FAPESP (Grant Refs: BB/S018719/1 and BB/R022623/1).
Collaborator Contribution The collaborators have provided a route to disseminate the project results in order to enhance the impact from our projects (Grant Refs: BB/S018719/1 and BB/R022623/1).
Impact The Soybean and Maize Growers Association (APROSOJA) will consider our findings during the creation of recommendations for insecticide use targeted at their growers. These will aim to reduce the loss of insecticides due to resistance, with associated economic and environmental benefits.
Start Year 2018
 
Description The Technical Advisory Committee of Pesticides (CTA) of the Brazilian Ministry of Agriculture 
Organisation Government of Brazil
Department Ministry of Agriculture, Livestock, and Food Supply
Country Brazil 
Sector Public 
PI Contribution We have provided information and knowledge on insecticide resistance in key crop pests of Brazilian Agri-Ecosystems and the development of tools and resources to combat it from two projects funded by the BBSRC/FAPESP (Grant Refs: BB/S018719/1 and BB/R022623/1).
Collaborator Contribution The collaborators have provided a route to disseminate the project results in order to enhance the impact from our projects (Grant Refs: BB/S018719/1 and BB/R022623/1).
Impact The Technical Advisory Committee of Pesticides (CTA) of the Brazilian Ministry of Agriculture will consider our findings during the creation of recommendations for insecticide use and regulation. These will aim to reduce the loss of insecticides due to resistance, with associated economic and environmental benefits.
Start Year 2018
 
Description University of Glasgow 
Organisation University of Glasgow
Country United Kingdom 
Sector Academic/University 
PI Contribution Collaboration / partnership included as part of a grant application, (partnership between the UK and organisation in a DAC list country). This allowed joint funding between the the Biotechnology and Biological Sciences Research Council (BBSRC) and São Paulo Research Foundation (FAPESP) to be obtained (Grant Refs: BB/S018719/1 and BB/R022623/1). In the funded research we provided expertise in insect genomics to colleagues at the the University of Glasgow (most significantly insect genome assemblies). Together our research will facilitate the control of damaging crop pests of Brazilian Agri-ecoystems.
Collaborator Contribution Collaboration / partnership included as part of a grant application, (partnership between the UK and organisation in a DAC list country). This allowed joint funding between the the Biotechnology and Biological Sciences Research Council (BBSRC) and São Paulo Research Foundation (FAPESP) to be obtained (Grant Refs: BB/S018719/1 and BB/R022623/1). In the funded research our partners provided expertise in insect transcriptomics (most significantly insect gene expression atlases). Together our research will facilitate the control of damaging crop pests of Brazilian Agri-ecoystems.
Impact This collaboration allowed joint funding between the the Biotechnology and Biological Sciences Research Council (BBSRC) and São Paulo Research Foundation (FAPESP) to be obtained, Grant Refs: BB/S018719/1 and BB/R022623/1 (see relevant sections of the form for details).
Start Year 2018
 
Description University of São Paulo 
Organisation Universidade de São Paulo
Country Brazil 
Sector Academic/University 
PI Contribution Collaboration / partnership included as part of the original application, (partnership between the UK and organisation in a DAC list country). This allowed joint funding between the the Biotechnology and Biological Sciences Research Council (BBSRC) and São Paulo Research Foundation (FAPESP) to be obtained (Grant Refs: BB/S018719/1 and BB/R022623/1). In the funded research we provided expertise in insect genomics and transcriptomics to colleagues at the the University of São Paulo. Together our research will facilitate the control of damaging crop pests of Brazilian Agri-ecoystems.
Collaborator Contribution Collaboration / partnership included as part of the original application, (partnership between the UK and organisation in a DAC list country). This allowed joint funding between the the Biotechnology and Biological Sciences Research Council (BBSRC) and São Paulo Research Foundation (FAPESP) to be obtained (Grant Refs: BB/S018719/1 and BB/R022623/1). In the funded research our partners provided expertise in practical aspects of insecticide resistance (including the role of the microbiome in resistance) including (indirect) access to insect material. Together our research will facilitate the control of damaging crop pests of Brazilian Agri-ecoystems.
Impact This collaboration allowed joint funding between the Biotechnology and Biological Sciences Research Council (BBSRC) and São Paulo Research Foundation (FAPESP) to be obtained, Grant Refs: BB/S018719/1 and BB/R022623/1 (see relevant sections of the form for details).
Start Year 2018
 
Description Return to Learning, Widening Participation through Skills 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other audiences
Results and Impact I presented an interactive talk at a Return to Learning, Widening Participation through Skills event. This was an outreach activity enabling those who have never studied at degree level to gain an insight into what's on offer at university and the research we do. The event was open to the general public and gave a sense of what university study and research is like, with the aim that some individuals may be interest in pursuing further studies and developing their careers. The response from the attendees was enthusiastic and raised a lot of questions. Some of the participants indicated they planned to give serious thought to pursuing further education linked to this topic.
Year(s) Of Engagement Activity 2019
 
Description School visit - Science at Christmas 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact More than 150 year six and seven students from primary schools attended for a school visit to the University for a series of talks on research conducted at the University. I delivered an interactive lecture including several activities for the children to inspire (which also included research from this BBSRC funded project) and enthuse them on both the topic of insects and science generally. Following the event the teachers in attendance provided very positive feedback and increased interest in insects and research.
Year(s) Of Engagement Activity 2019
 
Description Visit to St Francis School Falmouth 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact I visited St Francis School in Falmouth and conducted an interactive workshop on insects (covering in very general terms current BBSRC research) to >60 primary school children. Their teachers at the school reported significsant increased interest in this topic and appreciation for insects following my visit.
Year(s) Of Engagement Activity 2020