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Resistance is threatening the effectiveness of insecticide-based interventions in use for malaria control. Pinpointing genes associated with resistance is crucial for evidence-based resistance management targeting the major malaria vectors. Here, a combination of RNA-seq based genome-wide transcriptional analysis and RNA-silencing in vivo functional validation were used to identify key insecticide resistance genes associated with DDT and DDT/permethrin cross-resistance across Africa. A cluster of glutathione-S-transferase from epsilon group were found to be overexpressed in resistant populations of  Anopheles funestus  across Africa including  GSTe1  [Cameroon (fold change, FC: 2.54), Ghana (4.20), Malawi (2.51)],  GSTe2  [Cameroon (4.47), Ghana (7.52), Malawi (2.13)],  GSTe3  [Cameroon (2.49), Uganda (2.60)],  GSTe4  in Ghana (3.47),  GSTe5  [Ghana (2.94), Malawi (2.26)],  GSTe6  [Cameroun (3.0), Ghana (3.11), Malawi (3.07), Uganda (3.78)] and  GSTe7  (2.39) in Ghana. Validation of  GSTe  genes expression profiles by qPCR confirmed that the genes are differentially expressed across Africa with a greater overexpression in DDT-resistant mosquitoes. RNAi-based knock-down analyses supported that five  GSTe  genes are playing a major role in resistance to pyrethroids (permethrin and deltamethrin) and DDT in  An. funestus , with a significant recovery of susceptibility observed when  GSTe2 ,  3 ,  4 ,  5  and  GSTe6  were silenced. These findings established that  GSTe3 ,  4 ,  5  and  6  contribute to DDT resistance and should be further characterized to identify their specific genetic variants, to help design DNA-based diagnostic assays, as previously done for the  119F-GSTe2  mutation. This study highlights the role of  GSTe s in the development of resistance to insecticides in malaria vectors and calls for actions to mitigate this resistance.

genes

Genome-Wide Transcriptional Analysis and Functional Validation Linked a Cluster of Epsilon Glutathione S-Transferases with Insecticide Resistance in the Major Malaria Vector Anopheles funestus across Africa