Deciphering the underlying genetics of galling resistance to the blueberry stem gall wasp in northern highbush blueberry

Abstract

Certain specialist herbivorous insects have evolved elegant mechanisms to manipulate the physiology of their host plants, including the ability to redirect the fate of plant cells toward the creation of a novel, tumor-like organ, called ‘galls’. While some plants have evolved resistance to gall-inducing insects, the underlying genetic mechanisms remain poorly understood. In this study, we focused on the chalcid gall-inducing wasp, Hemadas nubilipennis (Ormyridae) and its host plant, highbush blueberry Vaccinium corymbosum (Ericaceae). To identify the genetic basis of resistance to gall induction in blueberry, we developed a genetic mapping population derived from the susceptible ‘Liberty’ and resistant ‘Draper’ cultivars. We identified four quantitative trait loci (QTLs) associated with galling resistance, with candidate genes in these regions associated with plant defense, biotic stress response, and phytohormone metabolism. Furthermore, we analyzed gene expression on days one through seven post-oviposition in both susceptible and resistant genotypes, compared to controls, to identify genes and pathways that may contribute to galling resistance. Gene expression analyses, including genes within the four identified QTL regions, revealed a robust early defense response in the resistant genotype, marked by upregulation of defense, stress, and immunity genes following oviposition, ultimately leading to insect death. Conversely, the susceptible genotype exhibited a delayed and weaker response, allowing gall development and insect survival. We expect these results to serve as a resource that will enable breeding programs to employ molecular approaches for selection of resistant cultivars, while also guiding future research aimed at studying the evolution of galling resistance.

Acknowledgements

This project was funded by MSU AgBioResearch and Rackham Foundation Endowment to P.P.E., United States Department of Agriculture NIFA Crop Protection and Pest Management Program (2018-70006-28917) to R.I. and P.P.E., Specialty Crop Research Initiative (USDA-SCRI) 2019-51181-30015 to P.P.E, USDA HATCH Project MICL02742 to P.P.E., and National Science Foundation Research Traineeship Program (DGE-1828149). We would like to thank the Institute for Cyber-Enabled Research at MSU for computational resources, and Pete Callow, Beth Alger, Alexys Kelsey, Henry Pointon, and Parker Graham for their assistance with plant care and phenotyping for gall resistance.

Author contributions

P.P.E. conceived and designed the project; M.C. collected the samples and extracted the RNA; J.B. and P.M. led the development of the genotyping array; M.C., P.D.F., J.A.P., and R.I. led phenotyping for gall resistance; S.J.T., M.J.A.B., A.F., A.E.P., R.R.A., and P.P.E. performed bioinformatic and statistical analyses; S.J.T. and P.P.E. were in charge of data submission; M.B., S.J.T., J.C.S., and P.P.E. wrote the manuscript draft, and all coauthors reviewed and revised the manuscript.

Data availability

Genomic target sequence capture and RNA-seq data that were generated for this study are available at NCBI SRA under BioProject PRJNA842728. All version-controlled code related to the analyses can be found at https://github.com/sjteresi/Blueberry_RNA_Seq_Expression_Analysisand https://github.com/sjteresi/Blueberry_Network_Rewiring.Annotated scripts and READMEs containing additional information can be found in the GitHub repositories.

Conflict of interest statement

The authors declare no conflict of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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