Comparative Hessian Fly Larval Transcriptomics Provides Novel Insight into Host and Nonhost Resistance

Subhashree Subramanyam,Shaojun Xie,Nagesh Sardesai,Jyothi Thimmapuram,Jill A Nemacheck,Steven R Scofield,Ketaki Bhide

doi:10.3390/ijms222111498

Abstract

The Hessian fly is a destructive pest of wheat. Employing additional molecular strategies can complement wheat’s native insect resistance. However, this requires functional characterization of Hessian-fly-responsive genes, which is challenging because of wheat genome complexity. The diploid Brachypodium distachyon (Bd) exhibits nonhost resistance to Hessian fly and displays phenotypic/molecular responses intermediate between resistant and susceptible host wheat, offering a surrogate genome for gene characterization. Here, we compared the transcriptomes of Biotype L larvae residing on resistant/susceptible wheat, and nonhost Bd plants. Larvae from susceptible wheat and nonhost Bd plants revealed similar molecular responses that were distinct from avirulent larval responses on resistant wheat. Secreted salivary gland proteins were strongly up-regulated in all larvae. Genes from various biological pathways and molecular processes were up-regulated in larvae from both susceptible wheat and nonhost Bd plants. However, Bd larval expression levels were intermediate between larvae from susceptible and resistant wheat. Most genes were down-regulated or unchanged in avirulent larvae, correlating with their inability to establish feeding sites and dying within 4–5 days after egg-hatch. Decreased gene expression in Bd larvae, compared to ones on susceptible wheat, potentially led to developmentally delayed 2nd-instars, followed by eventually succumbing to nonhost resistance defense mechanisms.

Highlights

The Hessian fly, Mayetiola destructor (Say), belonging to the gall midge family Cecidomyiidae is an obligate pest of host bread wheat (Triticum aestivum) causing severe economic losses [1,2]
RNA-Seq identified several transcriptional changes occurring in Biotype L larvae feeding on both host wheat and nonhost Brachypodium distachyon (Bd) plants
To reveal global transcriptome changes, RNA-Seq analysis was carried out with RNA extracted from avirulent (A1 and A3) and virulent (V1 and V3) larval samples collected from host wheat at 1 and 3 days after egg-hatch (DAH) and from larvae feeding on nonhost Bd plants at 3 (Bd3) and 9 (Bd9) DAH

Summary

Introduction

The Hessian fly, Mayetiola destructor (Say), belonging to the gall midge family Cecidomyiidae (order: Diptera) is an obligate pest of host bread wheat (Triticum aestivum) causing severe economic losses [1,2]. The recognition of insect avirulence (avr) gene product by plant Hessian fly resistance (H) gene product [3] yields an incompatible interaction (avirulent larvae, resistant plants). In this interaction, the wheat seedling mounts H-gene-mediated resistance, resulting in increased accumulation of defense proteins [4,5,6,7] that disrupt larval midgut microvilli [8]. The virulent larvae complete their development, and the susceptible plant has a stunted phenotype, leading to the eventual death of the wheat seedling [17]

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Conclusion