Multiple molecular defense strategies in Brachypodium distachyon surmount Hessian fly (Mayetiola destructor) larvae-induced susceptibility for plant survival

Subhashree Subramanyam,Brandon J. Schemerhorn,Nagesh Sardesai,Andrea M. Hargarten,Christie E. Williams,Jill A. Nemacheck

doi:10.1038/s41598-019-39615-2

Subhashree Subramanyam, Brandon J. Schemerhorn + Show 4 more

Open Access

https://doi.org/10.1038/s41598-019-39615-2

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Abstract

The Hessian fly is a destructive pest of wheat causing severe economic damage. Numerous genes and associated biological pathways have been implicated in defense against Hessian fly. However, due to limited genetic resources, compounded with genome complexity, functional analysis of the candidate genes are challenging in wheat. Physically, Brachypodium distachyon (Bd) exhibits nonhost resistance to Hessian fly, and with a small genome size, short life cycle, vast genetic resources and amenability to transformation, it offers an alternate functional genomic model for deciphering plant-Hessian fly interactions. RNA-sequencing was used to reveal thousands of Hessian fly-responsive genes in Bd one, three, and five days after egg hatch. Genes encoding defense proteins, stress-regulating transcription factors, signaling kinases, and secondary metabolites were strongly up-regulated within the first 24 hours of larval feeding indicating an early defense, similar to resistant wheat. Defense was mediated by a hypersensitive response that included necrotic lesions, up-regulated ROS-generating and -scavenging enzymes, and H2O2 production. Suppression of cell wall-associated proteins and increased cell permeability in Bd resembled susceptible wheat. Thus, Bd molecular responses shared similarities to both resistant and susceptible wheat, validating its suitability as a model genome for undertaking functional studies of candidate Hessian fly-responsive genes.

Highlights

In recent years, the small grass species Brachypodium distachyon (Bd hereafter) has been extensively explored as a useful functional genomic model for grasses[1]
Fewer number of differentially expressed genes (DEGs) were observed in Bd1 samples, there were more up-regulated than down-regulated genes
HPRG: hydroxyproline-rich glycoprotein, AGP: arabinogalactan protein, PGIP: polygalacturonase inhibiting protein, CWII: cell wall invertase inhibitor, GRP: glycine-rich protein, CesA: cellulose synthase, Csl: cellulose synthase-like, COBRA: glycosyl-phosphatidyl inositol-anchored protein, SuSy: sucrose synthase, PME: pectin methylesterase, PAE: pectin acetylesterase, PLL: pectin-lyase like, XTH: xyloglucan endotransglucosylase/ hydrolase, β-gal: beta-galactosidase, β-xyl: beta-D-xylosidase, β-glu: beta-glucosidase, α-glu: alpha-glucosidase, GH: glycosylhydrolase, GT: glycosyltransferase, EXP: expansin. Among these responses were the early activation of certain Transcription factors (TFs) known to be associated with susceptibility and a suppression of other TFs that play a role in defense

Summary

Introduction

The small grass species Brachypodium distachyon (Bd hereafter) has been extensively explored as a useful functional genomic model for grasses[1] This genome offers advantages such as small size (diploid), short generation time, availability of vast genetic and genomic resources (T-DNA insertion mutant lines), and amenability to transformation[1,2]. Further functional analyses of these defense proteins through supplementation and/or mutational approaches are challenging due to the complexity of the wheat genome, and limited genetic and genomic resources This necessitates the use of model systems, such as Bd, which displays nonhost Hessian fly resistance, to undertake downstream functional studies. Bd and wheat diverged from a common ancestor very recently, and share highly conserved sequence homology and gene synteny[24]

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