Abstract

The wheat stem sawfly (WSS), Cephus cinctus Norton (Hymenoptera: Cephidae), is an important pest of wheat and other cereals, threatening the quality and quantity of grain production. WSS larvae feed and develop inside the stem where they are protected from the external environment; therefore, pest management strategies primarily rely on host plant resistance. A major locus on the long arm of wheat chromosome 3B underlies most of the variation in stem solidness; however, the impact of stem solidness on WSS feeding has not been completely characterized. Here, we used a multiomics approach to examine the response to WSS in both solid- and semi-solid-stemmed wheat varieties. The combined transcriptomic, proteomic, and metabolomic data revealed that two important molecular pathways, phenylpropanoid and phosphate pentose, are involved in plant defense against WSS. We also detected a general downregulation of several key defense transcripts, including those encoding secondary metabolites such as DIMBOA, tricetin, and lignin, which suggested that the WSS larva might interfere with plant defense. We comparatively analyzed the stem solidness genomic region known to be associated with WSS tolerance in wild emmer, durum, and bread wheats, and described syntenic regions in the close relatives barley, Brachypodium, and rice. Additionally, microRNAs identified from the same genomic region revealed potential regulatory pathways associated with the WSS response. We propose a model outlining the molecular responses of the WSS–wheat interactions. These findings provide insight into the link between stem solidness and WSS feeding at the molecular level.

Highlights

  • Wheat (Triticum aestivum) is a staple food for 30% of the global population and is the most extensively grown crop in the world, ranking third in terms of production with an annual output of over 700 million tons

  • To explore the physical locations of the genetic determinants of stem solidness, including the Qss.msub-3BL locus, previously published molecular markers linked to this trait (Nilsen et al 2017) were mapped to the chromosome 3B pseudomolecules of T. turgidum ssp. dicoccoides genotype Zavitan, T. turgidum ssp. durum genotype MWG, and T. aestivum cv

  • Wild emmer wheat is a close wild relative of durum wheat, as both diverged from the common ancestor T. turgidum, the tetraploid progenitor of T. aestivum

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Summary

Introduction

Wheat (Triticum aestivum) is a staple food for 30% of the global population and is the most extensively grown crop in the world, ranking third in terms of production with an annual output of over 700 million tons (http://faostat3.fao.org/). Female adults, which live for 7–10 days, lay their eggs inside the wheat stem, and the resulting larvae begin feeding on the parenchyma and vascular tissues. Following the fifth instar stage, the larvae move down the inside of the stem and cut the stem at the base. The toppled stem provides shelter for the larvae, allowing them to overwinter during the obligatory diapause stage (Beres et al 2011a). Heavy WSS infestation can cause up to 95% of the stems to lodge due to this stem-cutting behavior (Beres et al 2011b). Since the larvae are protected inside the stems and the adult flies do not feed, chemical control strategies against WSS are ineffective. WSS management strategies have conventionally relied on host plant resistance (Beres et al 2011b)

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