A large-scale multiomics analysis of wheat stem solidness and the wheat stem sawfly feeding response, and syntenic associations in barley, Brachypodium, and rice

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.Electronic supplementary materialThe online version of this article (10.1007/s10142-017-0585-5) contains supplementary material, which is available to authorized users.

Antixenosis, Antibiosis, and Potential Yield Compensatory Response in Barley Cultivars Exposed to Wheat Stem Sawfly (Hymenoptera: Cephidae) Under Field Conditions

“…Tricetin activates lignin biosynthesis in secondary cell wall production ( Moheb et al 2013 ). However, C. cinctus feeding downregulated the synthesis of these metabolites, perhaps supporting the idea that these larvae disrupt signals and limit subsequent synthesis of these metabolites ( Biyiklioglu et al 2018 ). Cultivated barley has lost the biosynthetic capability to produce DIMBOA ( Nomura et al 2002 , Grun et al 2005 ), but there are other groups of compounds, such as flavonoids and alkaloids that may be synthesized to ward off insect pests ( Balmer et al 2013 ).…”

“…One major factor causing larval mortality is host plant antibiosis in barley and certain wheat cultivars ( Wallace and McNeal 1966 , Buteler et al 2015 , Varella et al 2018 ). Some defense related secondary metabolites, such as DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one), tricetin, and lignin are downregulated in C. cinctus -infested wheat stems ( Biyiklioglu et al 2018 ), indicating that these compounds are synthesized in response to and have a negative effect on C. cinctus . Although cultivated barley has lost the ability to biosynthesize DIMBOA ( Nomura et al 2002 , Grun et al 2005 ), other groups of defensive compounds, such as benzoxazinoids, flavonoids, and alkaloids can be synthesized to ward off insect pests ( Balmer et al 2013 ).…”

“…Although host plant resistance that is due to the presence of solid pith in the stem can be relatively successful for reducing stem cutting in wheat ( Beres et al 2013 , Wu et al 2013 , Talbert et al 2014 , Carcamo et al 2016 , Varella et al 2016 , Adhikari et al 2018 ), solid stems may be compromised by environmental effects on pith expression ( Beres et al 2009 , 2017 ) and relative expression of the trait in different backgrounds ( Cook et al 2019 , Varella et al 2019 , Bainsla et al 2020 ). In addition to stem solidness, other defense-related metabolites, such as DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one), tricetin, and lignin are downregulated in C. cinctus -infested wheat stems when compared with uninfested stems ( Biyiklioglu et al 2018 ). Among these identified compounds, DIMBOA is well investigated as a toxin from cereals for different classes of herbivores, notably aphids and caterpillars ( Martos et al 1992 , Erb et al 2009 , Niemeyer 2009 ).…”

MicroRNAome Profile of Euphorbia kansui in Response to Methyl Jasmonate

“…Some studies have found that miRNAs are involved in the drought stress of wheat [30,31] or dehydration stress in Triticeae [32]. A large-scale multiomics analysis showed that miRNAs involved the potential regulatory in wheat stem sawfly [33]. Shen et al reported that some miRNAs of Oryza sativa responded to a drought, salt and the cold [34].…”

Phenology and Dispersal of the Wheat Stem Sawfly (Hymenoptera: Cephidae) Into Winter Wheat Fields in Nebraska

“…Border modifications or the use of seed blends to limit the amount of solid stem wheat planted have had some success in limiting wheat stem sawfly damage; however, planting the entire crop to a solid stem variety remains the best option ( Beres et al 2009 ). Recent molecular investigations into barley’s resistance to wheat stem sawfly larvae and the characterization of wheat’s response to wheat stem sawfly larval feeding have the potential to create new mechanisms of plant resistance against the wheat stem sawfly ( Biyiklioglu et al 2018 , Varella et al 2018 ).…”