Aphid-Responsive Defense Networks in Hybrid Switchgrass

Abstract

Aphid herbivory elicits plant defense-related networks that are influenced by host genetics. Plants of the upland switchgrass (Panicum virgatum) cultivar Summer can be a suitable host for greenbug aphids (Schizaphis graminum; GB), and yellow sugarcane aphids (Sipha flava, YSA), whereas the lowland cultivar Kanlow exhibited multi-species resistance that curtails aphid reproduction. However, stabilized hybrids of Summer (♀) x Kanlow (♂) (SxK) with improved agronomics can be damaged by both aphids. Here, hormone and metabolite analyses, coupled with RNA-Seq analysis of plant transcriptomes, were utilized to delineate defense networks induced by aphid feeding in SxK switchgrass and pinpoint plant transcription factors (TFs), such as WRKYs that potentially regulate these responses. Abscisic acid (ABA) levels were significantly higher in GB infested plants at 5 and 10 days after infestation (DAI). ABA levels were highest at 15DAI in YSA infested plants. Jasmonic acid levels were significantly elevated under GB infestation, while salicylic acid levels were signifi40cantly elevated only at 15 DAI in YSA infested plants. Similarly, levels of several metabolites were altered in common or specifically to each aphid. YSA infestation induced a significant enrichment of flavonoids consistent with an upregulation of many genes associated with flavonoid biosynthesis at 15DAI. Gene co-expression modules that responded singly to either aphid or in common to both aphids were differentiated and linked to specific TFs. Together, these data provide important clues into the interplay of metabolism and transcriptional remodeling accompanying defense responses to aphid herbivory in hybrid switchgrass.

Differential Defense Responses of Upland and Lowland Switchgrass Cultivars to a Cereal Aphid Pest

“…Similar approaches have been used by other researchers to understand plant–aphid interactions [ 55 , 56 , 57 , 58 , 59 , 60 , 61 ]. As examples, Zhang et al [ 56 ] found that GB infestation of wheat increases endogenous reactive oxygen species (ROS) production compared to the non-phytotoxic aphid Sitobion avenae , suggesting a similarity in responses observed in Summer and hybrid switchgrass infested with GB or YSA [ 29 , 30 ]. Phloem-resident mechanisms (other than callose) can also impact aphid and virus responses [ 62 ], although it is unclear if such mechanisms are resident in Kanlow plants [ 4 ].…”

“…Transcriptional and metabolic outcomes upon infestation with GB have been evaluated in Summer switchgrass plants [ 29 ], and those of GB and YSA infestation on Summer and Kanlow switchgrass hybrids [ 30 ]. In both studies, similarities and differences were observed in the defense responses to the different aphids.…”

“…Additionally, GB induced a strong defense response more characteristic of a non-host response, while YSA herbivory was more nuanced, causing a gradual increase in plant defense-related processes over the 15-day time course of the experiment. In both of these studies, several transcription factors (TFs) were identified that were significantly associated with one or more defensive processes [ 29 , 30 ].…”

“…Hybrid switchgrass utilized by Koch and colleagues were from a stabilized population derived from crosses of randomly selected Summer (♀) x Kanlow (♂) plants [ 31 ]. These plants were able to serve as hosts for both GB and YSA [ 30 ], indicating that Kanlow traits regulating GB feeding were suppressed in the hybrids. However, because YSA could infest both Summer and Kanlow plants, it provided a route to investigating different aspects of the defense responses of Kanlow plants to aphid herbivory and simultaneously compare these data with the more permissive host Summer.…”

Redox-Dependent Structural Modification of Nucleoredoxin Triggers Defense Responses against Alternaria brassicicola in Arabidopsis

“…To account for this possibility, several hypotheses have been proposed, including the heterodimerization of JA-responsive TFs with other types of TFs, and the recruitment of other co-regulators that compete to bind to the TFs. To gain a more complete understanding of how JA signaling regulates its diverse metabolic and physiological outputs, it is important to identify novel JA signaling regulators or TFs [26,49].…”