Effects of sugarcane aphid herbivory on transcriptional responses of resistant and susceptible sorghum

Abstract

BackgroundSugarcane aphid (Melanaphis sacchari) outbreaks in sorghum that were first reported in 2013 are now the most significant threat to this crop in all major sorghum production areas in the U.S. The outcomes of interactions between sugarcane aphid and sorghum and thus the severity of the outbreaks depend on sorghum genotype and potentially also on the phenology of sorghum. Mechanisms underlying these interactions are not known, however. Thus, the goal of this research was to characterize transcriptional changes in a commercially available resistant and a susceptible genotype of sorghum at 2- and 6-wk post-emergence exposed to M. sacchari herbivory. The effects of sorghum age and genotype on the daily change in aphid densities were also evaluated in separate greenhouse experiments.ResultsA higher number of diffentially expressed genes (DEGs) was recovered from the 2-wk plants exposed to aphid herbivory compared to the 6-wk plants across genotypes. Further, gene ontology and pathway analysis indicated a suite of transcriptional changes in the resistant genotype that were weak or absent in the susceptible sorghum. Specifically, the aphid-resistant genotype exposed to M. sacchari up-regulated several genes involved in defense, which was particularly evident in the 2-wk plants that showed the most robust transcriptional responses. These transcriptional changes in the younger resistant sorghum were characterized by induction of hormone-signaling pathways, pathways coding for secondary metabolites, glutathion metabolism, and plant-pathogen interaction. Furthermore, the 2-wk resistant plants appeared to compensate for the effects of oxidative stress induced by sugarcane aphid herbivory with elevated expression of genes involved in detoxification. These transcriptional responses were reflected in the aphid population growth, which was significantly faster in the susceptible and older sorghum than in the resistant and younger plants.ConclusionThis experiment provided the first insights into molecular mechanisms underlying lower population growth of M. sacchari on the resistant sorghum genotype. Further, it appears that the younger resistant sorghum was able to mount a robust defense response following aphid herbivory, which was much weaker in the older sorghum. Several pathways and specific genes provide specific clues into the mechanisms underlying host plant resistance to this invasive insect.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5095-x) contains supplementary material, which is available to authorized users.

Constitutive H2O2 is involved in sorghum defense against aphids

“…It has been reported that during sorghum-aphid interactions a higher number of DEGs and expression of a higher number of defense-related genes have been detected in the resistant genotype in response to aphid herbivory than in the susceptible genotype (Kiani and Szczepaniec 2018). However, in this study, only 32% DEGs in ROS scavenging had more changes in resistant HN16 than that in susceptible asm1 and has been deduced to play a part directly in the H 2 O 2 elimination.…”

Plant Genes Benefitting Aphids—Potential for Exploitation in Resistance Breeding

“…Since aphids, in general, have been shown to be more sensitive to plant defense involving the JA signaling pathway, SA induction is considered to be a way for aphids to deceive the plant because cross-talk between hormonal pathways hinders the SA-induced plant to fully induce the JA and ET pathways (Thompson and Goggin 2006; De Vos et al, 2007; Goggin, 2007; Walling, 2008). Indications of this SA–JA antagonism have been found in the global expression studies of Acyrthosiphon pisum Harris on susceptible barrel medic (Sun et al, 2018), Myzus persicae Sulzer on potato (Alvarez et al, 2014), Schizaphis graminum Rondani on susceptible sorghum (Zhu-Salzman et al, 2004), Melanaphis sacchari Zehntner on sorghum (Kiani and Szczepaniec, 2018), Macrosiphum euphorbiae Thomas on susceptible tomato (Coppola et al, 2013), and Sitobion avenae Fabricius on susceptible wheat (Ferry et al, 2011). However, in the study by Bricchi et al (2012), there was no indication of SA-dependant crosstalk and yet many genes in the JA pathway were downregulated by M. persicae on susceptible Arabidopsis at the early sampling of 5 h after aphid infestation.…”

Aphid-Responsive Defense Networks in Hybrid Switchgrass

“…Several omics strategies alone or in combination have been used to evaluate plant-aphid, and plant-insect interactions [for example: ( Wu and Baldwin, 2010 ; Maag et al., 2015b ; Tzin et al., 2015 ; Zhou et al., 2015 ; Wozniak et al., 2017 ; Kiani and Szczepaniec, 2018 ; Erb and Reymond, 2019 ; Nalam et al., 2019 ; Sanchez-Arcos et al., 2019 ; He et al., 2020 ; Zhang et al., 2020 ; Zogli et al., 2020 )]. In general, these studies have shown extensive changes in the transcriptomes and metabolomes upon insect herbivory.…”