Untargeted Metabolomics Approach Reveals Differences in Host Plant Chemistry Before and After Infestation With Different Pea Aphid Host Races

Abstract

The pea aphid ( Acyrthosiphon pisum ), a phloem-sucking insect, has undergone a rapid radiation together with the domestication and anthropogenic range expansion of several of its legume host plants. This insect species is a complex of at least 15 genetically different host races that can all develop on the universal host plant Vicia faba . However, each host race is specialized on a particular plant species, such as Medicago sativa , Trifolium pratense , or Pisum sativum , which makes it an attractive model insect to study ecological speciation. Previous work revealed that pea aphid host plants produce a specific phytohormone profile depending on the host plant – host race combination. Native aphid races induce lower defense hormone levels in their host plant than non-native pea aphid races. Whether these changes in hormone levels also lead to changes in other metabolites is still unknown. We used a mass spectrometry-based untargeted metabolomic approach to identify plant chemical compounds that vary among different host plant-host race combinations and might therefore, be involved in pea aphid host race specialization. We found significant differences among the metabolic fingerprints of the four legume species studied prior to aphid infestation, which correlated with aphid performance. After infestation, the metabolic profiles of M. sativa and T. pratense plants infested with their respective native aphid host race were consistently different from profiles after infestation with non-native host races and from uninfested control plants. The metabolic profiles of P. sativum plants infested with their native aphid host race were also different from plants infested with non-native host races, but not different from uninfested control plants. The compounds responsible for these differences were putatively identified as flavonoids, saponins, non-proteinogenic amino acids and peptides among others. As members of these compound classes are known for their activity against insects and aphids in particular, they may be responsible for the differential performance of host races on native vs. non-native host plants. We conclude that the untargeted metabolomic approach is suitable to identify candidate compounds involved in the specificity of pea aphid – host plant interactions.

Changes in Aphid Host Plant Diet Influence the Small-RNA Expression Profiles of Its Obligate Nutritional Symbiont,Buchnera

“…The two A. pisum host plants used in this study are known to vary significantly in essential amino acid profiles (35) and metabolite profiles, including host plant defense compounds (38, 39). Aphid stylectomy experiments have also shown that fava bean and alfalfa have different concentrations of arginine, isoleucine, leucine, lysine, phenylalanine, tryptophan, tyrosine, valine, and histidine, with alfalfa generally having lower concentrations of essential amino acids than fava bean (35).…”

“…When comparing the metabolite profiles among the A. pisum host plants alfalfa, fava bean, pea, and red clover, Sanchez-Arcos et al (38) found that alfalfa plants contain the highest number of unique metabolites, especially compared to that of fava bean plants. Notably, Sanchez-Arcos et al (38) found that saponins, a known A.…”

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.…”

“…The net result of these changes in TF expression levels is the modulation of primary and secondary metabolic pathways, which serve to trigger defense responses to mitigate herbivory. Although several components of defense responses are conserved among multiple plant species, plant genotype, environment, and other factors can lead to variations in the cellular metabolism of the same hosts challenged by insect herbivores ( Coppola et al., 2013 ; Maag et al., 2015a ; Castano-Duque and Luthe, 2018 ; Muneer et al., 2018 ; Sanchez-Arcos et al., 2019 ; Zhao et al., 2019 ). Despite variations in metabolite profiles, certain pathways and compounds produced by these pathways are known to confer protection to plants against biotic stressors.…”

The metabotyping of an East African cassava diversity panel: A core collection for developing biotic stress tolerance in cassava

“…Annotation and characterisation of unknown molecular or chemical features is the bottleneck of untargeted metabolomics studies which limits the discovery of relevant biological markers to a reduced number of overrepresented chemical classes. Phenylpropanoids constitute one of these examples of a recurrent marker of multiple agronomic trait or biological activities with emphasis on chlorogenic acid and flavonoids [35][36][37][38][39][40]. The large-scale nature of untargeted metabolomics studies requires high throughput methods that likely favour the extraction and detection of, for example, phenylpropanoids and underestimate the presence of minor chemical families are likely to be a contributing factor to these outcomes.…”