Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization

Abstract

Soybean aphids (Aphis glycines Matsumura) are specialized insects that feed on soybean (Glycine max) phloem sap. Transcriptome analyses have shown that resistant soybean plants mount a fast response that limits aphid feeding and population growth. Conversely, defense responses in susceptible plants are slower and it is hypothesized that aphids block effective defenses in the compatible interaction. Unlike other pests, aphids can colonize plants for long periods of time; yet the effect on the plant transcriptome after long-term aphid feeding has not been analyzed for any plant–aphid interaction. We analyzed the susceptible and resistant (Rag1) transcriptome response to aphid feeding in soybean plants colonized by aphids (biotype 1) for 21 days. We found a reduced resistant response and a low level of aphid growth on Rag1 plants, while susceptible plants showed a strong response consistent with pattern-triggered immunity. GO-term analyses identified chitin regulation as one of the most overrepresented classes of genes, suggesting that chitin could be one of the hemipteran-associated molecular pattern that triggers this defense response. Transcriptome analyses also indicated the phenylpropanoid pathway, specifically isoflavonoid biosynthesis, was induced in susceptible plants in response to long-term aphid feeding. Metabolite analyses corroborated this finding. Aphid-treated susceptible plants accumulated daidzein, formononetin, and genistein, although glyceollins were present at low levels in these plants. Choice experiments indicated that daidzein may have a deterrent effect on aphid feeding. Mass spectrometry imaging showed these isoflavones accumulate likely in the mesophyll cells or epidermis and are absent from the vasculature, suggesting that isoflavones are part of a non-phloem defense response that can reduce aphid feeding. While it is likely that aphid can initially block defense responses in compatible interactions, it appears that susceptible soybean plants can eventually mount an effective defense in response to long-term soybean aphid colonization.

Characterization of Induced Susceptibility Effects of Soybean Aphid on Soybean

“…The differential expression of ferritin as a resistance response has been shown in previous studies as a part of constitutive resistance mechanism in soybean-soybean aphid interactions [18,21,67]. Upregulation of ferritins in resistant plants can limit the availability of iron to the insect [67]. At day 11, four TNL genes, four homologs of WRKY40, one homolog of WRKY67, four senescence-related genes, four UDPglucosyltransferases, two myo-inositol oxygenases, five glutathione S-transferases were uniquely upregulated in the resistant cultivar when treated with biotype 2 as an inducer.…”

“…Another gene that encodes Ferritin/ribonucleotide reductase-like family protein was upregulated at day 1 response. The differential expression of ferritin as a resistance response has been shown in previous studies as a part of constitutive resistance mechanism in soybean-soybean aphid interactions [18,21,67]. Upregulation of ferritins in resistant plants can limit the availability of iron to the insect [67].…”

“…These are the major components of the PTI program of defense mechanism. Such an effect in which significant induction of defense programs in susceptible cultivar aphid-susceptible SD01-76R when infested with soybean aphid for 21 days [67]. The DEGs in resistant cultivar were enriched for Photosynthesis, Glutathione metabolism, Cutin, suberine and wax biosynthesis, Cysteine and methionine metabolism, and Flavonoid biosynthesis.…”

Genome scan detection of selective sweeps among biotypes of the soybean aphid, Aphis glycines, with differing virulence to resistance to A. glycines (Rag) traits in soybean, Glycine max

“…Glucosinolates also can act as feeding stimulants for specialist herbivores, such as the cabbage aphid, B. brassicae (Gabrys et al, 1997), or be sequestered and used by insects for their own defense against predators (Müller et al, 2001;Jones et al, 2002;Kazana et al, 2007). An analogous system in G. max involves the cleavage of isoflavonoid compounds by β-glucosidases could play a role in host plant specialization or antibiosis and antixenosis-based defenses against A. glycines (Meng et al, 2011;Hohenstein et al, 2019), but this requires additional investigation.…”

The Cytotoxic Effect of Genistein, a Soybean Isoflavone, against Cultured Tribolium Cells

“…Secondary metabolites, such as flavonoids and isoflavonoids, especially isoflavones, saponins, and phenolic acids, play important roles in plant-insect interactions as defensive agents [14][15][16][17]. High doses of two polyphenolic flavonoids, luteolin and genistein, have been shown to repulse Acyrthosiphon pisum due to their antifeedant and toxic effects [18,19].…”