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Virus-induced changes in host plant phenotype cue behavioral changes in Aphis glycines that enhance acquisition and transmission of soybean mosaic virus

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Abstract

Vector-borne viruses can modify the phenotype of their host plants to manipulate the behavior of their vectors and maximize their dissemination. The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a primary vector of soybean mosaic virus (SMV), a non-persistent potyvirus that is a serious disease of soybean. We investigated mechanisms by which SMV changes A. glycines feeding and dispersal behavior via virus-induced modifications of plant phenotype. These changes affect gustatory, visual and olfactory cues that alter the behavior of both viruliferous and virus-free aphids to enhance virus acquisition and transmission. SMV-infected soybean seedlings exhibited up-regulation of the amino acids threonine and tyrosine which rendered viruliferous aphids more restless and prone to dispersal. Whereas dispersing viruliferous A. glycines preferred to settle and feed on virus-free soybean seedlings, virus-free aphids preferred SMV-infected seedlings. Volatile cues emanating from SMV-infected seedlings, primarily up-regulated methyl salicylate and down-regulated (Z)-3-hexen-1-ol, were implicated in repulsion of viruliferous aphids, whereas the mottled yellow coloration of SMV-infected seedlings was a visual attractant for aphids regardless of virus status. Our results reveal how a non-persistent virus uses multimodal 'push and pull' mechanisms to manipulate vector behavior for its own benefit, and suggests new avenues for exploring the mechanisms of altered behavior in viruliferous aphids.

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Acknowledgements

This research was supported by National Natural Science Foundation of China (grant 31972278) for Zhen Li, and also supported by the General Project of Science and Technology Plan of Beijing Municipal Education Commission (KM202212448003) and the National Natural Science Foundation of China (grant 32001571) for Le Gao. We would like to thank Pro. Haijian Zhi and Dr. Kai Li from the Nanjing Agricultural University for providing the soybean cv. Nannong 1138-2 and SMV strain SC7.

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Authors and Affiliations

  1. Department of Entomology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Yuanmingyuan West Road, Beijing, China

    Haibo Fang, Haowei Chen, Xiaoxia Liu, Songdou Zhang & Zhen Li

  2. Department of Horticulture, Beijing Vocational College of Agriculture, Beijing, China

    Le Gao

  3. Department of Entomology, Kansas State University, Agricultural Research Center-Hays, Hays, KS, USA

    J. P. Michaud

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  1. Haibo Fang
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  2. Le Gao
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  3. J. P. Michaud
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Correspondence to Zhen Li.

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10340_2023_1718_MOESM1_ESM.tif

Relative expression levels of the SMV coat protein (cp) in A. glycines at various times after feeding on SMV-infected soybean plants (A), and in various body parts (B). Columns bearing different letters were significantly different (one-way ANOVA followed by Fisher′s LSD (α= 0.05) (TIF 10261 kb)

10340_2023_1718_MOESM2_ESM.tif

Percentages of viruliferous A. glycines fourth instars remaining on SMV-infected leaf discs (A), or seedlings (B) at different times post-release. *, Log-rank test, P < 0.05 (TIF 8184 kb)

10340_2023_1718_MOESM3_ESM.tif

Schematic diagram of the experimental procedure for choice tests in which fourth instar A. glycines were provided a choice between either SMV-infected or uninfected leaf discs (A), or soybean seedlings (B). (TIF 23577 kb)

10340_2023_1718_MOESM4_ESM.tif

Schematic diagram of the experimental procedure for choice tests in which fourth instar A. glycines were provided a choice between either green or mottled yellow paper sections (TIF 8335 kb)

10340_2023_1718_MOESM5_ESM.tif

Schematic diagram of the experimental procedure in which A. glycines were fed artificial diets presented in a sachet of parafilm (TIF 14052 kb)

10340_2023_1718_MOESM6_ESM.tif

Schematic diagram of the apparatus used for EPG recording of A. glycines feeding behavior, with an example of a feeding observation and expanded close-ups of the various behaviors distinguished: non penetration waves (np), potential drops (pd), waveform C, and waveform E (TIF 16023 kb)

10340_2023_1718_MOESM7_ESM.tif

Schematic diagram of the Petri dish arena in which A. glycines were tested for response to various VOCs presented on balls of cotton placed above soybean leaf discs (TIF 11911 kb)

10340_2023_1718_MOESM8_ESM.tif

Mean (±SE) durations of np waveforms (A), number of potential drops (B), durations of C waveforms (C), and durations of E waveforms (D) when virus-free A. glycines fed on SMV-infected or uninfected soybean seedlings. *, Student′s t-test, P < 0.05. (TIF 20088 kb)

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Fang, H., Gao, L., Michaud, J.P. et al. Virus-induced changes in host plant phenotype cue behavioral changes in Aphis glycines that enhance acquisition and transmission of soybean mosaic virus. J Pest Sci (2024). https://doi.org/10.1007/s10340-023-01718-1

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