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Initial ingestion of CMV-infected plants reduces subsequent aphid performance

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Abstract

The tritrophic interactions among plant virus, host plants, and insect vectors directly influence the natural ecosystem, which, in turn, has tremendous practical implications in the sustainable pest control strategies. Cucumber mosaic virus (CMV), transmitted by aphids in a non-persistent manner, causes severe damage in diverse crops worldwide. There is a wealth of information on the initial round of interactions within this tritrophic system. However, knowledge on the subsequent round of interactions is very limited. In this research, we focused on their interactions among Nicotiana tabacum cv. Samsum plants, CMV, and green peach aphids, Myzus persicae specifically after the initial round of aphid feeding on CMV-infected plants. Our results show that initial aphid feeding on CMV-infected plants reduces the fitness of the subsequent aphids. The reproduction capacity, longevity, and survival rate of M. persicae are reduced on CMV-infected plants, previously foraged by M. persicae. Furthermore, the initial aphid feeding on CMV-infected plants induce gene expression involved in the salicylic acid (SA) signaling pathway and suppresses the expression of downstream genes associated with jasmonic acid (JA) signaling pathway. Besides, plant chlorophyll content and nitrogen source are reduced on those CMV-infected plants, previously foraged by aphids. The negative impacts on the fitness and performance of the subsequent aphids may have significant implications in virus transmission, distribution, and epidemiology.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 31872932, 31571981), the National Key R&D Program of China (2018YFE0112600), the Agriculture Research System of China (CARS-23-D-02), the National Agricultural Outstanding Talent Program ([2015]62), and the Hunan Natural Science Foundation (2019JJ30014).

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Author notes

  1. Xiao-bin Shi and Jun Deng are equal contributors.

Authors and Affiliations

  1. Key Laboratory of Integrated Management of the Pests and Diseases on Horticultural Crops in Hunan Province, Institute of Plant Protection, Hunan Academy of Agricultural Sciences, No. 798 Yuanda Road, Rurong District, Changsha, 410125, China

    Xiao-bin Shi, Zhuo Zhang, Shuo Yan, Li-min Zheng, Shu-e Sun, Yang Gao, De-yong Zhang & Yong Liu

  2. People’s Government Office of Hunan Province, Changsha, 410125, China

    Jun Deng

  3. Department of Entomology, University of Kentucky, Lexington, KY, 40546, USA

    Xu-guo Zhou

Authors
  1. Xiao-bin Shi
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  4. Shuo Yan
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  9. De-yong Zhang
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  10. Yong Liu
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Contributions

XBS, DYZ, and YL designed the experiment. XBS and SY carried the experimental work. JD, ZZ, LMZ, SES, YG, and XGZ contributed reagents/materials. XBS wrote the paper.

Corresponding authors

Correspondence to De-yong Zhang or Yong Liu.

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Shi, Xb., Deng, J., Zhang, Z. et al. Initial ingestion of CMV-infected plants reduces subsequent aphid performance. Arthropod-Plant Interactions 15, 153–160 (2021). https://doi.org/10.1007/s11829-021-09804-w

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  • DOI: https://doi.org/10.1007/s11829-021-09804-w

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