Fungi from the black cutworm Agrotis ipsilon oral secretions mediate plant–insect interactions

Abstract

It is well known that the interactions of insect herbivores and their host plant can be mediated by microbes. Our central hypothesis is that herbivore-associated fungi might directly or indirectly affect plant–insect interactions. In this study, we identified five orally secreted fungi from field-collected black cutworm, Agrotis ipsilon, including Aspergillus parasiticus, Aspergillus niger, Geotrichum candidum, Fusarium subglutinans, and Mucor circinelloides f. lusitanicus. We found that caterpillars inoculated with F. subglutinans or M. circinelloides f. lusitanicus induced higher defense responses in plants, but with different patterns between different plants. These herbivore-induced defense responses reduced the growth of caterpillars. However, direct application of fungi to mechanically wounded tomato did not induce JA-related defense responses. The application of regurgitant from fungi-inoculated or non-inoculated caterpillars, suggested that regurgitant might be responsible for the fungi-mediated defense response in plants against caterpillar attack. Furthermore, both F. subglutinans and M. circinelloides f. lusitanicus benefited caterpillar growth when they fed on detached tomato leaves, but had no influence when caterpillars fed on artificial diet. Our finding suggests that insect-associated fungi could influence plant–insect interactions by indirectly mediating plant defense responses, and directly affecting caterpillar performance on host plants.

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Acknowledgements

This work was supported by the Agricultural and Food Research Initiative Program of United States Department of Agriculture (Grant No. 2017-67013-26596). Xuewei Chen was financially supported by China Scholarship Council (File No. 201706350199).

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Correspondence to Gary W. Felton.

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Supplementary file1 (TIF 1705 kb) Supplemental Fig. 1 The detection of regurgitant using fluorescent dye Alexa 488. A) Fluorescent dye (green) was detected on the edges of the damaged leaves fed by caterpillars which were pretreated with fluorescent dye. B) No fluorescence was detected on the edges of the damaged leaves fed by caterpillars which were not pretreated with fluorescent dye.

Supplementary file2 (TIF 2171 kb) Supplemental Fig. 2 Fungi from regurgitant of fungi-inoculated or non-inoculated caterpillars and fungi from plant tissues fed by fungi-inoculated or non-inoculated caterpillars. Caterpillars were fed with Fusarium subglutinans (FS), or Mucor circinelloides f. lusitanicus (MC), or without fungi (CK).

Supplementary file3 (TIF 711 kb) Supplemental Fig. 3 Polyphenol oxidase (PPO) and trypsin proteinase inhibitor (TPI) activities of plants fed on by Agrotis ipsilon. Plants were damaged by caterpillars which were pretreated with fungal solution of Aspergillus parasiticus (AP), Aspergillus niger (AN), or Geotrichum candidum (GC), or without fungi (CK), and a set of undamaged plants was included as negative control (Untreated). Values are mean ± SEM, different letters indicate significant differences obtained with ANOVA following by LSD test. PPO (F4,37 = 1.760, P = 0.158) and TPI (F4,31 = 10.140, P < 0.001) activities in tomato.

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Chen, X., Peiffer, M., Tan, C. et al. Fungi from the black cutworm Agrotis ipsilon oral secretions mediate plant–insect interactions. Arthropod-Plant Interactions 14, 423–432 (2020). https://doi.org/10.1007/s11829-020-09767-4

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Keywords

  • Oral secretions
  • Fungi
  • Phytobiome
  • Microbiome
  • Induced defenses
  • Plant–herbivore interaction
  • Tomato
  • Maize