Root-associated entomopathogenic fungi manipulate host plants to attract herbivorous insects

Belén Cotes,Ondřej Novák,Gunda Thöming,Carol V. Amaya-Gómez,Christian Nansen

doi:10.1038/s41598-020-80123-5

Abstract

Root-associated entomopathogenic fungi (R-AEF) indirectly influence herbivorous insect performance. However, host plant-R-AEF interactions and R-AEF as biological control agents have been studied independently and without much attention to the potential synergy between these functional traits. In this study, we evaluated behavioral responses of cabbage root flies [Delia radicum L. (Diptera: Anthomyiidae)] to a host plant (white cabbage cabbage Brassica oleracea var. capitata f. alba cv. Castello L.) with and without the R-AEF Metarhizium brunneum (Petch). We performed experiments on leaf reflectance, phytohormonal composition and host plant location behavior (behavioral processes that contribute to locating and selecting an adequate host plant in the environment). Compared to control host plants, R-AEF inoculation caused, on one hand, a decrease in reflectance of host plant leaves in the near-infrared portion of the radiometric spectrum and, on the other, an increase in the production of jasmonic, (+)-7-iso-jasmonoyl-l-isoleucine and salicylic acid in certain parts of the host plant. Under both greenhouse and field settings, landing and oviposition by cabbage root fly females were positively affected by R-AEF inoculation of host plants. The fungal-induced change in leaf reflectance may have altered visual cues used by the cabbage root flies in their host plant selection. This is the first study providing evidence for the hypothesis that R-AEF manipulate the suitability of their host plant to attract herbivorous insects.

Highlights

Root-associated entomopathogenic fungi (R-AEF) indirectly influence herbivorous insect performance
We investigated whether R-AEF inoculation affects: (1) phytohormonal composition [jasmonic, (+)-7-iso-jasmonoyl-l-isoleucine and salicylic acid] of host plants, (2) leaf reflectance (Fig. 1d), and (3) host plant location or acceptance behavior of cabbage root flies (Fig. 1e,f)
Both jasmonic acid (JA) and JA-Ile were found in higher amounts in the fungal (R-AEF)-inoculated plants (FIP) compared to non-inoculated plants (NIP) in host plant leaves (Table 1, Fig. 3a,c)

Summary

Introduction

Root-associated entomopathogenic fungi (R-AEF) indirectly influence herbivorous insect performance. The fungal-induced change in leaf reflectance may have altered visual cues used by the cabbage root flies in their host plant selection This is the first study providing evidence for the hypothesis that R-AEF manipulate the suitability of their host plant to attract herbivorous insects. Castello L.) are significantly increased compared to non-inoculated plants To address this hypothesis, we performed greenhouse and field experiments with cabbage root flies host plants with and without the bioinsectide Met[52] Granular (Novozymes Biologicals Inc., Salem, VA) (Fig. 1d–f). We performed greenhouse and field experiments with cabbage root flies host plants with and without the bioinsectide Met[52] Granular (Novozymes Biologicals Inc., Salem, VA) (Fig. 1d–f) This commercial product is the M. anisopliae Strain F52, re-classified as Metarhizium brunneum (Petch). We investigated whether R-AEF inoculation affects: (1) phytohormonal composition [jasmonic, (+)-7-iso-jasmonoyl-l-isoleucine and salicylic acid] of host plants (and relative suitability of host plants for cabbage root flies), (2) leaf reflectance (and visual cues used by cabbage root flies in their host selection) (Fig. 1d), and (3) host plant location or acceptance behavior of cabbage root flies (Fig. 1e,f)

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Discussion

Conclusion