Powdery mildew suppresses herbivore-induced plant volatiles and interferes with parasitoid attraction in Brassica rapa

Authors: DESURMONT, GAYLORD - European Biological Control Laboratory (EBCL); XU, HAO - Neuchatel University - Switzerland; TURLINGS, TED - Neuchatel University - Switzerland

Submitted to: Plant Cell and Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/21/2016
Publication Date: 8/15/2016
Citation: Desurmont, G., Xu, H., Turlings, T.C. 2016. Powdery mildew suppresses herbivore-induced plant volatiles and interferes with parasitoid attraction in Brassica rapa. Plant Cell and Environment. Vol 39, Pages 1920-1927. DOI: 10.1111/pce.12752.

Interpretive Summary: Powdery mildew is a major pathogen of many plant species, including many crops, and the imported cabbageworm (Pieris brassicae) is an important insect pest of cole crops. However, it is not known how powdery mildew interacts with imported cabbageworm or its insect parasite (Cotesia glomerata), which is used as a biological control agent. We measured the release of volatile organic compounds by Chinese cabbage plants with or without powdery mildew and/or cabbageworm, and tested the attractiveness of these different odor combinations to female parasites. The results show that powdery mildew decreases plant attractiveness to the parasite, which is because plants with powdery mildew plus cabbageworms emit less odors than plants with only cabbageworms. Consequently, caterpillars feeding on plants infected by powdery mildew may be less detectable by this biological control agent. Furthermore, powdery mildew reduced survival of the parasite larvae, but not of cabbageworm larvae. Thus powdery mildew not only directly damages Chinese cabbage, but it also probably interferes with biological control of the cabbageworm, likely increasing damage to the crop by cabbageworm.

Technical Abstract: The co-occurrence of different antagonists on a plant can greatly affect infochemicals with ecological consequences for higher trophic levels. Here we investigated how the presence of a plant pathogen, the powdery mildew Erysiphe cruciferarum, on Brassica rapa affects 1) plant volatiles emitted in response to damage by a specialist herbivore, Pieris brassicae, 2) the attraction of the parasitic wasp Cotesia glomerata, and 3) the performance of P. brassicae and C. glomerata. Plant volatiles were significantly induced by herbivory in both healthy and mildew-infected plants, but were 41% lower for mildew-infected plants compared to healthy plants. Parasitoids strongly preferred Pieris-infested plants to dually-infested (Pieris + mildew) plants, and preferred dually-infested plants over only mildew-infected plants. The performance of P. brassicae was unaffected by powdery mildew, but C. glomerata cocoon mass was reduced when parasitized caterpillars developed on mildew-infected plants. Thus, avoidance of mildew-infested plants may be adaptive for C. glomerata parasitoids, whereas P. brassicae caterpillars may suffer less parasitism on mildew-infected plants in nature. From a pest management standpoint, the concurrent presence of multiple plant antagonists may affect the efficiency of specific natural enemies, which may in turn have a negative impact on the regulation of pest populations.