Abstract

In natural ecological systems, plants are often simultaneously attacked by both insects and pathogens, which can affect each other’s performance and the interactions can be extended to higher trophic levels, such as parasitoids. The English grain aphid (Sitobion avenae) and powdery mildew (Blumeria graminis f. sp. tritici) are two common antagonists that pose a serious threat to wheat production. Numerous studies have investigated the effect of a single factor (insect or pathogen) on wheat production. However, investigation on the interactions among insect pests, pathogens, and parasitoids within the wheat crop system are rare. Furthermore, the influence of the fungicide, propiconazole, has been found to imitate the natural ecosystem. Therefore, this study investigated the effects of B. graminis on the biological performance of grain aphids and the orientation behavior of its endoparasitic wasp Aphidius gifuensis in the wheat system. Our findings indicated that B. graminis infection suppressed the feeding behavior, adult and nymph weight, and fecundity and prolonged the developmental time of S. avenae. We found that wheat host plants had decreased proportions of essential amino acids and higher content of sucrose following aggravated B. graminis infection. The contents of Pro and Gln increased in the wheat plant tissues after B. graminis infection. In addition, B. graminis infection elicited immune responses in wheat: increase in the expression of defense genes, content of total phenolic compounds, and activity of three related antioxidant enzymes. Moreover, co-infection of B. graminis and S. avenae increased the attraction to A. gifuensis compare to that after infestation with aphids alone. In conclusion, our results indicated that B. graminis infection adversely affected the performance of S. avenae in wheat through restricted nutrition and induced defense response. Furthermore, the preference of parasitoids in such an interactive environment might provide an important basis for pest management control.

Highlights

  • In nature, herbivorous insects are known to attack host plants along with a variety of other species, including both pathogens and natural enemies (Stout et al, 2006; Tack et al, 2013; Franco et al, 2017)

  • Performance parameters of the grain aphid varied among treatments but were generally worse on Mildew and mildew plus propiconazole (M+P) treatments compared to that for other treatments (Figure 2)

  • The development time of each instar remained unchanged for aphids regardless of host plant treatment, but the total development time was significantly lower for aphids on control leaves than on other treatments (F3,96 = 8.447, P < 0.001; Figure 2A)

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Summary

Introduction

Herbivorous insects are known to attack host plants along with a variety of other species, including both pathogens and natural enemies (Stout et al, 2006; Tack et al, 2013; Franco et al, 2017). Plants serve as shared hosts allowing interactions among these species. Insects and pathogens have multiple interactions that might result in altered host plant quality and plant defense responses (Biere and Tack, 2013; Mauck et al, 2014). Herbivory by an insect pest primes the host plant immune response, making the plant resistant to future pathogen infection. Feeding by the white-backed planthopper, Sogatella furcifera, induced host plant resistance to rice blast caused by Magnaporthe grisea (Kanno and Fujita, 2003; Kanno et al, 2005). Another study suggested physiological changes in cotton seedlings caused by previous exposure to spider mites, Tetranychus urticae, which reduced the probability of infection and severity of symptoms caused by the wilt fungus Verticillium dahlia (Karban et al, 1987)

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