Contrasting effects of necrotrophic and biotrophic plant pathogens on the aphid Aphis fabae

Abstract

Phytophagous insects have to contend with a wide variation in food quality brought about by a variety of factors intrinsic and extrinsic to the plant. One of the most important factors is infection by plant pathogenic fungi. Necrotrophic and biotrophic plant pathogenic fungi may have contrasting effects on insect herbivores due to their different infection mechanisms and induction of different resistance pathways, although this has been little studied and there has been no study of their combined effect. We studied the effect of the biotrophic rust fungus Uromyces viciae‐fabae (Pers.) Schroet (Basidiomycota: Uredinales: Pucciniaceae) and the necrotrophic fungus Botrytis cinerea Pers. (Ascomycota: Helotiales: Sclerotiniaceae) singly and together on the performance of the aphid Aphis fabae Scopoli (Hemiptera: Aphididae) on Vicia faba (L.) (Fabaceae). Alone, botrytis had an inhibitory effect on individual A. fabae development, survival, and fecundity, whereas rust infection consistently enhanced individual aphids' performance. These effects varied in linear relation to lesion or pustule density. However, whole‐plant infection by either pathogen resulted in a smaller aphid population of smaller aphids than on uninfected plants, indicating a lowering of aphid carrying capacity with infection. When both fungi were applied simultaneously to a leaf they generally cancelled the effect of each other out, resulting in most performance parameters being similar to the controls, although fecundity was reduced. However, sequential plant infection (pathogens applied 5 days apart) led to a 70% decrease in fecundity and 50% reduction in intrinsic rate of increase. The application of rust before botrytis had a greater inhibitory effect on aphids than applying botrytis before rust. Rust infection increased leaf total nitrogen concentration by 30%, whereas infection by botrytis with or without rust led to a 38% decrease. The aphids' responses to the two plant pathogens individually is consistent with the alteration in plant nutrient content by infection and also the induction of different plant defence pathways and the possible cross‐talk between them. This is the first demonstration of the complex effects of the dual infection of a plant by contrasting pathogens on insect herbivores.

Fungi reduce preference and performance of insect herbivores on challenged plants

“…Current thinking often states that while the pathway involving salicylic acid (SA) is usually induced by and effective against biotrophic pathogens and sucking herbivores (Ali and Agrawal , Thaler et al. , Al‐Naemi and Hatcher ), necrotrophic pathogens and chewing herbivores principally activate and negatively respond to the jasmonic acid (JA) pathway (Ali and Agrawal , Thaler et al. ).…”

“…, Ali and Agrawal , Thaler et al. , Al‐Naemi and Hatcher ). Given these specificities, we predict that the response of herbivores to plant infection by fungi will depend interactively on fungus lifestyle and herbivore feeding guild, with stronger negative effects of necrotrophic fungi on chewing than on sap feeding insects, but conversely more negative effects of biotrophic fungi on sap feeding insects.…”

Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra

“…Moreover, pathogen effects on plant resistance to insects will depend on the biology of the herbivore, e.g., whether it is a phloem feeder or a chewing larva [19]. For example, the necrotrophic pathogen Botrytis cinerea inhibited the development, fecundity and survival rate of the aphid Aphis fabae in Vicia faba, whereas the biotrophic fungus Uromyces viciae-fabae enhanced aphid performance [21]. Most interestingly, the effect of combined B. cinerea and U. viciae-fabae stress on aphid performance seemed to fluctuate depending on the order of infection [21].…”

“…For example, the necrotrophic pathogen Botrytis cinerea inhibited the development, fecundity and survival rate of the aphid Aphis fabae in Vicia faba, whereas the biotrophic fungus Uromyces viciae-fabae enhanced aphid performance [21]. Most interestingly, the effect of combined B. cinerea and U. viciae-fabae stress on aphid performance seemed to fluctuate depending on the order of infection [21]. In contrast, B. cinerea pretreatment had no significant effect on further performance of Pieris rapae caterpillars in Arabidopsis [22].…”

Sharing a Host Plant (Wheat [Triticum aestivum]) Increases the Fitness of Fusarium graminearum and the Severity of Fusarium Head Blight but Reduces the Fitness of Grain Aphids (Sitobion avenae)

“…The interactions of phytopathogenic fungi and insect herbivores on shared host plants can have a variety of outcomes (10). It has been hypothesized that necrotrophs, such as F. graminearum (11), consistently reduce the fitness of insects feeding on the infected host, although there is evidence contradicting this claim (12,13). It has also been shown that insect herbivory of hosts indirectly causes changes to plant chemistry, biochemistry, physiology, and growth (14) in such a way as to alter the host's capacity to withstand secondary infection.…”