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)

Abstract

bWe hypothesized that interactions between fusarium head blight-causing pathogens and herbivores are likely to occur because they share wheat as a host plant. Our aim was to investigate the interactions between the grain aphid, Sitobion avenae, and Fusarium graminearum on wheat ears and the role that host volatile chemicals play in mediating interactions. Wheat ears were treated with aphids and F. graminearum inoculum, together or separately, and disease progress was monitored by visual assessment and by quantification of pathogen DNA and mycotoxins. Plants exposed to both aphids and F. graminearum inoculum showed accelerated disease progression, with a 2-fold increase in disease severity and 5-fold increase in mycotoxin accumulation over those of plants treated only with F. graminearum. Furthermore, the longer the period of aphid colonization of the host prior to inoculation with F. graminearum, the greater the amount of pathogen DNA that accumulated. Headspace samples of plant volatiles were collected for use in aphid olfactometer assays and were analyzed by gas chromatography-mass spectrometry (GC-MS) and GC-coupled electroantennography. Disease-induced plant volatiles were repellent to aphids, and 2-pentadecanone was the key semiochemical underpinning the repellent effect. We measured aphid survival and fecundity on infected wheat ears and found that both were markedly reduced on infected ears. Thus, interactions between F. graminearum and grain aphids on wheat ears benefit the pathogen at the expense of the pest. Our findings have important consequences for disease epidemiology, because we show increased spread and development of host disease, together with greater disease severity and greater accumulation of pathogen DNA and mycotoxin, when aphids are present. P lant interactions with pathogens or insects are usually studied in isolation, even though plants are exposed to both in the field. It is likely that organisms that share the same host plant can alter its condition and thereby interact with each other. Although Fusarium pathogens and grain aphids cause substantial damage to wheat and coincide, little is known about interactions between these species.Fusarium head blight (FHB) is a disease of small grain cereals that occurs globally and is caused by a complex of species from the genera Fusarium and Microdochium (1, 2). The most aggressive species causing FHB is Fusarium graminearum, a potent producer of the mycotoxin deoxynivalenol (DON), which is harmful to human and animal health if consumed (3). European legislation has set the acceptable limit of DON in grain marketed for human consumption at 1,250 g kg Ϫ1 (4) in unprocessed cereals. Consequently, FHB epidemics result in large economic losses from the combined effects of reductions in yield, increased mycotoxin contamination, and reduced quality and marketability of the crop (5).In the spring, ascospores and/or conidia of Fusarium graminearum are released from crop residues and are spread by wind or rainsplash. Wheat is most susceptible to FHB du...

Aphid Infestation Increases Fusarium langsethiae and T-2 and HT-2 Mycotoxins in Wheat

“…The amount of T-2 plus HT-2 in 1 of the 10 aphid-infested inoculated wheat plants breached the recommended tolerable daily limit of 100 g per kg. A similar finding has recently been reported for F. graminearum in association with grain aphids on wheat (36). The authors showed a rise in DON and pathogen DNA in ears treated with aphids and F. graminearum and that increased time of aphid colonization prior to inoculation led to increased pathogen DNA accumulation.…”

“…This is in contrast to F. graminearum-infected wheat plants, which produced repellent VOCs (36). F. graminearum rapidly produces visible symptoms, including ear bleaching, which reduces the green area of the ear available for aphid feeding.…”

“…Following inoculation, ears were bagged in polyethylene for 72 h, and then bags were removed and plants were incubated for a further 14 days to allow the infection to develop until lesions were visible on the infected ears. The volatile organic chemical (VOC) emissions were then collected using the headspace sampling methods described previously (36,41), and VOC samples were used in 4-arm olfactometer bioassays using individual alate (winged) Sitobion avenae (n ϭ 10) with one treated arm and three solvent arms. The assays were conducted over a period of 16 min, rotating the chamber every 2 min to eliminate lighting bias, at 23°C under uniform lighting; the chamber was lined with filter paper (Whatman no.…”

“…Aphids are repelled by volatile chemical emissions from wheat hosts that are infected with F. graminearum (36), and as such, aphids would be expected to avoid hosts infected with this species. While this may provide a stimulus to induce emigration from infected hosts, this is unlikely to directly affect the spread of the disease, as aphids were shown to be incapable of transmitting the pathogen.…”

“…English grain aphids, Sitobion avenae, have been described as ear-feeders (33) that are more strongly influenced by the volatile organic chemical (VOC) emissions of wheat ears over wheat seedlings (34) and have been recorded as being present during ear emergence in Belgian wheat fields (35). We hypothesized that, because they occur on wheat ears alongside FHB pathogens, grain aphids may influence disease epidemiology, and we have recently shown that FHB caused by F. graminearum was influenced by aphid activity when the insect and pathogen shared the same host plant (36). Our previous study showed that grain aphids were unable to transmit F. graminearum between wheat ears but that coincidence of aphids and the pathogen lead to increased disease severity, fungal biomass, and DON accumulation in hosts.…”