Endophytic Trichoderma spp. can protect strawberry and privet plants from infection by the fungus Armillaria mellea.

Armillaria mellea is an important fungal pathogen worldwide, affecting a large number of hosts in the horticulture and forestry industries. Controlling A. mellea infection is expensive, labour intensive and time-consuming, so a new, environmentally friendly management solution is required. To this effect, endophytic Trichoderma species were studied as a potential protective agent for Armillaria root rot (ARR) in strawberry and privet plants. A collection of forty endophytic Trichoderma isolates were inoculated into strawberry (Fragaria × ananassa) plants and plant growth was monitored for two months, during which time Trichoderma treatment had no apparent effect. Trichoderma-colonised strawberry plants were then inoculated with A. mellea and after three months plants were assessed for A. mellea infection. There was considerable variation in ARR disease levels between plants inoculated with different Trichoderma spp. isolates, but seven isolates reduced ARR below the level of positive controls. These isolates were further tested for protective potential in Trichoderma-colonized privet (Ligustrum vulgare) plants where five Trichoderma spp. isolates, including two highly effective Trichoderma atrobrunneum isolates, were able to significantly reduce levels of disease. This study highlights the potential of plants pre-colonised with T. atrobrunneum for effective protection against A. mellea in two hosts from different plant families.

Susceptibility of Garden Trees and Shrubs to Armillaria Root Rot.

Armillaria root rot (ARR) is a serious disease of woody plants caused by several species of Armillaria. Armillaria isolates from diagnostic samples received in 2017 were identified by genus- and species-specific PCR and compared with isolates from an earlier survey (2004 to 2007). The results were comparable and, therefore, were combined for further analysis. Three species were identified: Armillaria mellea (83%), A. gallica (15%), and A. ostoyae (2%). Their wide host range makes choice of resistant plants in management of the disease difficult. We used the Royal Horticultural Society diagnostic dataset of ARR records from U.K. gardens to compare the susceptibility of different host genera to the disease. The dataset was compared with an earlier experiment at the University of California. An index-based approach was used to separate genera into three categories: 77 low-index (<0.99), 37 medium-index (0.99 to 1.76), and 56 high-index (>1.76) genera were recorded. All three species were associated with both angiosperms and gymnosperms; moreover, A. ostoyae did not show the host preference for gymnosperms that has been reported elsewhere. A. gallica was particularly common on herbaceous perennials and showed a trend to occur on resistant hosts that may be under other stress, supporting its description as an opportunistic pathogen. Four monocotyledons grown as trees or shrubs in U.K. gardens had a very low ARR index according to indices associated with A. mellea and A. ostoyae. Genera in the order Myrtales were almost always low index, while those in the Saxifragales and Fagales were mostly high index. These results provide confidence in the use of host resistance as part of the integrated management of ARR.

Associations Between Armillaria Species and Host Plants in U.K. Gardens.

Honey fungus (Armillaria spp.) root rot is the disease most frequently inquired about by U.K. gardeners to the Royal Horticultural Society. Armillaria epidemiology has been studied within forestry and agriculture, but data are lacking within gardens, which have greater host plant diversity than orchards and vineyards and greater disturbance than woodlands. Which Armillaria species are responsible for garden disease, and how the broad range of susceptible ornamentals are differentially affected is not known. To address this, isolates of Armillaria were obtained from dead and dying plants from across the U.K. over a 4-year period (2004 to 2007). Species were identified by PCR-RFLP for IGS, and further verified by species-specific PCR for EF-1 α. Of the seven species known in the U.K., three were identified: A. mellea (83.1%), A. gallica (15.8%), and A. ostoyae (1.1%). Armillaria was isolated from trees, shrubs, and nonwoody plants including bulbs and vegetables, with newly recorded hosts listed herein. A. mellea was associated with infections of multiple hosts, and with all infections of the most common host, Ligustrum. In sites where more than one Armillaria species was found, the combination was of A. mellea and A. gallica, raising questions regarding the interactions of these species in U.K. gardens.

Contrasting Roles of Deoxynivalenol and Nivalenol in Host-Mediated Interactions between Fusarium graminearum and Sitobion avenae.

Fusarium graminearum is the predominant causal species of Fusarium head blight in Europe and North America. Different chemotypes of the species exist, each producing a plethora of mycotoxins. Isolates of differing chemotypes produce nivalenol (NIV) and deoxynivalenol (DON), which differ in toxicity to mammals and plants. However, the effect of each mycotoxin on volatile emissions of plant hosts is not known. Host volatiles are interpreted by insect herbivores such as Sitobion avenae, the English grain aphid, during host selection. Previous work has shown that grain aphids are repelled by wheat infected with DON-producing F. graminearum, and this study seeks to determine the influence of pathogen mycotoxins to host volatile chemistry. Volatile collections from infected hosts and olfactometer bioassays with alate aphids were performed. Infections with isolates that produced DON and NIV were compared, as well as a trichothecene deficient transformant derived from the NIV-producing isolate. This work confirmed the repellent nature of infected hosts with DON accumulation. NIV accumulation produced volatiles that were attractive to aphids. Attraction did not occur when NIV was absent and was, therefore, a direct consequence of NIV production.

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

Fusarium langsethiae is a fungal pathogen of cereal crops that is an increasing problem in northern Europe, but much of its epidemiology is poorly understood. The species produces the mycotoxins T-2 and HT-2, which are highly toxic. It was hypothesized that grain aphids, Sitobion avenae, may transmit F. langsethiae inoculum between wheat plants, and a series of transmission experiments and volatile chemical analyses was performed to test this. Manual translocation of aphids from inoculated to uninfected hosts resulted in pathogen DNA accumulation in hosts. However, the free movement of wingless aphids from infected to healthy plants did not. The addition of winged aphids reared on F. langsethiae-inoculated wheat seedlings to wheat plants also did not achieve successful pathogen transfer. While our data suggested that aphid transmission of the pathogen was not very efficient, we observed an increase in disease when aphids were present. After seedling inoculation, an increase in pathogen DNA accumulation in seedling leaves was observed upon treatment with aphids. Furthermore, the presence of aphids on wheat plants with F. langsethiae-inoculated ears not only led to a rise in the amount of F. langsethiae DNA in infected grain but also to an increase in the concentrations of T-2 and HT-2 toxins, with more than 3-fold higher toxin levels than diseased plants without aphids. This work highlights that aphids increase the susceptibility of wheat host plants to F. langsethiae and that aphid infestation is a risk factor for accumulating increased levels of T-2 and HT-2 in wheat products. IMPORTANCE: Fusarium langsethiae is shown here to cause increased contamination levels of grain with toxins produced by fungus when aphids share the host plant. This effect has also recently been demonstrated with Fusarium graminearum, yet the two fungal species show stark differences in their effect on aphid populations. In both cases, aphids improve the ability of the pathogens to cause and initiate Fusarium head blight (FHB) disease in wheat, but F. langsethiae may be able to act as a dispersal agent. F. langsethiae contributes harmful toxins to wheat grain that need to be controlled, but as yet, its epidemiology is unresolved. This work reveals insights into the role aphids play in promoting the successful colonization of this species in wheat and the benefit of controlling aphid populations on crops that are at high risk of FHB.

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).

We 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.