Etiology and diversity of Fusarium species causing head blight of wheat in Australia

Fusarium head blight (FHB) has recently re-emerged worldwide as a disease of economic importance of wheat and barley. Fusarium species, including two subgroups of F. graminearum initially assigned to Group 1 and Group 2 and recently re-classified as F. pseudograminearum and F. graminearum, respectively, cause FHB. Both species also cause crown rot of wheat in Australia. The relative distribution and abundance of these two Fusarium species causing FHB on wheat have not been systematically studied. In Australia, a lack of knowledge of pathogen diversity and aggressiveness has impeded the development and deployment of host resistance against the dominant and damaging pathogen strains. The aims of this study were: to determine the identity and relative prevalence of Fusarium species causing FHB in Australia; to enumerate genetic and pathogenic variability within the predominant species; to improve understanding of pathogen aggressiveness for use as a tool to select for quantitative FHB resistance in wheat; to consider mechanisms that generate variation in the pathogen population; and to explore relationships among traits that contribute to increased pathogen fitness.  This study used over 400 isolates from different plant parts of wheat in various cropping systems collected from surveys of Queensland and northern New South Wales in 2001 and 2003. Twenty Fusarium species were identified using morphology and species-specific PCR assays. Representing 48% of all isolates, F. pseudograminearum was very widespread and more frequently obtained from the crown than F. graminearum, which made up 28% of all isolates and was mainly collected from spike. All 17 Fusarium species tested caused FHB in plant infection assays, with significant differences in aggressiveness evident between species and among isolates within species. However, there was no significant difference in aggressiveness between F. pseudograminearum and F. graminearum. Overall, isolates collected from the flag leaf node and wheat following maize or sorghum were most commonly highly aggressive for FHB.  Fifty-three wheat lines were screened as potential sources of host differentials using one aggressive isolates of both F. graminearum and F. pseudograminearum.The isolate of each species infected all the 53 germplasm used in this study. All durum wheat germplasm used were consistently rated as susceptible to FHB while nine germplasm, including Sumai 3, were consistently grouped as resistant. These nine wheat germplasm were selected as putative differentials and screened in a controlled environment with 22 isolates using a point inoculation method. A significant isolate x germplasm interaction suggested a potential pathogenic specialisation among isolates. In a principal component analysis the first component explained 90% of the variation. The relatively large effect of the first component indicates that isolates differ largely in their aggressiveness with only small differential effects between the putative races. A cluster analysis demarcated three race clusters, based mainly on their aggressiveness on Sumai 3.  The diversity in the Australian F. graminearum and F. pseudograminearum populations were assessed based on growth rate, fecundity and genetically. Genetic diversity was determined using the selectively-neutral amplified fragment length polymorphism (AFLP) marker. There was a high degree of variation in growth rate and fecundity among Australian F. pseudograminearum and F. graminearum isolates. Using AFLP data the F. graminearum isolates could be grouped into 5 clusters, with representative isolates of F. graminearum lineages 1-7 distributed within two of the clusters. Cluster 1 contained over 40% of the Australian F. graminearum population. The F. pseudograminearum population was not delineated into distinct subdivisions. There was no strong relationship between AFLP clusters, aggressiveness, source of isolation or toxin production. The level of gametic disequilibrium within populations of both species was significantly (P < 0.02) different from that expected in randomly mating populations and recombination was more common in F. graminearum than in F. pseudograminearum. Neither of the population is panmictic or strictly clonal. Spatial distribution of AFLP haplotypes was determined for isolates collected from NSW and Qld and those collected using a hierarchical sampling from within a field in Australia and Canada. Many isolates of F. pseudograminearum from NSW and Qld were genetically similar but F. graminearum isolates from the same spike were highly diverse. As expected, the Canadian isolates of F. graminearum were very different from the Australian collection.  The Australian F. pseudograminearum and F. graminearum isolates belong to a large number of mycelial compatibility groups (MCG) as determined using a barrage zone formation technique. Hyphal anastomosis has been observed in selected pairing of isolates. However, compatible isolate pairs were not consistently compatible or incompatible, and this gave as many MCGs as isolates. A scheme for the grouping of isolates according to their MCG is suggested. When a subset of isolates from the two species was paired, only 2% of F. pseudograminearum produced fertile heterothallic perithecia, far less than the 90% of homothallic perithecia produced by Gibberella zeae (Anamorph F. graminearum). Putative inter-species hybridisation was observed in culture but this has not been conclusively proven. Results suggest a potential role for both sexual and asexual means in generating variation in the FHB pathogen.  Aggressiveness of selected isolates on wheat, pathogenicity on 10 alternative host plants, saprophytic growth rate and fecundity and changes in aggressiveness to wheat following a passage through an alternative host were examined to better understand the apparent superior ecological fitness of F. pseudograminearum over F. graminearum in Australia. There was a change in fecundity of some isolates after passing through an alternative host and the increase in fecundity of some secondary isolates was correlated to their increased aggressiveness on wheat. These findings show significant variation in the pathogen and the possibility of pathogenic specialisation, which should be considered in the screening of wheat germplasm and the breeding for disease resistance against FHB. Further research is needed to examine mechanisms that generate variation in the pathogen.

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