PATHOGENICITY, TOXIGENIC POTENTIAL, AND GENOMICS OF Fusarium graminearum AND F. meridionale CAUSING EAR AND STALK ROT OF MAIZE

Field: Agricultural and Biological Sciences (Life Sciences)

Gibberella ear (GER) and stalk rot (GSR) diseases of maize in Brazil are caused mainly by Fusarium meridionale, a species belonging to the Fusarium graminearum species complex (FGSC). Another species within this complex, F. graminearum sensu stricto (hereafter F. graminearum), is second in importance on maize, but is the most common species found causing Fusarium Head Blight disease of wheat in Brazil. The latter species is the predominant cause of GER and GSR in North America, where F. meridionale has not been found thus far. In this dissertation I undertook a comparative analysis of pathogenic, saprophytic, toxigenic and genomic traits among a collection of strains representative of the two species and two hosts of origin to address possible explanations for the observed shift in the species dominance between maize and wheat. I initially hypothesized that the shift was due to their differential aggressiveness. To address this hypothesis, four field trials were conducted at different locations in order to study the aggressiveness (percent GER severity) of two F. meridionale and two F. graminearum strains, all isolated from maize, on maize hybrids with different levels of resistance. Plants were inoculated with single isolates, or with pairs of isolates sequentially and alternately at the silking stage. The results indicated that F. meridionale was more aggressive to maize than F. graminearum. Fusarium meridionale was also more competitive in ears that were co-inoculated with both species. In a second study I used a larger and more representative sample of strains of each species, isolated from both maize and wheat, to inoculate maize ears and stalks in the field. Consistent with my previous study, I found that F. meridionale was, on average, more aggressive than F. graminearum on maize ears. In contrast, F. graminearum was slightly more aggressive on maize stalks than F. meridionale. Both species contaminated maize ears with trichothecene mycotoxins, but F. graminearum strains produced primarily deoxynivalenol (DON) and its acetylated derivative 15ADON, whereas F. meridionale strains produced only nivalenol (NIV). The host of origin made no difference, and there was a lot of intraspecies variation in GER or GSR severity caused by isolates of both species. In a third study, an expanded collection of isolates of the two species was compared for 17 additional saprophytic, pathogenic, and toxigenic traits. Although there was significant intraspecies variation for most of these traits as well, the strains were strongly structured by species regardless of the host of origin, based on a multivariate analysis. Fusarium graminearum was a more aggressive pathogen of wheat, and produced primarily DON in rice cultures or in wheat heads. DON is known to be an important factor driving aggressiveness of F. graminearum in wheat. On the other hand, F. meridionale grew faster in culture. All F. meridionale strains produced mainly NIV both in vitro and in planta, with the exception of two strains from maize that produced more DON than NIV in wheat heads. In a fourth study, whole genome analysis of selected representatives of both species showed that they were genetically divergent, based on patterns of conservation of single-nucleotide polymorphisms (SNPs) across alignments. There was evidence of frequent outcrossing among strains within both species. The genome analysis also provided clear evidence of recombination between the two phylogenetic species, indicating that they are not genetically isolated, and thus belong to a single biological species. Genetic and phenotypic divergence of F. meridionale and F. graminearum may indicate adaptive selection to different environmental niches. The results of this study suggest differential aggressiveness and toxigenicity as partial explanations for the predominance of F. meridionale on maize and F. graminearum on wheat, and they lay a foundation for future studies to explore these associations.