Comparative genomics reveals low levels of inter- and intraspecies diversity in the causal agents of dwarf and common bunt of wheat and hint at conspecificity of Tilletia caries and T. laevis

Abstract

Tilletia caries and T. laevis, which are the causal agents of common bunt, as well as T. controversa, which causes dwarf bunt of wheat, threaten especially organic wheat farming. The three closely related fungal species differ in their teliospore morphology and partially in their physiology and infection biology. The gene content as well as intraspecies variation in these species and the genetic basis of their separation is unknown. We sequenced the genome of four T. caries, five T. controversa, and two T. laevis and extended this dataset with five publicly available ones. The genomes of the three species displayed microsynteny with up to 94.3% pairwise aligned regions excluding repetitive regions. The majority of functionally characterized genes involved in pathogenicity, life cycle, and infection of corn smut, Ustilago maydis, were found to be absent or poorly conserved in the draft genomes and the biosynthetic pathway for trimethylamine in Tilletia spp. could be different from bacteria. Overall, 75% of the identified protein-coding genes comprising 84% of the total predicted carbohydrate utilizing enzymes, 72.5% putatively secreted proteins, and 47.4% of effector-like proteins were conserved and shared across all 16 isolates. We predicted nine highly identical secondary metabolite biosynthesis gene clusters comprising in total 62 genes in all species and none were species-specific. Less than 0.1% of the protein-coding genes were species-specific and their function remained mostly unknown. Tilletia controversa had the highest intraspecies genetic variation, followed by T. caries and the lowest in T. laevis. Although the genomes of the three species are very similar, employing 241 single copy genes T. controversa was phylogenetically distinct from T. caries and T. laevis, however these two could not be resolved as individual monophyletic groups. This was in line with the genome-wide number of single nucleotide polymorphisms and small insertions and deletions. Despite the conspicuously different teliospore ornamentation of T. caries and T. laevis, a high degree of genomic identity and scarcity of species-specific genes indicate that the two species could be conspecific.

Draft genome sequencing of Tilletia caries inciting common bunt of wheat provides pathogenicity-related genes

“…Higher genome sequencing coverage was achieved compared to other genomes available in the public domain. This genome assembly was larger in size, better quality, and more accurate than other available assemblies of T. caries , ranging from 27.14 to 35.80 Mb ( Nguyen et al, 2019 ; Sedaghatjoo et al, 2022 ). Previously, six T. caries genomes were available in the GenBank and NCBI, but these genomes were small in size (USA, Canada) and had a high number of scaffolds (3,606–8,169).…”

Rapid molecular assay for the evaluation of clove essential oil antifungal activity against wheat common bunt

“…To our knowledge, several DNA-based methods have attempted to distinguish Tilletia species, but none have been able to separate T. caries and T. laevis ( Mulholland and Mc Ewan, 2000 ; Zouhar et al., 2010 ; Pieczul et al., 2018 ; Forster et al., 2022 ). Phylogenetic studies also failed to distinguish these two species and more recently some authors have suggested that T. caries and T. laevis could be considered as two morphotypes of the same species ( Sedaghatjoo et al., 2021 ; Sedaghatjoo et al., 2022 ; Forster et al., 2022 ).…”

Common bunt in organic wheat: unravelling infection characteristics relevant for resistance breeding

“…The causal agents of this fungal disease belong to the division of the Basidiomycota and show differences in teliospore morphology. Despite this phenotypic variation, genetic studies suggest that T. tritici and T. laevis might be the same species ( Carris, 2010 ; Sedaghatjoo et al., 2022 ). They also have identical life cycles with teliospores germinating at temperatures between 5°C and 20°C, relatively independent of light conditions ( Lowther, 1950 ).…”