Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation

Abstract

Generation of genetic diversity is crucial for the evolution of new traits, with mutation and sexual 34 recombination as the main drivers of diversity in most eukaryotes. However, many species in the 35 fungal kingdom can propagate asexually for extended periods and therefore understanding alternative 36 mechanisms contributing to genetic diversity in asexual populations has been of great interest 1,2 . Some 37 fungi can use a parasexual mechanism to exchange genetic material independently of meiosis 2 . This 38 process involves anastomosis of haploid hyphae and fusion of two nuclei to generate a single diploid 39 nucleus, which subsequently undergoes progressive chromosome loss to generate recombinant haploid 40 offspring. Parasexuality has been described in members of the ascomycete phylum (64% of described 41 fungal species) in which the dominant asexually propagating form is haploid 3 . However, in 42 basidiomycete fungi (34% of described species), the predominant life stage is generally dikaryotic, 43 with two different haploid nuclei maintained within each individual 3 . The role of non-sexual genetic 44 exchange between such dikaryons in generating genetic diversity is not known. 45 Basidiomycetes include many fungi with critical ecosystem functions, such as wood decay and 46 plant symbiosis, as well as agents of important human and plant diseases 1 . Rust fungi (subphylum 47 Pucciniomycotina) comprise over 8,000 species including many pathogens of major agricultural and 48 ecological significance 4 . These organisms are obligate parasites with complex life cycles that can 49 include indefinite asexual reproduction through infectious dikaryotic urediniospores. Early researchers 50 speculated that rust fungi can exchange genetic material during the asexual phase 5-8 , but these 51 hypotheses could not be confirmed molecularly. Some naturally occurring rust pathotypes have been 52 suggested to have arisen by somatic hybridisation and genetic exchange based on limited molecular 53 evidence of shared isozyme or random amplified polymorphic DNA (RAPD) markers 9,10 . Mechanisms 54 underlying genetic exchange are unknown, but may involve hyphal anastomosis followed by nuclear 55 exchange and/or nuclear fusion and recombination 11 . Recent advances in assembling complete karyon 56 sequences in rust fungi 12,13 provide the opportunity to definitively detect and discriminate between 57 nuclear exchange and recombination. 58 4The Ug99 strain (race TTKSK) of the wheat stem rust pathogen Puccinia graminis f. sp. tritici 59 (Pgt) presents a significant threat to global wheat production 14 . It was first detected in Uganda in 1998 60 and described in 1999 15 , and has since given rise to an asexual lineage that has spread through Africa 61 and the Middle East causing devastating epidemics 14 . The origin of the Ug99 lineage is unknown, 62 although it is genetically distinct from other Pgt races 16,17 . To resolve the genetic makeup of Ug99, we 63 generated a haplotype-phased genome reference for the origi...

Evolutionary and genomic comparisons of hybrid uninucleate and nonhybrid Rhizoctonia fungi

“…In this study, we identified naturally occurring uninucleate Rhizoctonia isolates as hybrid genomes which maintained in their diploid nuclei. Hybrid fungal species have been shown in Saccharomyces, Cryptococcus, Verticillium, and Puccinia 11,14,30,41 . The fused fungal hyphae normally restore the haploid state from the hybrid diploid nucleus by chromosome loss 10 .…”

“…Genomic analyses of wheat stem rust (Puccinia graminis f. sp. tritici, Ug99) and wheat leaf rust (P. triticina, Pt64) demonstrated that the virulent isolates arose from somatic hybridization and had nuclear exchange between dikaryons 14,15 . The results suggest that hybrid genomes of phytopathogens can provide evolutionary flexibility for the pathogen enabling rapid adaptation to different hosts and other environmental changes.…”

Genetic Characterization and Genome-Wide Association Mapping for Stem Rust Resistance in Spring Bread Wheat

“…Stem rust of wheat disease has been increasing in severity and incidence and now poses a serious threat to global wheat production [8]. To overcome this threat, efforts are going on worldwide to monitor rust diseases, identify rust pathotypes, and to evaluate wheat germplasm for rust resistance [26].…”

Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)

“…tritici) resistance were overcome in recent years by a novel rust lineage known as Ug99 (Singh et al, 2015). Ug99 originated from the dikaryotic parasexual combination of two asexual rust lineages (Li et al, 2019). If rust species are geographically restricted, switchgrass may evolve local resistance mechanisms to respond to specific rusts.…”