Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust

Abstract

Coffee leaf rust, caused by Hemileia vastatrix (Hv), represents the biggest threat to coffee production worldwide and ranks amongst the most serious fungal diseases in history. Despite a recent series of outbreaks and emergence of hypervirulent strains, the population evolutionary history and potential of this pathogen remain poorly understood. To address this issue, we used restriction site-associated DNA sequencing (RADseq) to generate ∼19 000 single nucleotide polymorphisms (SNPs) across a worldwide collection of 37 Hv samples. Contrary to the long-standing idea that Hv represents a genetically unstructured and cosmopolitan species, our results reveal the existence of a cryptic species complex with marked host tropism. Using phylogenetic and pathological data, we show that one of these lineages (C3) infects almost exclusively the most economically valuable coffee species (tetraploids that include Coffea arabica and interspecific hybrids), whereas the other lineages (C1 and C2) are severely maladapted to these hosts, but successfully infect diploid coffee species. Population dynamic analyses suggest that the C3 group may be a recent 'domesticated' lineage that emerged via host shift from diploid coffee hosts. We also found evidence of recombination occurring within this group, which could explain the high pace of pathotype emergence despite the low genetic variation. Moreover, genomic footprints of introgression between the C3 and C2 groups were discovered and raise the possibility that virulence factors may be quickly exchanged between groups with different pathogenic abilities. This work advances our understanding of the evolutionary strategies used by plant pathogens in agro-ecosystems with direct and far-reaching implications for disease control.

Fifty Aureobasidium pullulans genomes reveal a recombining polyextremotolerant generalist

“…Genomic data can provide a wealth of information. Indeed, even for some species previously thought to have homogeneous population genetics structure, detailed analyses have uncovered cryptic populations with differences in their animal or plant virulence (Desjardins et al ., ; Douglass et al ., ; Silva et al ., ), metabolism (Dhami et al ., ), domestication patterns (Duan et al ., ; Peter et al ., ) and adaptation to differences in climate (Ellison et al ., ; Branco et al ., ; ). This does not appear to be the case for A. pullulans .…”

“…Two non-recombining African lineages have been described for Cryptococcus neoformans, one of which has accumulated adaptations presumably (coincidentally) predisposing it for human virulence (Desjardins et al, 2017). Hemileia vastatrix is the cause of coffee leaf rust, and it was initially believed to be a genetically unstructured and cosmopolitan species, but was later revealed to be a complex of cryptic species with marked host tropism (Silva et al, 2018). Population structuring (with no significant geographic structure) has been reported for the pathogenic Pneumocystis species (Cissé et al, 2018).…”

Genome-scale data reveal the role of hybridization in lichen-forming fungi

“…open Scientific RepoRtS | (2020) 10:1497 | https://doi.org/10.1038/s41598-020-58279-x www.nature.com/scientificreports www.nature.com/scientificreports/ nuclear markers, which in turn can influence the genome in both adaptive and maladaptive ways 5,[19][20][21][22] . Adaptive introgression of mitochondrial DNA may play an important role in speciation and phylogeography 23,24 .While hybridization has been well-documented among pathogenic fungi 21,[25][26][27][28][29][30] , the role of hybridization on the process of speciation of fungal lineages with different life histories and ecological functions is not well understood, including among lichen-forming fungi. The role of gene flow and hybridization in lichen-forming fungal evolution has been a long-standing question [31][32][33][34][35] .…”

On the hunt for the alternate host of Hemileia vastatrix

“…Modern coffee breeding and cultivation have led to a continuous evolution exertion on H. vastatrix by selection for resistance to CLR in commercial Coffea spp. cultivars (Silva, Várzea, Paulo, & Batista, 2018). Today, more than 50 races of H. vastatrix are known (Talhinhas et al, 2017).…”

“…Today, more than 50 races of H. vastatrix are known (Talhinhas et al, 2017). This is an inexplicable evolution for a pathogen that supposedly only utilizes clonal reproduction (Silva et al, 2018). Some reports have started to emerge, hypothesizing that the different races of H. vastatrix are the result of cryptosexuality, that is, the occurrence of hidden sexual reproduction within the urediniospores (Carvalho et al, 2011).…”