The Genomic Basis of Adaptation in the Barley Fungal Pathogen Rhynchosporium Commune

Plant fungal pathogens cause significant damage, jeopardize modern agricultural ecosystems and global food security. Fungal pathogens possess a high evolutionary potential that enables rapid evolution to environmental changes. Despite many evidence pointing to local adaptations in fungal pathogens,...

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Bibliographic Details
Main Author: Mohd Assaad, Norfarhan B.
Other Authors: McDonald, Bruce A., Croll, Daniel, Roulin, Anne
Format: Doctoral or Postdoctoral Thesis
Language:English
Published: ETH Zurich 2018
Subjects:
Online Access:https://hdl.handle.net/20.500.11850/284275
https://doi.org/10.3929/ethz-b-000284275
Description
Summary:Plant fungal pathogens cause significant damage, jeopardize modern agricultural ecosystems and global food security. Fungal pathogens possess a high evolutionary potential that enables rapid evolution to environmental changes. Despite many evidence pointing to local adaptations in fungal pathogens, the genetic basis underpinning the adaptation processes remains poorly understood. The main objective of this PhD thesis is to study the genetic basis of adaptation in Rhynchosporium commune, the causal agent of the devastating barley scald disease. In this study, we resequenced the whole genome of 125 R. commune isolates collected from nine global populations: Iceland, Norway, Finland, Switzerland, Spain, Ethiopia, USA, New Zealand, and Australia. These populations represent a wide range of climatic conditions and agricultural practices with evident of selection acting on quantitative traits of virulence, thermal adaptation, and fungicide sensitivity. The analysis of population structures using single nucleotide polymorphisms (SNPs) spanning the whole genome grouped these isolates into three main clusters with evidence of gene flow among clusters. We performed a genome-wide association study (GWAS) to investigate the genetic basis of fungal resistance to the widely used azole class of fungicides. We found significant associations with SNPs located in conserved genes encoding a vacuolar cation channel YVC1, a transcription activator, and a saccharopine dehydrogenase. The YVC1 gene is involved in a conserved pathway critical to azole resistance in human pathogenic fungi. We found evidence for fitness trade-offs in the isolates accumulating resistance mutations suggesting azole resistance evolutions impose costs. We also performed genome-wide selection scans to identify footprints of recent selection that shaped the genetic variation in R. commune populations. Our analyses revealed widespread signals of selective sweeps across the genomes with little overlaps between the genetic clusters, suggesting that ecological differences drive divergent selection among these clusters. The strongest selective sweeps identified in our study encoded protein associated with various functions in response to abiotic and biotic stresses. Finally, we performed a comparative genomic analysis to investigate the evolution of a known R. commune effector, namely necrosis-inducing protein 1 (NIP1) and its association with host adaptation. In addition to the 125 genome sequences of R. commune, this study also included the whole genome assemblies of nine, eight, and four R. secalis, R. agropyri, and R. orthosporum strains, respectively. We found that the NIP1 effector gene shows presenceabsence polymorphism in all the four species. The phylogenetic analysis revealed a clear division of NIP1 into two major clades we named NIP1A and NIP1B. We found recent duplications of NIP1A and NIP1B following the speciation of R. commune with statistical evidence for the association with fungal virulence. Selection analyses suggest that NIP1A experienced a strong positive selection, while NIP1B experienced a relaxed purifying selection in R. commune. This suggests that selection pressures exerted by the host plant led to the rapid diversification of at least one paralog of the NIP1 effector gene. This study demonstrates the importance of nucleotide polymorphisms and structural variations in the evolution and rapid adaptation of NIP1 effector gene. Overall, these studies demonstrate the potential applications of multiple genomics approaches to substantially enhance our understanding of adaptive evolution in plant fungal pathogen.