Natural selection drives population divergence for local adaptation in a wheat pathogen

Pereira, Daniel; Croll, Daniel; Brunner, Patrick C.; McDonald, Bruce A.

doi:10.1016/j.fgb.2020.103398

Cited by 17 publications

(20 citation statements)

References 79 publications

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“…The genetic structure of P. nodorum populations has been analysed at field, regional, continental, and global scales using several types of neutral genetic markers, including restriction fragment length polymorphisms (RFLPs) (McDonald et al ., 1994; Keller et al ., 1997a, 1997b), amplified fragment length polymorphisms (AFLPs) (Bennett et al ., 2005), microsatellites (also called simple sequence repeats or SSRs) (Stukenbrock et al ., 2005), and single nucleotide polymorphisms from entire genome sequences (Richards et al ., 2019; Pereira et al ., 2020a, 2020b). Populations of P. nodorum exhibited high levels of genetic diversity in North America, Europe, Africa, Australia, and China.…”

Section: Introductionmentioning

confidence: 99%

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SnToxA, SnTox1, and SnTox3 originated in Parastagonospora nodorum in the Fertile Crescent

et al. 2020

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The centre of origin of the globally distributed wheat pathogen Parastagonospora nodorum has remained uncertain because only a small number of isolates from the Fertile Crescent were included in earlier population genetic and phylogeographic studies. We isolated and genetically analysed 193 P. nodorum strains from three naturally infected wheat fields distributed across Iran using 11 neutral microsatellite loci. Compared to previous studies that included populations from North America, Europe, Africa, Australia, and China, the populations from Iran had the highest genetic diversity globally and also exhibited greater population structure over smaller spatial scales, patterns typically associated with the centre of origin of a species. Genes encoding the necrotrophic effectors SnToxA, SnTox1, and SnTox3 were found at a high frequency in the Iranian population. By sequencing 96 randomly chosen Iranian strains, we detected new alleles for all three effector genes. Analysis of allele diversity showed that all three effector genes had higher diversity in Iran than in any population included in previous studies, with Iran acting as a hub for the effector diversity that was found in other global populations. Taken together, these findings support the hypothesis that P. nodorum originated either within or nearby the Fertile Crescent with a genome that already encoded all three necrotrophic effectors during its emergence as a pathogen on wheat. Our findings also suggest that P. nodorum was the original source of the ToxA genes discovered in the wheat pathogens Phaeosphaeria avenaria f. sp. tritici 1, Pyrenophora tritici‐repentis, and Bipolaris sorokiniana.

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Section: Introductionmentioning

confidence: 99%

“…Populations of P. nodorum exhibited high levels of genetic diversity in North America, Europe, Africa, Australia, and China. Migration rates between continents were high, resulting in a shallow population structure even on continental and global scales (Stukenbrock et al ., 2006; Pereira et al ., 2020a).…”

Section: Introductionmentioning

confidence: 99%

SnToxA, SnTox1, and SnTox3 originated in Parastagonospora nodorum in the Fertile Crescent

et al. 2020

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“…Earlier publications referred to the Switzerland 1999B population as being of Chinese origin (Sommerhalder et al 2006; Stukenbrock, Banke & McDonald 2006; McDonald et al 2012, 2013; Pereira et al 2017). A more recent study corrected the population origin (Pereira, Croll, et al 2020). Illumina whole-genome sequence data was generated for all 366 isolates with paired-end sequencing and a read length of 100-150 bp.…”

Section: Methodsmentioning

confidence: 99%

“…In the wheat pathogen Parastagonospora nodorum , TEs caused significant genetic alterations and likely facilitated the transfer of a key virulence gene. P. nodorum is a pathogen with high evolutionary potential to adapt to local conditions (Richards et al 2019; Pereira, McDonald, et al 2020; Pereira, Croll, et al 2020) and a worldwide distribution causing significant wheat yield losses (Oliver et al 2012). The pathogen harbors a repertoire of various effector genes (named Tox genes) that confer host adaptation by causing cell death on susceptible plants.…”

Section: Introductionmentioning

confidence: 99%

The population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen

Pereira

Oggenfuss

McDonald

et al. 2020

Preprint

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The activity of transposable elements (TEs) can be an important driver of genetic diversity with TE-mediated mutations having a wide range of fitness consequences. To avoid deleterious effects of TE activity, some fungi evolved highly sophisticated genomic defences to reduce TE proliferation across the genome. Repeat-induced point (RIP) mutations is a fungal-specific TE defence mechanism efficiently targeting duplicated sequences. The rapid accumulation of RIP mutations is expected to deactivate TEs over the course of a few generations. The evolutionary dynamics of TEs at the population level in a species with highly repressive genome defences is poorly understood. Here, we analyze 366 whole-genome sequences of Parastagonospora nodorum, a fungal pathogen of wheat with efficient RIP. A global population genomics analysis revealed high levels of genetic diversity and signs of frequent sexual recombination. Contrary to expectations for a species with RIP, we identified recent TE activity in multiple populations. The TE composition and copy numbers showed little divergence among global populations regardless of the demographic history. Miniature inverted-repeat transposable elements (MITEs) and terminal repeat retrotransposons in miniature (TRIMs) were largely underlying recent intra-species TE expansions. We inferred RIP footprints in individual TE families and found that recently active, high-copy TEs have possibly evaded genomic defences. We find no evidence that recent positive selection acted on TE-mediated mutations rather that purifying selection maintained new TE insertions at low insertion frequencies in populations. Our findings highlight the complex evolutionary equilibria established by the joint action of TE activity, selection and genomic repression.Data SummaryAll Illumina sequence data is available from the NCBI SRA BioProject numbers PRJNA606320, PRJNA398070 and PRJNA476481 (https://www.ncbi.nlm.nih.gov/bioproject). The Methods and Supplementary Figures S1-S11 and Supplementary Tables S1-S4 provide all information on strain locations and outcomes of genome analyses.

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“…Hence, with reliable and robust phenotyping, GWAS analyses can identify genes underlying specific gains in virulence. Mapping populations of ~100 strains were sufficient to identify key virulence factors [139] , [140] , [141] and fungicide resistance loci in fungal pathogens [135] , [139] , [140] , [142] , [143] . Genetic mapping studies can also inform the development process of new fungicides by the early identification of resistance “hotspot” genes [135] .…”

Section: Introductionmentioning

confidence: 99%

Tackling microbial threats in agriculture with integrative imaging and computational approaches

Singh

Dutta

Puccetti

et al. 2021

Computational and Structural Biotechnology Journal

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Natural selection drives population divergence for local adaptation in a wheat pathogen

Cited by 17 publications

References 79 publications

SnToxA, SnTox1, and SnTox3 originated in Parastagonospora nodorum in the Fertile Crescent

SnToxA, SnTox1, and SnTox3 originated in Parastagonospora nodorum in the Fertile Crescent

The population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen

Tackling microbial threats in agriculture with integrative imaging and computational approaches

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