Genomic variability as a driver of plant–pathogen coevolution?

Karasov, Talia L.; Horton, Matthew; Bergelson, Joy

doi:10.1016/j.pbi.2013.12.003

Cited by 126 publications

(106 citation statements)

References 68 publications

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“…Hence, these fungi are ideal models to study the impact of recombination on pathogen evolution. Loci contributing to virulence in pathogens undergo rapid allele frequency changes in response to changes in host populations (Barrett et al 2009;Thrall et al 2012), and fungal pathogenicity is often found to be encoded by a large number of virulence loci distributed throughout the genome (Karasov et al 2014). Recombination enables the emergence of pathogen strains that carry novel combinations of virulence alleles that may increase virulence in specific hosts.…”

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confidence: 99%

The Impact of Recombination Hotspots on Genome Evolution of a Fungal Plant Pathogen

et al. 2015

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Recombination has an impact on genome evolution by maintaining chromosomal integrity, affecting the efficacy of selection, and increasing genetic variability in populations. Recombination rates are a key determinant of the coevolutionary dynamics between hosts and their pathogens. Historic recombination events created devastating new pathogens, but the impact of ongoing recombination in sexual pathogens is poorly understood. Many fungal pathogens of plants undergo regular sexual cycles, and sex is considered to be a major factor contributing to virulence. We generated a recombination map at kilobase-scale resolution for the haploid plant pathogenic fungus Zymoseptoria tritici. To account for intraspecific variation in recombination rates, we constructed genetic maps from two independent crosses. We localized a total of 10,287 crossover events in 441 progeny and found that recombination rates were highly heterogeneous within and among chromosomes. Recombination rates on large chromosomes were inversely correlated with chromosome length. Short accessory chromosomes often lacked evidence for crossovers between parental chromosomes. Recombination was concentrated in narrow hotspots that were preferentially located close to telomeres. Hotspots were only partially conserved between the two crosses, suggesting that hotspots are short-lived and may vary according to genomic background. Genes located in hotspot regions were enriched in genes encoding secreted proteins. Population resequencing showed that chromosomal regions with high recombination rates were strongly correlated with regions of low linkage disequilibrium. Hence, genes in pathogen recombination hotspots are likely to evolve faster in natural populations and may represent a greater threat to the host.KEYWORDS recombination hotspots; pathogen evolution; restriction site-associated DNA sequencing; population genomics; linkage disequilibrium R ECOMBINATION is a fundamental process that shapes the evolution of genomes. Crossover between homologous chromosomes ensures proper segregation during meiosis (Mather 1938;Baker et al. 1976;Hassold and Hunt 2001), and the integrity of chromosomal structure over evolutionary time is affected by the frequency of recombination. Sex chromosomes in plants and animals and mating-type regions of fungi experience degeneration, including significant gene loss and sequence rearrangements, after cessation of recombination between homologs (Bull 1983;Charlesworth and Charlesworth 2000;Brown et al. 2005;Menkis et al. 2008;Wilson and Makova 2009). Recombination breaks up linkage between alleles of different loci and creates novel haplotypes and phenotypic diversity. Through this process, recombination promotes adaptation because selection acting across multiple loci becomes more efficient as the linkage between loci decreases (Hill and Robertson 1966;Otto and Barton 1997;Otto and Lenormand 2002).Recombination also plays a major role in the coevolutionary dynamics of hosts and their pathogens. A major driver to maintain sexual...

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confidence: 99%

The Impact of Recombination Hotspots on Genome Evolution of a Fungal Plant Pathogen

et al. 2015

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“…Selective sweeps, usually associated with purifying selection, occur when environments select for the same traits/genotypes among populations inhabiting different ecological niches, thereby reducing genetic differentiation in related traits/genotypes among geographic populations (Zhan et al. 2004; Karasov et al., 2014). The hypothesis of a selective sweep occurring in the effector gene was supported by a comparative population genetic analysis of Avr3a and SSR marker loci which showed that genetic differentiation in Avr3a (assessed through the G ST statistic) was significantly lower than genetic differentiation in the SSR marker loci (assessed through the F ST statistic, Zhan et al., 2005).…”

Section: Discussionmentioning

confidence: 99%

Evidence for intragenic recombination and selective sweep in an effector gene of Phytophthora infestans

Yang

Ouyang

Fang

et al. 2018

Evolutionary Applications

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Effectors, a group of small proteins secreted by pathogens, play a critical role in the antagonistic interaction between plant hosts and pathogens through their dual functions in regulating host immune systems and pathogen infection capability. In this study, evolution in effector genes was investigated through population genetic analysis of Avr3a sequences generated from 96 Phytophthora infestans isolates collected from six locations representing a range of thermal variation and cropping systems in China. We found high genetic variation in the Avr3a gene resulting from diverse mechanisms extending beyond point mutations, frameshift, and defeated start and stop codons to intragenic recombination. A total of 51 nucleotide haplotypes encoding 38 amino acid isoforms were detected in the 96 full sequences with nucleotide diversity in the pathogen populations ranging from 0.007 to 0.023 (mean = 0.017). Although haplotype and nucleotide diversity were high, the effector gene was dominated by only three haplotypes. Evidence for a selective sweep was provided by (i) the population genetic differentiation (G ST) of haplotypes being lower than the population differentiation (F ST ) of SSR marker loci; and (ii) negative values of Tajima's D and Fu's FS. Annual mean temperature in the collection sites was negatively correlated with the frequency of the virulent form (Avr3aEM), indicating Avr3a may be regulated by temperature. These results suggest that elevated air temperature due to global warming may hamper the development of pathogenicity traits in P. infestans and further study under confined thermal regimes may be required to confirm the hypothesis.

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“…Examples of complex R loci in crop plants include the resistance genes Rp1 in maize (Smith et al, 2004), Cf-4/9 in tomato (Parniske et al, 1997), M in flax (Anderson et al, 1997), Dm3 in lettuce (Shen et al, 2002) and R1 in potato (Ballvora et al, 2002). Typically, the recognized effectors as well as the recognizing NLRs show increased levels of polymorphisms and are likely under balancing selection to maintain allelic diversity within natural populations (Bergelson et al, 2001;Karasov et al, 2014). These complexities have limited the ability to determine the sequences of complex NLR loci in the past, especially using short-read sequencing data (Cao et al, 2011).…”

Section: Widespread Complexity At An Arabidopsis Tir-nlr Locusmentioning

confidence: 99%

“…By contrast, many NLRs conferring resistance to naturally occurring pathogens recognize single 'cognate' effectors, leading to co-evolutionary arms races on ligandand receptor-binding surfaces (Dodds et al, 2006;Krasileva et al, 2010;Kanzaki et al, 2012;Cesari et al, 2013). Pressure to evade and re-establish immunity is evident from allelic sequence divergence with the signature of positive selection (Bergelson et al, 2001;Karasov et al, 2014). New recognition capability can also result from the complexity of NLR genetic loci, where gene rearrangements, duplications and transposon insertions can result in dozens of NLR receptor variants (McDowell et al, 1998;Baumgarten et al, 2003;Meyers et al, 2003;Leister, 2004).…”

Section: Introductionmentioning

confidence: 99%

Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector

et al. 2016

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Nucleotide-binding leucine-rich repeat (NB-LRR, or NLR) receptors mediate pathogen recognition. The Arabidopsis thaliana NLR RPP1 recognizes the tandem WY-domain effector ATR1 from the oomycete Hyaloperonospora arabidopsidis through direct association with C-terminal LRRs. We isolated and characterized homologous NLR genes RPP1-EstA and RPP1-ZdrA from two Arabidopsis ecotypes, Estland (Est-1) and Zdarec (Zdr-1), responsible for recognizing a novel spectrum of ATR1 alleles. RPP1-EstA and -ZdrA encode nearly identical NLRs that are phylogenetically distinct from known immunity-activating RPP1 homologs and possess greatly expanded LRR domains. Site-directed mutagenesis and truncation analysis of ATR1 suggests that these homologs recognize a novel surface of the 2(nd) WY domain of ATR1, partially specified by a C-terminal region of the LRR domain. Synteny comparison with RPP1 loci involved in hybrid incompatibility suggests that these functions evolved independently. Closely related RPP1 homologs have diversified their recognition spectra through LRR expansion and sequence variation, allowing them to detect multiple surfaces of the same pathogen effector. Engineering NLR receptor specificity may require a similar combination of repeat expansion and tailored amino acid variation.

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Genomic variability as a driver of plant–pathogen coevolution?

Cited by 126 publications

References 68 publications

The Impact of Recombination Hotspots on Genome Evolution of a Fungal Plant Pathogen

The Impact of Recombination Hotspots on Genome Evolution of a Fungal Plant Pathogen

Evidence for intragenic recombination and selective sweep in an effector gene of Phytophthora infestans

Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector

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