Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species

Menardo, Fabrizio; Praz, Coraline R.; Wyder, Stefan; Ben‐David, Roi; Bourras, Salim; Matsumae, Hiromi; McNally, Kaitlin E.; Parlange, Francis; Riba, Andrea; Roffler, Stefan; Schaefer, Luisa Katharina; Shimizu, Kentaro; Valenti, L.; Zbinden, Helen; Wicker, Thomas; Keller, Beat

doi:10.1038/ng.3485

Cited by 184 publications

(171 citation statements)

References 49 publications

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“…Evidence for prevalent clonal over sexual B. graminis reproduction in natural environments, together with a short lifespan of its airborne asexual propagules-called conidiospores, whose survival declines rapidly within 24 h-predicts a limited geographic dispersal for clonal progeny (17,18,47). Although these Bgh features could explain a distinctive population lineage detected for the Australian isolates ( Fig.…”

Section: Discussionmentioning

confidence: 95%

Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen

Kracher

Saur

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

150

202

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Disease-resistance genes encoding intracellular nucleotide-binding domain and leucine-rich repeat proteins (NLRs) are key components of the plant innate immune system and typically detect the presence of isolate-specific avirulence (AVR) effectors from pathogens. NLR genes define the fastest-evolving gene family of flowering plants and are often arranged in gene clusters containing multiple paralogs, contributing to copy number and allele-specific NLR variation within a host species. Barley mildew resistance locus a (Mla) has been subject to extensive functional diversification, resulting in allelic resistance specificities each recognizing a cognate, but largely unidentified, AVRa gene of the powdery mildew fungus, Blumeria graminis f. sp. hordei (Bgh). We applied a transcriptome-wide association study among 17 Bgh isolates containing different AVRa genes and identified AVRa1 and AVRa13, encoding candidate-secreted effectors recognized by Mla1 and Mla13 alleles, respectively. Transient expression of the effector genes in barley leaves or protoplasts was sufficient to trigger Mla1 or Mla13 allele-specific cell death, a hallmark of NLR receptor-mediated immunity. AVRa1 and AVRa13 are phylogenetically unrelated, demonstrating that certain allelic MLA receptors evolved to recognize sequence-unrelated effectors. They are ancient effectors because corresponding loci are present in wheat powdery mildew. AVRA1 recognition by barley MLA1 is retained in transgenic Arabidopsis, indicating that AVRA1 directly binds MLA1 or that its recognition involves an evolutionarily conserved host target of AVRA1. Furthermore, analysis of transcriptome-wide sequence variation among the Bgh isolates provides evidence for Bgh population structure that is partially linked to geographic isolation.

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Section: Discussionmentioning

confidence: 95%

Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen

Kracher

Saur

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

150

202

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“…tritici 2 d 6 Triticum dicoccoides a

See Material and Methods for the accession numbers.

Plants on which the isolates were collected.

B. graminis growing on Lolium sp. was never formally designated as a f.sp .

dThese two groups were found to be genomically divergent despite a common host range (Ben-David et al 2016; Menardo et al 2016). …”

Section: Introductionmentioning

confidence: 99%

Reconstructing the Evolutionary History of Powdery Mildew Lineages (Blumeria graminis) at Different Evolutionary Time Scales with NGS Data

Menardo¹,

Wicker²,

Keller³

2017

Genome Biology and Evolution

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Blumeria graminis (Ascomycota) includes fungal pathogens that infect numerous grasses and cereals. Despite its economic impact on agriculture and its scientific importance in plant–pathogen interaction studies, the evolution of different lineages with different host ranges is poorly understood. Moreover, the taxonomy of grass powdery mildew is rather exceptional: there is only one described species (B. graminis) subdivided in different formae speciales (ff.spp.), which are defined by their host range. In this study we applied phylogenomic and population genomic methods to whole genome sequence data of 31 isolates of B. graminis belonging to different ff.spp. and reconstructed the evolutionary relationships between different lineages. The results of the phylogenomic analysis support a pattern of co-evolution between some of the ff.spp. and their host plant. In addition, we identified exceptions to this pattern, namely host jump events and the recent radiation of a clade less than 280,000 years ago. Furthermore, we found a high level of gene tree incongruence localized in the youngest clade. To distinguish between incomplete lineage sorting and lateral gene flow, we applied a coalescent-based method of demographic inference and found evidence of horizontal gene flow between recently diverged lineages. Overall we found that different processes shaped the diversification of B. graminis, co-evolution with the host species, host jump and fast radiation. Our study is an example of how genomic data can resolve complex evolutionary histories of cryptic lineages at different time scales, dealing with incomplete lineage sorting and lateral gene flow.

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“…For the examples outlined above, sexual recombination was instrumental in the generation of new genotypes that were favoured by natural selection and propagated on a new host [48]. By recombination, parental genomes are re-assorted to generate new combinations of alleles in the progeny population.…”

Section: Example 2: Hybridization Of Crop Plants Driving Hybrid Specimentioning

confidence: 99%

“…B 371: 20160026 approach. They sequenced multiple B. graminis isolates sampled from wheat, rye and triticale and conducted a detailed analysis of the distribution of single nucleotide polymorphisms (SNPs) [48]. The three formae specialis mildew pathogens can be distinguished using fixed SNPs, which clearly separate the three pathogens.…”

Section: Example 2: Hybridization Of Crop Plants Driving Hybrid Specimentioning

confidence: 99%

“…B.g. triticale can infect wheat but not rye, and transcriptomic data were therefore generated only for the wheat and triticale host -pathogen interactions [48]. However, the infection experiments of the hybrid pathogen on wheat and triticale did not reveal genes differentially expressed in the two hosts, suggesting that virulence may depend on the effects of multiple genes [48].…”

Section: Example 2: Hybridization Of Crop Plants Driving Hybrid Specimentioning

confidence: 99%

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Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

McDonald

Stukenbrock

2016

Phil. Trans. R. Soc. B

290

199

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Agricultural ecosystems are composed of genetically depauperate populations of crop plants grown at a high density and over large spatial scales, with the regional composition of crop species changing little from year to year. These environments are highly conducive for the emergence and dissemination of pathogens. The uniform host populations facilitate the specialization of pathogens to particular crop cultivars and allow the build-up of large population sizes. Population genetic and genomic studies have shed light on the evolutionary mechanisms underlying speciation processes, adaptive evolution and long-distance dispersal of highly damaging pathogens in agro-ecosystems. These studies document the speed with which pathogens evolve to overcome crop resistance genes and pesticides. They also show that crop pathogens can be disseminated very quickly across and among continents through human activities. In this review, we discuss how the peculiar architecture of agro-ecosystems facilitates pathogen emergence, evolution and dispersal. We present four example pathosystems that illustrate both pathogen specialization and pathogen speciation, including different time frames for emergence and different mechanisms underlying the emergence process. Lastly, we argue for a re-design of agro-ecosystems that embraces the concept of dynamic diversity to improve their resilience to pathogens. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

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Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species

Cited by 184 publications

References 49 publications

Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen

Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen

Reconstructing the Evolutionary History of Powdery Mildew Lineages (Blumeria graminis) at Different Evolutionary Time Scales with NGS Data

Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

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