The wheat powdery mildew genome shows the unique evolution of an obligate biotroph

Journal name:
Nature Genetics
Volume:
45,
Pages:
1092–1096
Year published:
DOI:
doi:10.1038/ng.2704
Received
Accepted
Published online

Wheat powdery mildew, Blumeria graminis forma specialis tritici, is a devastating fungal pathogen with a poorly understood evolutionary history. Here we report the draft genome sequence of wheat powdery mildew, the resequencing of three additional isolates from different geographic regions and comparative analyses with the barley powdery mildew genome. Our comparative genomic analyses identified 602 candidate effector genes, with many showing evidence of positive selection. We characterize patterns of genetic diversity and suggest that mildew genomes are mosaics of ancient haplogroups that existed before wheat domestication. The patterns of diversity in modern isolates suggest that there was no pronounced loss of genetic diversity upon formation of the new host bread wheat 10,000 years ago. We conclude that the ready adaptation of B. graminis f.sp. tritici to the new host species was based on a diverse haplotype pool that provided great genetic potential for pathogen variation.

At a glance

Figures

  1. Comparison of 5,258 bidirectionally most closely related B. graminis f.sp. tritici and B. graminis f.sp. hordei homologs.
    Figure 1: Comparison of 5,258 bidirectionally most closely related B. graminis f.sp. tritici and B. graminis f.sp. hordei homologs.

    The x axis indicates the ratio of nonsynonymous to synonymous substitutions (dN/dS) for all gene pairs, and the y axis indicates the number of gene pairs in each class. The red series represents the 237 gene pairs of bidirectionally most closely related B. graminis f.sp. tritici and B. graminis f.sp. hordei homologs encoding CSEPs, and the blue series represents all 5,021 other gene pairs. For better visibility, the numbers for non-CSEP genes were divided by 10.

  2. Presence-absence polymorphisms and genome sequence variation between B. graminis f.sp. tritici isolates.
    Figure 2: Presence-absence polymorphisms and genome sequence variation between B. graminis f.sp. tritici isolates.

    (a) A map of the reference genome sequence of isolate 96224 is shown at the top. Isolate 94202 differs from the reference genome in the absence of the BgtE-5419 gene. The gene was lost in a deletion that removed over 8 kb. Homologous regions in the two isolates are connected with blue lines. The presence of a nearly identical 23-bp motif (signatures 1 and 2) precisely bordering the deleted fragment indicates that the deletion is the result of a double-strand break (Supplementary Note). SINE, short-interspersed nuclear element. (b) The candidate effector gene BgtE-5692 contains a highly divergent segment covering parts of exons 1 and 2 (gray boxes) as well as the intron. The small size of the divergent fragment suggests that it was introduced through gene conversion. SNPs are represented by blue vertical lines. Three SNPs that result in amino acid changes are indicated with red arrowheads. The sequence assemblies of both isolates 94202 and JIW2 contain a 110-bp gap in the 5′ region of the gene, indicating a deletion. (c,d) The B. graminis f.sp. tritici genome is a mosaic of different haplogroups. The reference genome sequence of isolate 96224 is shown at the top, and the three resequenced isolates are shown below (in arbitrary order). Positions of SNPs are indicated with colored vertical lines. Priority was assigned top to bottom. For example, all nucleotide differences between JIW2 and the reference isolate 96224 are shown in red. If one of the other two isolates shares a SNP with JIW2, this SNP is also shown in red. Groups of SNPs of the same color indicate extensive chromosomal segments that originate from a different haplogroup. (c) Large parts of the B. graminis f.sp. tritici genome are a complex mosaic of haplogroup segments that are dozens of kilobases long. (d) Examples of extensive regions of shared haplogroups.

  3. Divergence time estimates of genomic regions derived from different haplogroups.
    Figure 3: Divergence time estimates of genomic regions derived from different haplogroups.

    (a) Haplogroup segments in the genomes of the three resequenced B. graminis f.sp. tritici isolates were divided into regions derived from a young (Hyoung) and a more ancient (Hold) haplogroup relative to the 96224 reference isolate. Divergence time estimates were calculated individually for each of the 250 fingerprint (FP) contigs comprise the genome. The x axis shows ranges of divergence time estimates (with only every second age range labeled owing to space constraints), and the y axis shows how many FP contigs fall in the respective age categories. (b) Model for the evolution of powdery mildew isolates. The divergence and recombination of haplogroups is correlated to events such as the onset of agriculture and increasing temperatures (represented by the color of the arrow to the right).

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Author information

  1. These authors contributed equally to this work.

    • Thomas Wicker &
    • Simone Oberhaensli

Affiliations

  1. Institute of Plant Biology, University of Zurich, Zurich, Switzerland.

    • Thomas Wicker,
    • Simone Oberhaensli,
    • Francis Parlange,
    • Jan P Buchmann,
    • Margarita Shatalina,
    • Stefan Roffler,
    • Roi Ben-David,
    • Kentaro K Shimizu &
    • Beat Keller
  2. Centre of the Region Hana for Biotechnological and Agricultural Research, Institute of Experimental Botany, Olomouc-Holice, Czech Republic.

    • Jaroslav Doležel &
    • Hana Šimková
  3. Department of Plant Microbe Interactions, Max-Planck Institute for Plant Breeding Research, Cologne, Germany.

    • Paul Schulze-Lefert &
    • Emiel Ver Loren van Themaat
  4. Department of Life Sciences, Imperial College London, London, UK.

    • Pietro D Spanu
  5. Department of Biology, University of Bern, Bern, Switzerland.

    • Rémy Bruggmann
  6. Institut National de la Recherche Agronomique (INRA), Unité de Recherche Génomique Info (URGI), Versailles, France.

    • Joelle Amselem &
    • Hadi Quesneville
  7. Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.

    • Timothy Paape &
    • Kentaro K Shimizu
  8. Present addresses: MTT/BI Plant Genomics Laboratory, University of Helsinki, Helsinki, Finland (J.P.B.) and Department of Agronomy and Natural Resources, Institute of Plant Sciences, Agronomy and Natural Resources (ARO), The Volcani Center, Bet Dagan, Israel (R.B.-D.).

    • Jan P Buchmann &
    • Roi Ben-David

Contributions

B.K., T.W. and K.K.S. designed the project. S.O., T.W., J.P.B., M.S., T.P. and S.R. designed software and analyzed the genome sequence. R.B. performed genome sequence assemblies. F.P. and R.B.-D. designed and performed crossing experiments. P.S.-L. and E.V.L.v.T. identified CSEPs. J.A. and H.Q. performed repeat analysis. J.D. and H.Š. constructed the BAC library. K.K.S. and P.D.S. discussed and commented on results and edited the manuscript. S.O., T.W. and B.K. wrote the manuscript and supplementary information and prepared the figures.

Competing financial interests

The authors declare no competing financial interests.

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Supplementary information

PDF files

  1. Supplementary Text and Figures (8,840.5)

    Supplementary Figures 1–13, Supplementary Tables 1–10 and Supplementary Note

Excel files

  1. Supplementary Table 11 (1,358.8)

    Results of MK tests in CSEP/CEP genes

  2. Supplementary Table 12 (1,466.8)

    Results of MK tests in non-CSEP/CEP genes

Additional data