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Convergent molecular evolution among ash species resistant to the emerald ash borer

Nature Ecology & Evolution volume 4, pages 1116–1128 (2020)Cite this article

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Abstract

Recent studies show that molecular convergence plays an unexpectedly common role in the evolution of convergent phenotypes. We exploited this phenomenon to find candidate loci underlying resistance to the emerald ash borer (EAB, Agrilus planipennis), the United States’ most costly invasive forest insect to date, within the pan-genome of ash trees (the genus Fraxinus). We show that EAB-resistant taxa occur within three independent phylogenetic lineages. In genomes from these resistant lineages, we detect 53 genes with evidence of convergent amino acid evolution. Gene-tree reconstruction indicates that, for 48 of these candidates, the convergent amino acids are more likely to have arisen via independent evolution than by another process such as hybridization or incomplete lineage sorting. Seven of the candidate genes have putative roles connected to the phenylpropanoid biosynthesis pathway and 17 relate to herbivore recognition, defence signalling or programmed cell death. Evidence for loss-of-function mutations among these candidates is more frequent in susceptible species than in resistant ones. Our results on evolutionary relationships, variability in resistance, and candidate genes for defence response within the ash genus could inform breeding for EAB resistance, facilitating ecological restoration in areas invaded by this beetle.

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Fig. 1: Fraxinus species’ resistance to EAB in bioassays.
Fig. 2: Species-tree for the genus Fraxinus.
Fig. 3: Predicted protein structure for OG15551.

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Data availability

Underlying data for Fig. 1 are available in Supplementary Tables 1 and 2. All trimmed read data and genome assemblies have been deposited in the European Nucleotide Archive under accession no. PRJEB20151. The genome assemblies are also available to download at: http://www.ashgenome.org.

Code availability

The custom scripts used is this study have been deposited in GitHub: https://github.com/lkelly3/eab-ms-scripts.

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Acknowledgements

This research used Queen Mary’s Apocrita HPC facility, supported by QMUL Research-IT (https://doi.org/10.5281/zenodo.438045). We thank J. Carlson for providing F. pennsylvanica DNA; T. Baxter, S. Brockington, P. Brownless, D. Crowley, S. Honey, R. Irvine, R. Jinks, P. Jones, T. Kirkham, H. McAllister, I. Parkinson and S. Redstone for help with obtaining Fraxinus materials from UK collections; T. Poland for providing EAB eggs; M. Miller for propagating trees for the bioassays; R. Matko for preparation of voucher specimens; J. Pellicer for advice on flow cytometry; P. Howard and M. Struebig for advice on DNA extractions; J. Keilwagen for help with GeMoMa; K. Davies and J. Parker for help with convergence analysis software; the Evolution Labchat group and Rossiter Lab at QMUL for discussions; and R. Rose and J. Sayers for advice on protein-modelling analyses. This project was funded by the Living with Environmental Change Tree Health and Plant Biosecurity Initiative – Phase 2 (grant no. BB/L012162/1), funded jointly by BBSRC, Defra, ESRC, Forestry Commission, NERC and the Scottish Government. R.J.A.B. acknowledges additional support from the DEFRA Future Proofing Plant Health scheme. R.J.A.B. and L.J.K. acknowledge additional support from the Erica Waltraud Albrecht Endowment Fund. W.J.P. was funded by the Walsh Scholarship Programme of the Department of Agriculture, Food and the Marine, Ireland. E.D.C. was supported by the Marie Skłodowska-Curie Individual Fellowship ‘FraxiFam’ (grant agreement no. 660003).

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  1. William Crowther

    Present address: School of Life Sciences, The University of Warwick, Coventry, UK

Authors and Affiliations

  1. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Laura J. Kelly, William J. Plumb, Endymion D. Cooper, William Crowther, Stephen J. Rossiter & Richard J. A. Buggs

  2. Royal Botanic Gardens, Kew, Richmond, UK

    Laura J. Kelly, William J. Plumb & Richard J. A. Buggs

  3. Forestry Development Department, Teagasc, Dublin, Republic of Ireland

    William J. Plumb

  4. United States Department of Agriculture, Forest Service, Northern Research Station, Delaware, OH, USA

    David W. Carey, Mary E. Mason & Jennifer L. Koch

  5. United States Department of Agriculture, Agricultural Research Service, US National Arboretum, Washington, DC, USA

    Alan T. Whittemore

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Contributions

R.J.A.B. conceived and oversaw the project. L.J.K. and R.J.A.B. wrote the manuscript, with input from J.L.K., W.J.P. and S.J.R. L.J.K. conducted gene annotation, orthologue inference, convergence analyses, calling and analysis of variants, GO enrichment analysis and phylogenetic analyses. L.J.K., W.C. and A.T.W. performed genome size estimation by flow cytometry. L.J.K., W.C., E.D.C. and D.W.C. extracted DNA. L.J.K. and E.D.C. assembled the genomes. J.L.K. conceived and oversaw the EAB bioassays. D.W.C. conducted the EAB bioassays. J.L.K. and M.E.M. analysed EAB bioassay data. W.J.P. conducted protein-modelling analyses. S.J.R. advised on convergence analyses.

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Correspondence to Laura J. Kelly or Richard J. A. Buggs.

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Extended data

Extended Data Fig. 1 Predicted protein structures for selected candidate loci.

a, Predicted protein structure for OG36502, modelled using the protein sequence for Fraxinus platypoda. The serine/asparagine variant at the site where convergence was detected is highlighted; the serine is a putative phosphorylation site. b, Predicted protein structure for OG40061, modelled using the protein sequence for F. mandshurica. The asparagine/serine variant at the site where convergence was detected is highlighted; the serine is a putative phosphorylation site. The putative substrate, NADP, is shown docked within the predicted active site. c, Predicted protein structure for OG38407, modelled using the protein sequence for F. mandshurica. The aspartic acid/asparagine variant at the site where convergence was detected is highlighted; the site falls within a leucine rich repeat region (LRR; shaded blue) which is predicted to span from position 111–237 within the protein sequence (detected using the GenomeNet MOTIF tool (www.genome.jp/tools/motif/), searching against the NCBI-CDD and Pfam databases with default parameters; the LRR region was identified as positions 111–237 with an e-value of 1e-05). d, Predicted protein structure for OG21033, modelled using the protein sequence for F. platypoda. The lysine/glutamine at the site where convergence was detected is highlighted. The putative substrate, β-D-Glcp-(1 → 3)-β-D-GlcpA-(1 → 4)-β-D-Glcp, is shown docked within the predicted active site.

Supplementary information

Supplementary Information

Supplementary Figs. 1–2 and Notes 1–6.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–10.

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Kelly, L.J., Plumb, W.J., Carey, D.W. et al. Convergent molecular evolution among ash species resistant to the emerald ash borer. Nat Ecol Evol 4, 1116–1128 (2020). https://doi.org/10.1038/s41559-020-1209-3

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