Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector

Nature Plants volume 7, pages 198–208 (2021)Cite this article

Subjects

Abstract

Late blight caused by Phytophthora infestans greatly constrains potato production. Many Resistance (R) genes were cloned from wild Solanum species and/or introduced into potato cultivars by breeding. However, individual R genes have been overcome by P. infestans evolution; durable resistance remains elusive. We positionally cloned a new R gene, Rpi-amr1, from Solanum americanum, that encodes an NRC helper-dependent CC-NLR protein. Rpi-amr1 confers resistance in potato to all 19 P. infestans isolates tested. Using association genomics and long-read RenSeq, we defined eight additional Rpi-amr1 alleles from different S. americanum and related species. Despite only ~90% identity between Rpi-amr1 proteins, all confer late blight resistance but differentially recognize Avramr1 orthologues and paralogues. We propose that Rpi-amr1 gene family diversity assists detection of diverse paralogues and alleles of the recognized effector, facilitating durable resistance against P. infestans.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Map-based cloning of Rpi-amr1 and its resistance to P. infestans.
Fig. 2: Rpi-amr1 homologues and their phenotypes in transient assays.
Fig. 3: Differential recognition of Rpi-amr1 and Avramr1 homologues.
Fig. 4: Rpi-amr1 is NRC2- or NRC3-dependent.

Similar content being viewed by others

Data availability

Supporting raw reads were deposited in European Nucleotide Archive under project number PRJEB38240. BAC and Rpi-amr1 allele sequences were deposited in GenBank under accession numbers MW345286-95 and MW348763. Detailed accession information is shown in Supplementary Table 7. All the materials in this study are available upon request.

References

  1. World Food and Agriculture: Statistical Pocketbook 2019 (FAO, 2019).

  2. Saville, A. et al. Fungicide sensitivity of U.S. genotypes of Phytophthora infestans to six oomycete-targeted compounds. Plant Dis. 99, 659–666 (2015).

    Article  CAS  PubMed  Google Scholar 

  3. Malcolmson, J. F. & Black, W. New R genes in Solanum demissum lindl. And their complementary races of Phytophthora infestans (Mont.) de Bary. Euphytica 15, 199–203 (1966).

    Article  Google Scholar 

  4. Park, T.-H. et al. The late blight resistance locus Rpi-bib3 from Solanum bulbocastanum belongs to a major late blight R gene cluster on chromosome 4 of potato. Mol. Plant Microbe Interact. 18, 722–729 (2005).

    Article  CAS  PubMed  Google Scholar 

  5. Huang, S. et al. Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J. 42, 251–261 (2005).

    Article  CAS  PubMed  Google Scholar 

  6. Vossen, J. H. et al. The Solanum demissum R8 late blight resistance gene is an Sw-5 homologue that has been deployed worldwide in late blight resistant varieties. Theor. Appl. Genet. 129, 1785–1796 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Song, J. et al. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl Acad. Sci. USA 100, 9128–9133 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. van der Vossen, E. A. G. et al. The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homologue conferring broad-spectrum late blight resistance in potato. Plant J. 44, 208–222 (2005).

    Article  PubMed  Google Scholar 

  9. Pel, M. A. et al. Mapping and cloning of late blight resistance genes from Solanum venturii using an interspecific candidate gene approach. Mol. Plant Microbe Interact. 22, 601–615 (2009).

    Article  CAS  PubMed  Google Scholar 

  10. Foster, S. J. et al. Rpi-vnt1.1, a Tm-22 homologue from Solanum venturii, confers resistance to potato late blight. Mol. Plant Microbe Interact. 22, 589–600 (2009).

    Article  CAS  PubMed  Google Scholar 

  11. Jones, J. D. G., Vance, R. E. & Dangl, J. L. Intracellular innate immune surveillance devices in plants and animals. Science 354, aaf6395 (2016).

    Article  PubMed  Google Scholar 

  12. Wu, C.-H. et al. NLR network mediates immunity to diverse plant pathogens. Proc. Natl Acad. Sci. USA 114, 8113–8118 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fry, W. Phytophthora infestans: the plant (and R gene) destroyer. Mol. Plant Pathol. 9, 385–402 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Jones, J. D. G. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  PubMed  Google Scholar 

  15. Rehmany, A. P. et al. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17, 1839–1850 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Vleeshouwers, V. G. A. A. et al. Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS ONE 3, e2875 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Haas, B. J. et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393–398 (2009).

    Article  CAS  PubMed  Google Scholar 

  18. Armstrong, M. R. et al. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl Acad. Sci. USA 102, 7766–7771 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Stam, R., Silva Arias, G. A. & Tellier, A. Subsets of NLR genes show differential signatures of adaptation during colonization of new habitats. New Phytol. 224, 367–379 (2019).

    Article  CAS  PubMed  Google Scholar 

  20. Van de Weyer, A.-L. et al. A species-wide inventory of NLR genes and alleles in Arabidopsis thaliana. Cell 178, 1260–1272 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  21. McDowell, J. M. et al. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10, 1861–1874 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Liu, J. et al. Genetic variation and evolution of the Pi9 blast resistance locus in the AA genome Oryza species. J. Plant Biol. 54, 294–302 (2011).

    Article  Google Scholar 

  23. Ellis, J. G., Lawrence, G. J., Luck, J. E. & Dodds, P. N. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11, 495–506 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Seeholzer, S. et al. Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Mol. Plant Microbe Interact. 23, 497–509 (2010).

    Article  CAS  PubMed  Google Scholar 

  25. Saur, I. M. et al. Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism. eLife 8, 1957 (2019).

    Article  Google Scholar 

  26. Anderson, C. et al. Genome analysis and avirulence gene cloning using a high-density RADseq linkage map of the flax rust fungus, Melampsora lini. BMC Genomics 17, 667 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Jupe, F. et al. Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J. 76, 530–544 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Thilliez, G. J. A. et al. Pathogen enrichment sequencing (PenSeq) enables population genomic studies in oomycetes. New Phytol. 4, 903 (2018).

    Google Scholar 

  29. Jouet, A. et al. Albugo candida race diversity, ploidy and host-associated microbes revealed using DNA sequence capture on diseased plants in the field. New Phytol. 93, 959 (2018).

    Google Scholar 

  30. Witek, K. et al. Accelerated cloning of a potato late blight-resistance gene using RenSeq and SMRT sequencing. Nat. Biotechnol. 34, 656–660 (2016).

    Article  CAS  PubMed  Google Scholar 

  31. Lin, X. et al. Identification of Avramr1 from Phytophthora infestans using long read and cDNA pathogen-enrichment sequencing (PenSeq). Mol. Plant Pathol. 21, 1502–1512 (2020).

  32. Kamoun, S., van West, P., Vleeshouwers, V. G. A. A., de Groot, K. E. & Govers, F. Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10, 1413–1425 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Grund, E., Tremousaygue, D. & Deslandes, L. Plant NLRs with integrated domains: unity makes strength. Plant Physiol. 179, 1227–1235 (2019).

    Article  CAS  PubMed  Google Scholar 

  34. Chen, X. et al. Identification and rapid mapping of a gene conferring broad-spectrum late blight resistance in the diploid potato species Solanum verrucosum through DNA capture technologies. Theor. Appl. Genet. 131, 1287–1297 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Xu, X. et al. Genome sequence and analysis of the tuber crop potato. Nature 475, 189–195 (2011).

    Article  CAS  PubMed  Google Scholar 

  36. Wu, C.-H. et al. NRC4 gene cluster is not essential for bacterial flagellin-triggered immunity. Plant Physiol. 182, 455–459 (2020).

    Article  CAS  PubMed  Google Scholar 

  37. Adachi, H. et al. An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species. eLife 8, 121 (2019).

    Article  Google Scholar 

  38. Colon, L. T. et al. Resistance to potato late blight (Phytophthora infestans (Mont.) de Bary) in Solanum nigrum, S. villosum and their sexual hybrids with S. tuberosum and S. demissum. Euphytica 66, 55–64 (1992).

    Article  Google Scholar 

  39. Lebecka, R. Host–pathogen interaction between Phytophthora infestans and Solanum nigrum, S. villosum, and S. scabrum. Eur. J. Plant Pathol. 120, 233–240 (2007).

    Article  Google Scholar 

  40. Poczai, P. & Hyvönen, J. On the origin of Solanum nigrum: can networks help? Mol. Biol. Rep. 38, 1171–1185 (2010).

    Article  PubMed  Google Scholar 

  41. Ward, B. J. & van Oosterhout, C. HYBRIDCHECK: software for the rapid detection, visualization and dating of recombinant regions in genome sequence data. Mol. Ecol. Resour. 16, 534–539 (2016).

    Article  CAS  PubMed  Google Scholar 

  42. Vleeshouwers, V. G. A. A. et al. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 49, 507–531 (2011).

    Article  CAS  PubMed  Google Scholar 

  43. Vleeshouwers, V. G. A. A., van Dooijeweert, W., Govers, F., Kamoun, S. & Colon, L. T. The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans. Planta 210, 853–864 (2000).

    Article  CAS  PubMed  Google Scholar 

  44. Jones, J. D. G. et al. Elevating crop disease resistance with cloned genes. Philos. Trans. R. Soc. Lond. B 369, 20130087 (2014).

    Article  Google Scholar 

  45. Dodds, P. N. et al. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl Acad. Sci. USA 103, 8888–8893 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Jouet, A., McMullan, M. & van Oosterhout, C. The effects of recombination, mutation and selection on the evolution of the Rp1 resistance genes in grasses. Mol. Ecol. 24, 3077–3092 (2015).

    Article  CAS  PubMed  Google Scholar 

  47. Ohta, T. Gene conversion vs point mutation in generating variability at the antigen recognition site of major histocompatibility complex loci. J. Mol. Evol. 41, 115–119 (1995).

    Article  CAS  PubMed  Google Scholar 

  48. Spurgin, L. G. et al. Gene conversion rapidly generates major histocompatibility complex diversity in recently founded bird populations. Mol. Ecol. 20, 5213–5225 (2011).

    Article  CAS  PubMed  Google Scholar 

  49. Huang, J. et al. Phytophthora effectors modulate genome-wide alternative splicing of host mRNAs to reprogram plant immunity. Mol. Plant 13, 1470–1484 (2020).

  50. Sato, S. et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635–641 (2012).

    Article  CAS  Google Scholar 

  51. Steuernagel, B. et al. NLR-parser: rapid annotation of plant NLR complements. Bioinformatics 10, 1665–1667 (2015).

    Article  Google Scholar 

  52. Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Stanke, M. & Morgenstern, B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 33, W465–W467 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Li, H. et al. The sequence alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Koboldt, D. C. et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568–576 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Fiume, M., Williams, V., Brook, A. & Bioinformatics, M. B. Savant: genome browser for high-throughput sequencing data. Bioinformatics 25, 1938–1944 (2010).

    Article  Google Scholar 

  59. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-seq. Bioinformatics 25, 1105–1111 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kumar, A., Taylor, M. A., Arif, S. A. M. & Davies, H. V. Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: antisense plants display abnormal phenotypes. Plant J. 9, 147–158 (1996).

    Article  CAS  Google Scholar 

  61. Castel, B. et al. Diverse NLR immune receptors activate defence via the RPW8- NLR NRG1. New Phytol. 222, 966–980 (2019).

    Article  CAS  PubMed  Google Scholar 

  62. Thompson, J. D., Higgins, D. G., Gibson, T. J. & CLUSTAL, W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Kumar, S., Nei, M., Dudley, J. & Tamura, K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 9, 299–306 (2008).

    Article  CAS  PubMed  Google Scholar 

  64. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Gouy, M., Guindon, S. & Gascuel, O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27, 221–224 (2009).

    Article  PubMed  Google Scholar 

  66. Rozas, J. & Sánchez-DelBarrio, J. C. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497 (2009).

    Article  Google Scholar 

  67. Xia, X. DAMBE: a comprehensive software package for data analysis in molecular biology and evolution. Mol. Biol. Evol. 30, 1720–1728 (2013).

  68. Ratmann, O., Lam, H. M. & Boni, M. F. Improved algorithmic complexity for the 3SEQ recombination detection algorithm. Mol. Biol. Evol. 35, 247–251 (2017).

    PubMed Central  Google Scholar 

  69. Kent, W. J. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Phanstiel D. H. Sushi: Tools for visualizing genomics data. R package version 1.26.0 (2020).

  71. Champouret, N. et al. Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato. Mol. Plant Microbe Interact. 22, 1535–1545 (2009).

    Article  CAS  PubMed  Google Scholar 

  72. Cooke, D. E. L. et al. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathog. 8, e1002940 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was financed from BBSRC grant no. BB/P021646/1 and the Gatsby Charitable Foundation. This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the provision of a High-Performance Computing Cluster. We would like to thank TSL bioinformatics team, transformation team and horticultural team for their support. We thank Experimental Garden and Genebank of Radboud University (Nijmegen, the Netherlands), IPK Gatersleben (Germany) and S. Knapp (Natural History Museum, London, United Kingdom) for access to S. americanum, S. nigrescens and S. nigrum genetic diversity and G. Kessel, F. Govers and P. Birch for providing P. infestans isolates.

Author information

Author notes

  1. Hari S. Karki

    Present address: US Department of Agriculture–Agricultural Research Service, Madison, WI, USA

  2. Florian Jupe

    Present address: Bayer Crop Science, Chesterfield, MO, USA

  3. William Barrett

    Present address: The New Zealand Institute for Plant & Food Research Ltd, Nelson, New Zealand

  4. Chih-Hang Wu

    Present address: Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan

  5. Tianqiao Song

    Present address: Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, P. R. China

  6. These authors contributed equally: K. Witek, X. Lin, H. S. Karki.

Authors and Affiliations

  1. The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, UK

    Kamil Witek, Xiao Lin, Hari S. Karki, Florian Jupe, Agnieszka I. Witek, Sebastian Fairhead, Robert Heal, William Barrett, Chih-Hang Wu, Hiroaki Adachi, Tianqiao Song, Sophien Kamoun, Laurence Tomlinson & Jonathan D. G. Jones

  2. John Innes Centre, Norwich Research Park, Norwich, UK

    Burkhard Steuernagel & Brande B. H. Wulff

  3. Phytopathology, Technical University Munich, Freising, Germany

    Remco Stam

  4. School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, UK

    Cock van Oosterhout

  5. Faculty of Biological Sciences, University of Leeds, Leeds, UK

    Jonathan M. Cocker

  6. University of Hull, Hull, UK

    Jonathan M. Cocker

  7. Plant Breeding, Wageningen University and Research, Wageningen, the Netherlands

    Shivani Bhanvadia & Vivianne G. A. A. Vleeshouwers

Authors
  1. Kamil Witek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hari S. Karki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florian Jupe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Agnieszka I. Witek
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Burkhard Steuernagel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Remco Stam
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Cock van Oosterhout
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sebastian Fairhead
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Robert Heal
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jonathan M. Cocker
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Shivani Bhanvadia
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. William Barrett
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Chih-Hang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Hiroaki Adachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Tianqiao Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Sophien Kamoun
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Vivianne G. A. A. Vleeshouwers
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Laurence Tomlinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Brande B. H. Wulff
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Jonathan D. G. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

K.W., X.L., F.J., R.S., C.O. and J.D.G.J. designed the study. K.W., X.L., H.S.K., F.J., A.I.W., S.B., R.H., W.B., L.T. and T.S. performed the experiments. K.W., X.L., H.S.K., F.J., A.I.W., B.S., R.S., C.O., S.F. and J.M.C. analysed the data. K.W., X.L., H.S.K., F.J. and J.D.G.J. wrote the manuscript with input from all authors. V.G.A.A.V., B.B.H.W, C.-H.W., H.A. and S.K. contributed resources. All authors approved the manuscript.

Corresponding author

Correspondence to Jonathan D. G. Jones.

Ethics declarations

Competing interests

K.W., H.S.K., F.G.J. and J.D.G.J. are named inventors on a patent application (PCT/US2017/066691) pertaining to Rpi-amr1 that was filed by the 2Blades Foundation on behalf of the Sainsbury Laboratory. The other authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Erik Andreasson, Marc Ghislain and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–8 and Tables 1–4.

Reporting Summary

Supplementary Tables 5–7

Table 5. Population genetics summary statistics calculated for Rpi-amr1 and Avramr1 homologues. Table 6. Evidence of sequence exchange between Rpi-amr1 orthologues and paralogues from SP2273 using 3SEQ. An exact non-parametric mosaicism statistic algorithm was implemented in 3SEQ; we found statistical evidence of recombination (the null hypothesis of clonal evolution was rejected). Table 7. Accession numbers of all sequencing data in this study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Witek, K., Lin, X., Karki, H.S. et al. A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector. Nat. Plants 7, 198–208 (2021). https://doi.org/10.1038/s41477-021-00854-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-021-00854-9

This article is cited by

Search

Advanced search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research