Skip to main content
SpringerLink
Log in

Genetic mapping of rust resistance loci in biomass willow

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Rust diseases caused by Melampsora spp. represent a major threat to the productivity of short rotation coppice (SRC) willows grown for biomass, causing yield losses of up to 40%. The routine use of fungicide in SRC plantations is not a viable option because of economic and environmental considerations; thus, breeding for rust resistance is a major target for willow breeding programmes. To characterise the genetic basis of rust resistance in willow and provide targets for use in future marker-assisted selections, quantitative trait analyses were performed using a large full-sib mapping population (K8) which segregates for rust resistance and several other important agronomic traits. Rust resistance in field conditions was assessed in three consecutive years. For a more detailed genetic dissection, laboratory inoculation tests using isolates of two distinct and prevalent pathotypes (LET1 and LET5) were also performed. For field-based resistance, a major quantitative resistance locus, designated SRR1 (Salix Rust Resistance 1), was detected in addition to several quantitative trait loci (QTL) of more modest effect. Inoculation test data also supported an important role for SRR1. Specific interactions between particular rust isolates and different QTL were detected, and QTL that only influenced resistance in field conditions were identified. The QTL reported here represent an important basis for the future development of markers for use in willow breeding programmes. As the linkage map for the K8 population is anchored to the Populus trichocarpa genome sequence, a more efficient marker development for future fine-scale mapping and candidate gene identification is possible.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Åhman I (2007) Rust scorings in a plantation of Salix viminalis clones during ten consecutive years. Eur J Forest Pathol 28:251–258

    Article  Google Scholar 

  • Beavis WD (1994) The power and deceit of QTL experiments: lessons from comparative QTL studies. Proceedings of the 49th Annual Corn and Sorghum Industry Research Conference, Washington, DC, ASTA

  • Cervera MT, Gusmao J, Steenackers M, Peleman J, Storme V, Vanden Broeck A, Van Montagu M, Boerjan W (1996) Identification of AFLP molecular markers for resistance against Melampsora larici-populina in Populus. Theor Appl Genet 86:301–307

    Google Scholar 

  • Cullis BR, Gleeson AC (1991) Spatial analysis of field experiments —and extension to two dimensions. Biometrics 47:1449–1460

    Article  Google Scholar 

  • Cullis BR, Gogel BJ, Verbyla A, Thompson R (1998) Spatial analysis of multi-environment early generation variety trials. Biometrics 54:1–19

    Article  Google Scholar 

  • Dowkiw A, Bastien C (2004) Characterization of two major genetic factors controlling quantitative resistance to Melampsora larici-populina leaf rust in hybrid poplars: strain specificity, field expression, combined effects, and relationship with a defeated qualitative resistance gene. Phytopathology 94:1358–1367

    Article  PubMed  CAS  Google Scholar 

  • Dowkiw A, Husson C, Frey P, Pinon J, Bastien C (2003) Partial resistance to Melampsora larici-populina leaf rust in hybrid poplars: genetic variability in inoculated excised leaf disk bioassay and relationship with complete resistance. Phytopathology 93:421–427

    Article  PubMed  CAS  Google Scholar 

  • Gleeson AC, Cullis BR (1987) Residual maximum likelihood (REML) estimation of a neighbour model for field experiments. J Agric Biol Environ Stat 2:1–25

    Google Scholar 

  • Gullberg U, Ryttman H (1993) Genetics of field resistance to Melampsora in Salix viminalis. Eur J Forest Pathol 23:75–84

    Article  Google Scholar 

  • Hanley SJ (2003) Genetic mapping of important agronomic traits in biomass willow. Ph.D. thesis. University of Bristol, UK

  • Hanley S, Barker JHA, Van Ooijen JW, Aldam C, Harris SL, Åhman I, Larsson S, Karp A (2002) A genetic linkage map of willow (Salix viminalis) based on AFLP and microsatellite markers. Theor Appl Genet 105:1087–1096

    Article  PubMed  CAS  Google Scholar 

  • Hanley S, Mallott MD, Karp A (2006) Alignment of a Salix linkage map to the Populus genomic sequence reveals macrosynteny between willow and poplar genomes. Tree Genet Genomes 3:35–48

    Article  Google Scholar 

  • Johansson LKH, Alström S (2000) Field resistance to willow leaf rust Melampsora epitea in inter- and intraspecific hybrids of Salix viminalis and S. dasyclados. Eur J Plant Pathol 106:763–769

    Article  Google Scholar 

  • Jorge V, Dowkiw A, Faivre-Rampant P, Bastien C (2005) Genetic architecture of qualitative and quantitative Melampsora larici-populina leaf rust resistance in hybrid poplar: genetic mapping and QTL detection. New Phytol 167:113–127

    Article  PubMed  CAS  Google Scholar 

  • Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers B, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Larsson S (2001) Commercial varieties from the Swedish willow breeding programme. Asp Appl Biol 65:193–198

    Google Scholar 

  • Lefèvre F, Gouè-Mourier MC, Faivre-Rampant P, Villar M (1998) A single gene cluster controls incompatibility and partial resistance to various Melampsora larici-populina races in hybrid poplars. Phytopathology 88:156–163

    Article  PubMed  Google Scholar 

  • Lehmann EL (1975) Nonparametrics. McGraw-Hill, New York

    Google Scholar 

  • Lescot M, Rombauts S, Zhang J, Aubourg S, Mathe C, Jansson S, Rouze P, Boerjan W (2004) Annotation of a 95-kb Populus deltoides genomic sequence reveals a disease resistance gene cluster and novel class I and class II transposable elements. Theor Appl Genet 109:10–22

    Article  PubMed  CAS  Google Scholar 

  • Maliepaard C, Van Ooijen JW (1994) QTL mapping in a full-sib family of an outcrossing species. In: Van Ooijen JW, Jansen J (eds) Biometrics in plant breeding: applications of molecular markers. Proceedings of the 9th Meeting EUCARPIA Section Biometrics and Plant Breeding. Plant Research International, Wageningen, pp 140–146

    Google Scholar 

  • McCracken AR, Dawson WM (1998) Short rotation coppice willow in Northern Ireland since 1973: development of the use of mixtures in the control of foliar rust (Melampsora spp.). Eur J Forest Pathol 28:241–251

    Article  Google Scholar 

  • McCracken AR, Dawson WM, Watson S, Allen CY (2000) Pathotype composition in Melampsora epitea populations occurring on willow (Salix) grown in mixed and monoculture plantations. Eur J Plant Pathol 106:879–886

    Article  Google Scholar 

  • Newcombe G, Bradshaw HD, Chastagner GA, Stettler RF (1996) A major gene for resistance to Melampsora medusa f. sp. deltoidae in a hybrid poplar pedigree. Phytopathology 86:87–94

    Article  CAS  Google Scholar 

  • Parker SR, Royle DJ, Hunter T (1993) Impact of Melampsora rust on yield of biomass willows. In: Abstracts of the 6th International Congress of Plant Pathology, Montreal, Canada, 28 July–6 Aug 1993, National Research Council Canada, Ottawa, ON, Canada, p 117

  • Patterson HD, Thompson R (1971) Recovery of inter-block information when block sizes are unequal. Biometrika 58:545–554

    Article  Google Scholar 

  • Pei MH, Royle DJ, Hunter T (1996) Pathogenic specialization in Melampsora epitea var. epitea on Salix. Plant Pathol 45:679–690

    Article  Google Scholar 

  • Pei MH, Hunter T, Ruiz C (1999) Occurrence of Melampsora rusts in biomass willow plantations for renewable energy in the United Kingdom. Biomass Bioenergy 17:153–163

    Article  Google Scholar 

  • Pei MH, Yuan ZW, Hunter T, Ruiz C (2000) Heterogeneous nature of a ‘new’ pathotype of Melampsora rust on Salix revealed by AFLP. Eur J Plant Pathol 106:771–779

    Article  Google Scholar 

  • Pei MH, Lindegaard KN, Hunter T, Ruiz C (2001) Preliminary studies of inheritance of rust resistance in biomass willows. Asp Appl Biol 65:281–288

    Google Scholar 

  • Pei MH, Lindegaard K, Ruiz C, Bayon C (2008) Rust resistance of some varieties and recently bred genotypes of biomass willows. Biomass Bioenergy 32:453–459

    Article  Google Scholar 

  • Pei MH, Ruiz C, Shield I, Macalpine W, Lindegaard K, Bayon C, Karp A (2010) Mendelian inheritance of rust resistance to Melampsora larici-epitea in crosses between Salix sachalinensis and S. viminalis. Plant Pathol 59:862–872

    Article  Google Scholar 

  • Pinon J, Frey P (2005) Interactions between poplar clones and Melampsora populations and their implications for breeding for durable resistance. In: Pei MH, McCracken AR (eds) Rust diseases of willow and poplar. CABI, Cambridge, pp 139–154

    Chapter  Google Scholar 

  • Robinson DL, Thompson R, Digby PGN (1982) REML—a program for the analysis of non-orthogonal data by restricted maximum likelihood. Proceedings in computational statistics, part II (supplement). Physica, Vienna, pp 231–232

    Google Scholar 

  • Rönnberg-Wästljung AC, Gullberg U (1999) Genetics of breeding characters with possible effects on biomass production in Salix viminalis (L.). Theor Appl Genet 98:531–540

    Article  Google Scholar 

  • Rönnberg-Wästljung AC, Samils B, Tsarouhas V, Gullberg U (2008) Resistance to Melampsora larici-epitea leaf rust in Salix: analyses of quantitative trait loci. J Appl Genet 49:321–331

    Article  PubMed  Google Scholar 

  • Searle SR, Casella G, McCulloch CE (1992) Variance components. Wiley, New York

    Book  Google Scholar 

  • Stirling B, Newcombe G, Vrebalov J, Bosdet I, Bradshaw HDJ (2001) Suppressed recombination around the MXC3 locus, a major gene for resistance to poplar leaf rust. Theor Appl Genet 103:1129–1137

    Article  CAS  Google Scholar 

  • Tsarouhas V, Gullberg U, Lagercrantz U (2002) An AFLP and RFLP linkage map and quantitative trait locus (QTL) analysis of growth traits in Salix. Theor Appl Genet 105:277–288

    Article  PubMed  CAS  Google Scholar 

  • Tsarouhas V, Gullberg U, Lagercrantz U (2004) Mapping of quantitative trait loci (QTLs) affecting autumn freezing resistance and phenology in Salix. Theor Appl Genet 108:1335–1342

    Article  PubMed  CAS  Google Scholar 

  • Villar M, Lefèvre F, Bradshaw HDK, Tessier du Cros E (1996) Molecular genetics of rust resistance in poplars (Melampsora larici-populina Kleb./Populus sp.) by bulked segregant analysis in a 2 × 2 factorial mating design. Genetics 143:531–536

    PubMed  CAS  Google Scholar 

  • Yin TM, DiFazio SP, Gunter LE, Jawdy SS, Boerjan W, Tuskan GA (2004) Genetic and physical mapping of Melampsora rust resistance genes in Populus and characterization of linkage disequilibrium and flanking genomic sequence. New Phytol 164:95–105

    Article  CAS  Google Scholar 

  • Yin T, DiFazio SP, Gunter LE, Zhang X, Sewell MM, Woolbright SA, Allan GJ, Kelleher CT, Douglas CJ, Wang M, Tuskan GA (2008) Genome structure and emerging evidence of an incipient sex chromosome in Populus. Genome Res 18:422–430

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Steenackers M, Storme V, Neyrink S, Van Montagu M, Gerats T, Boerjan W (2001) Fine mapping and identification of nucleotide binding site/leucine-rich repeat sequences at the Mer locus in Populus deltoides ‘S9-2’. Phytopathology 91:1069–1073

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the Department of Trade and Industry’s Renewable Energy Programme, UK (Agreement No. B/W6/00599/00/00), and later as part of the BEGIN (Biomass for Energy Genetic Improvement Network) project (UK Department of Environment, Food and Rural Affairs (Defra)—project no. NF0424). We also acknowledge additional funding support from the Biotechnology and Biological Sciences Research Council of the United Kingdom’s Institute Strategic Programme Grant for Rothamsted Research’s Centre for Bioenergy and Climate Change. Rothamsted Research is an institute of the Biotechnology and Biological Sciences Research Council of the UK.

Author information

Authors and Affiliations

  1. Centre for Bioenergy and Climate Change, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK

    Steven J. Hanley, Ming H. Pei, Carmen Ruiz, Mark D. Mallott & Angela Karp

  2. Centre for Mathematical and Computational Biology, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK

    Stephen J. Powers

  3. Centre for Crop Genetic Improvement, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK

    Jacqueline H. A. Barker

Authors
  1. Steven J. Hanley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming H. Pei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen J. Powers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carmen Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mark D. Mallott
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jacqueline H. A. Barker
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Angela Karp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven J. Hanley.

Additional information

Communicated by W. Boerjan

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hanley, S.J., Pei, M.H., Powers, S.J. et al. Genetic mapping of rust resistance loci in biomass willow. Tree Genetics & Genomes 7, 597–608 (2011). https://doi.org/10.1007/s11295-010-0359-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-010-0359-x

Keywords

Search

Navigation