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Interactions of Fr genes and mixed-pathogen inocula in the loblolly pine-fusiform rust pathosystem

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Abstract

Open-pollinated loblolly pine seedlings derived from seven maternal parents were inoculated in a greenhouse with 10 different bulked inocula of the fusiform rust fungus and assessed for disease incidence. The maternal parents are heterozygous (Rr) for one or two of nine known pathotype-specific Fr genes (fusiform rust resistance genes). Progeny were genotyped to identify carriers of known R and r alleles inherited from the maternal parents. The R alleles condition resistance to specific genotypes of the fungal pathogen, while r alleles do not condition for resistance. Interactions were tested among different host genotypes and different bulked inocula. Significant differences in virulence against R genotypes were observed in the bulked inocula. Likewise, the inocula were significantly different with regard to their ability to incite disease at the family level and in r genotypes. Across the inocula, disease levels differed significantly among families. Within each family, r genotype seedlings typically exhibited higher disease rates than did R genotype seedlings. The magnitude of difference (odds ratio) between the R versus r genotypes for disease incidence within each family varied from 1 to 32 times. Significant interactions between host and pathogen genotypes were observed in four of the seven families. These greenhouse assessments using bulked inocula sources revealed wide ranges of pathogen virulence levels against the different R alleles. Barring virulence masking by unknown resistance genes, similar virulence assessments should be effective guides for the field deployment of seedlings carrying specific R alleles to regions where inocula samples show low or no corresponding virulence.

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References

  • Amerson HV, Kubisiak TL, Garcia SA, Kuhlman GC, Nelson CD, McKeand SE, Mullin TJ, Li B (2005) Interacting genes in the pine-fusiform rust forest pathosystem. In: Proceedings of the 28th biennial southern forest tree improvement conference, June 21–23, 2005. Raleigh, NC: U.S. Department of Agriculture, Forest Service, p. 60. Available at http://www.treesearch.fs.fed.us/pubs/25641

  • Bent AF, Mackey D (2007) Elicitors, Effectors, and R Genes: The New Paradigm and a Lifetime Supply of Questions. Annu Rev Phytopathol 45:399–436

    Article  PubMed  CAS  Google Scholar 

  • Bridgwater F, Kubisiak T, Byram T, McKeand S (2005) Risk management with current deployment strategies for genetically improved loblolly and slash pines. South J Appl For 29(2):80–87

    Google Scholar 

  • Crute IR (1992) The role of resistance breeding in the integrated control of downy mildew (Bremia lactuca) in protected lettuce. Euphytica 63:95–102

    Article  Google Scholar 

  • Cubbage F, Pye J, Holmes T, Wagner J (2000) An economic analysis of fusiform rust protection research. South J Appl For 24:77–85

    Google Scholar 

  • Geron CD, Hafley LH (1988) Impact of fusiform rust on product yields of loblolly pine plantations. South J Appl For 12:226–231

    Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: Evolution and Utilization. Annu Rev Phytopathol 39:285–312

    Article  PubMed  CAS  Google Scholar 

  • Isik F, Amerson HV, Whetten RW, Garcia SA, Li B, McKeand S (2008) Resistance Assessments of Elite Loblolly Pine Families to Fusiform Rust Inocula in Greenhouse Testing. Can J For Res 38:2687–2696

    Article  Google Scholar 

  • Jordan AP (1997) Fusiform rust disease resistance and genomic mapping in loblolly pine. MS thesis. N.C. State Univ. Raleigh, NC. 105 pp

  • Kinloch BB Jr, Walkinshaw CH (1991) Resistance to fusiform rust in southern pines: How is it inherited? In: Hiratsuka Y, Samoil JK, Blenis PV, Crane PE, Laishley BL (eds) Proceedings of the IUFRO Rusts of Forest Trees Working Party Conference; Edmonton, Alberta, Canada. Northwest Region Information Report NOR-X-317: 219–228

  • Knighten JL, Young CH, McCartney TC, Anderson RL (1988) Resistance screening center procedures manual: a step by step guide used in the operational screening of southern pines for resistance to fusiform rust. USDA Forest Service Forest Pest Management. Report 83-1-18 (Revised 1988) 62 p

  • Kubisiak TL, Amerson HV, Nelson CD (2005) Genetic interaction of the fusiform rust fungus with resistance gene Fr1 in loblolly pine. Phytopathology 95:376–380

    Article  PubMed  CAS  Google Scholar 

  • Kubisiak TL, Anderson CL, Amerson HV, Smith JA, Davis JM, Nelson CD (2011) A genomic map enriched for markers linked to Avr1 in Cronartium quercuum f.sp. fusiforme. Fungal Genet Biol 48:266–274

    Article  PubMed  CAS  Google Scholar 

  • Kuhlman EG, Matthews FR (1993) Variation in virulence among single-aeciospore isolates from single-gall isolates of Cronartium quercuum f.sp. fusiforme. Can J For Res 23:67–71

    Article  Google Scholar 

  • Kuhlman EG, Amerson HV, Jordan AP, Pepper WP (1997) Inoculum density and expression of major gene resistance to fusiform rust disease in loblolly pine. Plant Dis 81:597–600

    Article  Google Scholar 

  • Li H (2003) Major gene detection for fusiform rust resistance using segregation analysis and linkage analysis in loblolly pine. Ph.D. Thesis N.C. State Univ. Raleigh, N.C. 130p

  • Li H, Ghosh S, Amerson H, Li B (2006) Major gene detection for fusiform rust resistance using Bayesian complex segregation analysis in loblolly pine. Theor Appl Genet 113:921–929

    Article  PubMed  CAS  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute, Cary, p 814

    Google Scholar 

  • McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Ann Rev Phytopathol 40:349–379

    Article  CAS  Google Scholar 

  • McIntosh RA (1992) Preemptive breeding to control wheat rusts. Euphytica 63:103–113

    Article  Google Scholar 

  • Millar CI, Kinloch, BB (1991) Taxonomy, phylogeny, and coevolution of pines and their stem rusts. In: Hiratsuka, Y., Samoil, J.K., Blenis, P.V., Crane, P.E., Laishley, B.L., eds., Proceedings of the IUFRO Rusts of Forest Trees Working Party Conference; Edmonton, Alberta, Canada. Northwest Region Information Report NOR-X-317: 1–38

  • Myburg H, Morse AM, Amerson HV, Kubisiak TL, Huber D, Osborne JA, Garcia SA, Nelson CD, Davis JM, Covert SF, van Zyl LM (2006) Differential gene expression in loblolly pine (Pinus taeda L.) challenged with the fusiform rust fungus, Cronartium quercuum f.sp. fusiforme. Physiol Mol Plant Pathol 68:79–91

    Article  CAS  Google Scholar 

  • Nelson CD, Doudrick RL, Nance WL, Hamaker JM, Capo B (1993) Specificity of host:pathogen genetic interaction for fusiform rust disease on slash pine. In: Proceedings of the 22nd Southern Forest Tree Improvement Conference, June 14–17, 1993, Atlanta, Georgia, USA, pp 403–411

  • Nelson CD, Amerson HV, Kubisiak TL (2010) Unraveling and managing fusiform rust disease: a model approach for coevolved forest tree pathosystems. For Path 40:67–72

    Article  Google Scholar 

  • Powers HR Jr, Kraus JF (1986) A comparison of fusiform rust-resistant loblolly pine seed sources. South J Appl For 10:230–232

    Google Scholar 

  • SAS Institute (2010) SAS/STAT version 92: Help and Documentation. SAS Institute, Cary

    Google Scholar 

  • Stelzer HE, Doudrick RL, Kubisiak TL, Nelson CD (1999) Prescreening Slash Pine and Cronartium Pedigrees for Evaluation of Complementary Gene Action in Fusiform Rust Disease. Plant Dis 83:385–389

    Article  Google Scholar 

  • Walkinshaw CH, Bey CF (1981) Reaction of field-resistant slash pine to selected isolates of Cronartium quercuum f.sp. fusiforme. Phytopathology 71:1090–1092

    Article  Google Scholar 

  • Wilcox PL, Amerson HV, Kuhlman EG, Liu BH, O’Malley DM, Sederoff RR (1996) Detection of a major gene for resistance to fusiform rust disease in loblolly pine by genomic mapping. Proc Natl Acad Sci USA 93:3859–3864

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Fikret Isik.

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Communicated by G. G. Vendramin

Henry V. Amerson - retired.

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Isik, F., Amerson, H.V., Whetten, R.W. et al. Interactions of Fr genes and mixed-pathogen inocula in the loblolly pine-fusiform rust pathosystem. Tree Genetics & Genomes 8, 15–25 (2012). https://doi.org/10.1007/s11295-011-0416-0

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  • DOI: https://doi.org/10.1007/s11295-011-0416-0

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