White pine blister rust (WPBR) is an exotic disease threatening five-needle pines in North America. In spite of its relatively recent introduction, some five-needle pines such as sugar pine (Pinus lambertiana) have developed both complete (major) gene resistance and partial (quantitative) resistance to WPBR. While significant effort has been dedicated to clone and locate the position of the major gene of WPBR resistance in sugar pine, the genetic basis of quantitative resistance remains largely unknown in all Strobus pines. In this work, we took a preliminary approach to identify potential genotype × phenotype associations using the results of long-term survival and symptoms of infection in both experimental and applied breeding populations. Our study found significant associations between several genes and WPBR disease symptoms such as normal active cankers and blights, important symptoms in the development of partial resistance. No significant associations were found with percentage of survival, probably due to the complex inheritance of the disease and long time to infection. With this study, we hope to lay the ground for further genome-wide association studies using large phenotypic data sets in sugar pine and other Strobus pines.
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Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Denslow SA, Walls AA, Daub ME (2005) Regulation of biosynthetic genes and antioxidant properties of vitamin B6 vitamers during plant defense responses. Physiol Mol Plant Pathol 66:244–255
Devey ME, Delfino-Mix A, Kinloch BB, Neale DB (1995) Random amplified polymorphic DNA markers tightly linked to a gene for resistance to white pine blister rust in sugar pine. PNAS 92:2066–2070
Earl D, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361
Eckert AJ, Maloney PE, Vogler DR, Jensen CE, Delfino Mix A, Neale DB (2015) Local adaptation at fine scales: an example from sugar pine (Pinus lambertiana, Pinaceae). Tree Genet Genomes 11:42
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620
Flint-Garcia S, Thuillet A-C, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J: Cell Mol Biol 44:1054–1064
Gernandt DS, Vázquez-Lobo A (2014) Conifers, the most diverse group of naked seed plants. In Vargas P, Zardoya R (eds). The tree of life. Sinauer Associates, Inc. pp. 122–131
Gonzalez-Ibeas D, Martinez-Garcia PJ, Famula R, Delfino-Mix A, Stevens KA, Loopstra CA, Langley C, Neale DB (2016) Assessing the gene content of the megagenome: sugar pine (Pinus lamertiana). G3: Genes Genomes Genetics 6(12):3787–3802
Harkins DM, Johnson GN, Skaggs PA, Mix AD, Dupper GE, Devey ME, Kinloch BB, Neale DB (1998) Saturation mapping of a major gene for resistance to white pine blister rust in sugar pine. Theor Appl Genet 97:1355–1360
Jermstad KD, Sheppard LA, Kinloch BB, Delfino-Mix A, Ersoz ES, Krutovsky KV, Neale DB (2006) Isolation of a full-length CC-NBS-LRR resistance gene analog candidate from sugar pine showing low nucleotide diversity. Tree Genet Genomes 2:76–85
Jermstad KD, Eckert AJ, Wegrzyn JL, Delfino-Mix A, Da D, Burton DC, Neale DB (2011) Comparative mapping in Pinus: sugar pine (Pinus lambertiana Dougl.) and loblolly pine (Pinus taeda L.) Tree Genet Genomes 7:457–468
Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics. https://doi.org/10.1093/bioinformatics/btr521
Kim MS, Klopfenstein NB, Ota Y, Lee SK, Woo KS, Kaneko S (2010) White pine blister rust in Korea, japan and other Asian regions: comparisons and implications for North America. For Pathol 40:382–401
Kinloch BB, Littlefield JL (1977) White pine blister rust: hypersensitive resistance in sugar pine. Can J Bot 55:1148–1155
Kinloch BB, Dupper GE (2002) Genetic specificity in the white pine-blister rust pathosystem. Phytopathology 92:278–280
Kinloch BB (2003) White pine blister rust in North America: past and prognosis. Phytopathology 93:1044–1047
Kinloch BB, Davis DA, Burton D (2008) Resistance and virulence interactions between two white pine species and blister rust in a 30-year field trial. Tree Genet Genomes 4(1):65–74
Krutovsky KV, St.Clair JB, Saich R, Hipkins VD, Neale DB (2009) Estimation of population structure in coastal Douglas-fir [Pseudotsuga menziesii (Mirb.) Franco var. menziesii] using allozyme and microsatellite markers. Tree Genet Genomes 5(4):641–658
Liu JJ, Sturrock RN, Sniezko RA, Williams H, Benton R, Zamany A (2015) Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors. BMC Genomics 16:678
Liu JJ, Schoettle AW, Sniezko RA, Sturrock RN, Zamany A, Williams H, Ha A, Chan D, Danchok B, Savin DP et al (2016) Genetic mapping of Pinus flexilis major gene (Cr4) for resistance to white pine blister rust using transcriptome-based SNP genotyping. BMC Genomics 17:753
Liu JJ, Sniezko RA, Zamany A, Williams H, Wang N, Kegley A, Savin DP, Chen H, Sturrock RN (2017) Saturated genic SNP mapping identified functional candidates and selection tools for the Pinus monticola Cr2 locus controlling resistance to white pine blister rust. Plant Biotechnol J. https://doi.org/10.1111/pbi.12705
Maloney PE, Vogler DR, Eckert AJ, Jensen CE, Neale DB (2011) Population biology of sugar pine (Pinus lambertiana Dougl.) with reference to historical disturbances in the Lake Tahoe Basin: implications for restoration. For Ecol Manag 262(5):770–779
Maloy OC (2003) White pine blister rust. Plant Health Instructor. https://doi.org/PHI-I-2003-0908-01 Updated 2008
McDonald GI, Hoff RJ (2001) Blister rust: an introduced plague. In: Tomback, Diana F; Arno Stephen F; Keane Robert E, eds. Whitebark pine communities: ecology and restoration. Washington, DC. Island Press: 195-220
Poland J, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotyped data. Genetics 155:945–959
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC (2007) PLINK: a toolset for whole-genome association and population-based linkage analysis Am J Human Genet 81
Sniezko RA, Smithy J, Liu JJ, Hamelin HC (2014) Genetic resistance to fusiform rust in southern pines and white pine blister rust in white pines—a contrasting tale of two rust pathosystems—current status and future prospects. Forests 5:2020–2083
Sniezko RA, Bower A, Danielson J (2000) A comparison of early field results of white pine blister rust resistance in sugar pine and western white pine. Hortechnology 10(3):519–522
Stenlid J, Oliva J, Boberg JB, Hopkins AJM (2011) Emerging diseases in European forest ecosystems and responses in society. Forests 2(2):486–504
Stevens KA, Wegrzyn JL, Zimin A, Puiu D, Crepeau M, Cardeno C, Paul R, Gonzalez D, Koribiane M, Holtz-Morris AE, Martinez-Garcia PJ, Sezen UU, Marcais G, Jermstad K, McGuire PE, Loopstra CA, Davis JM, Eckert A, deJong P, Yorke JA, Salzberg SL, Neale DB, Langley CH (2016) Sequence of the sugar pine megagenome: transposable elements and white pine blister rust resistance. Genetics 204(4):1613–1626
Sugimoto M, Yamaguchi Y, Nakamura K, Tatsumi Y, Sano H (2004) A hypersensitive response-induced ATPase associated with various cellular activities (AAA) protein from tobacco plants. Plant Mol Biol 56:973–985
Titiz O, Tambasco-Studart M, Warzych E, Apel K, Amrhein N, Laloi C, Fitzpatrick TB (2006) PDX1 is essential for vitamin B6 biosynthesis, development and stress tolerance in Arabidopsis. Plant J 48:933–946
Tomback DF, Achuff P (2010) Blister rust and western forest diversity: ecology, values and outlook for white pines. For Pathol 40:186–225
Vangestel C, Vasquez-Lobo A, Martínez-García PJ, Calic I, Wegrzyn JL, Neale DB (2016) Patterns of neutral and adaptive genetic diversity across the natural range of sugar pine (Pinus lambertiana Dougl.) Tree Genet Genomes 12:51
Van Mantgem PJ, Stephenson NL, Keifer M, Keeley JE (2004) Effects of an introduced pathogen and fire exclusion on the demography of sugar pine. Ecol Appl 14:1590–1602
Wu TD, Watanabe CK (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21:1859–1875
Yi SY, Lee HY, Ha K, Lim CJ, Kim WB, Ha J, Jeon J-S, Kwon S-Y (2013) Microarray analysis of bacterial blight resistance 1 mutant rice infected with Xanthomonas oryzae pv. oryzae. Plant Breed Biotechnol 1:354–365
Zambino PJ, McDonald GI (2004) Resistance to white pine blister rust in North American five-needle pines and Ribes and its implications. 51st western international Forest disease WorkConference, 18–22 august 2003, grants pass, OR, USA. Ed. by Geils, B. W. Flagstaff, AZ: USDA Forest service, Rocky Mountain Research Station, pp. 111–125
Zhang XY, Lu Q, Sniezko RA, Song RQ, Man G (2010) Blister rust in China: hosts, pathogens and management. For Pathol 50:369–381
Zhang B, Aken OV, Thatcher L, Clercq ID, Duncan O, Law SR, Murcha MW, van der Merwe M, Seifi HS, Carrie C et al (2014) The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana. Plant J Cell Mol Biol 80:709–727
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20
We would like to thank the U.S. Forest Service sugar pine breeding program in California for establishing the Mapping population used in this study. AVL was supported by a UC MEXUS-CONACyT Postdoctoral fellowship.
Conflict of interest
The authors declare that they have no conflict of interest.
Data Archiving Statement
SNP sequences will be submitted to Tree Genes database (http://treegenesdb.org) and accession numbers will be supplied once available, prior to final acceptance of the manuscript.
Communicated by S. C. González-Martínez
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Vázquez-Lobo, A., De La Torre, A.R., Martínez-García, P.J. et al. Finding loci associated to partial resistance to white pine blister rust in sugar pine (Pinus lambertiana Dougl.).. Tree Genetics & Genomes 13, 108 (2017). https://doi.org/10.1007/s11295-017-1190-4
- White pine blister rust
- Sugar pine
- Disease resistance
- Genotype × phenotype associations