Abstract
Resistance genes (R-genes) are essential for long-lived organisms such as forest trees, which are exposed to diverse herbivores and pathogens. In short-lived model species, R-genes have been shown to be involved in species isolation. Here, we studied more than 400 trees from two natural hybrid zones of the European Populus species Populus alba and Populus tremula for microsatellite markers located in three R-gene clusters, including one cluster situated in the incipient sex chromosome region. The results indicate that all three R-gene clusters present extensive linkage disequilibrium (LD). Outlier tests suggest balancing selection as a potential driver of R-gene diversity, but divergent selection was also detected. Nucleotide-binding site leucine-rich repeat (NBS-LRR) type R-gene clusters exhibit low species differentiation and appear to be affected by shared selection pressures between species, recurrent interspecific gene flow, or both. Our results are consistent with a role for R-gene clusters in the evolution of chromosome XIX, recently put forward as an incipient sex chromosome in Populus.
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Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJ, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R et al (2013) Hybridization and speciation. J Evol Biol 26:229–246
Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinf 9:323
Arnold ML (2006) Evolution through genetic exchange. Oxford University Press, Oxford
Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Philos Trans R Soc Lond B Biol Sci 263:1619–1626
Bergelson J (2001) Evolutionary dynamics of plant R-genes. Science 292:2281–2285
Bomblies K (2009) Too much of a good thing? Hybrid necrosis as a by-product of plant immune system diversification. Botany 87:1013–1022
Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8:382–393
Bresson A, Jorge V, Dowkiw A, Guerin V, Bourgait I, Tuskan GA, Schmutz J, Chalhoub B, Bastien C, Faivre Rampant P (2011) Qualitative and quantitative resistances to leaf rust finely mapped within two nucleotide-binding site leucine-rich repeat (NBS-LRR)-rich genomic regions of chromosome 19 in poplar. New Phytol 192:151–163
Brown JKM, Tellier A (2011) Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu Rev Phytopathol 49:345–367
Charlesworth D (2013) Plant sex chromosome evolution. J Exp Bot 64:405–420
De Meaux J, Mitchell-Olds T (2003) Evolution of plant resistance at the molecular level: ecological context of species interactions. Heredity 91:345–352
Ellegren H (2009) The different levels of genetic diversity in sex chromosomes and autosomes. Trends Genet 25:278–284
Feder JL, Egan SP, Nosil P (2012) The genomics of speciation-with-gene-flow. Trends Genet 28:342–350
Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993
Fussi B, Lexer C, Heinze B (2010) Phylogeography of Populus alba (L.) and Populus tremula (L.) in Central Europe: secondary contact and hybridisation during recolonisation from disconnected refugia. Tree Genet Genomes 6:439–450
Garnier-Gere P, Dillmann C (1992) A computer program for testing pairwise linkage disequilibria in subdivided populations. J Hered 83:239
Gaudet M, Jorge V, Paolucci I, Beritognolo I, Mugnozza GS, Sabatti M (2008) Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait. Tree Genet Genomes 4:25–36
Geraldes A, Hefer CA, Capron A, Kolosova N, Martinez-Nuñez F, Soolanayakanahally RY, Stanton B, Guy RD, Mansfield SD, Douglas CJ, Cronk QCB (2015) Recent Y chromosome divergence despite ancient origin of dioecy in poplars (Populus). Mol Ecol. doi:10.1111/mec.13126
Germain H, Séguin A (2010) Innate immunity: has poplar made its BED? New Phytol 189:678–687
Gompert Z, Buerkle CA (2010) INTROGRESS: a software package for mapping components of isolation in hybrids. Mol Ecol Resour 10:378–384
Gompert Z, Buerkle CA (2012) bgc: software for Bayesian estimation of genomic clines. Mol Ecol Resour 12:1168–1176
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Hou J, Ye N, Zhang D, Chen Y, Fang L, Dai X, Yin T (2015) Different autosomes evolved into sex chromosomes in the sister genera of Salix and Populus. Sci Rep 5:9076
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
Keith R, Olds TM (2013) Genetic variation for resistance to herbivores and plant pathogens: hypotheses, mechanisms and evolutionary implications. Plant Pathol 62:122–132
Kersten B, Pakull B, Groppe K, Lueneburg J, Fladung M (2014) The sex-linked region in Populus tremuloides Turesson 141 corresponds to a pericentromeric region of about two million base pairs on P. trichocarpa chromosome 19. Plant Biol 16:411–418
Klevebring D, Street NR, Fahlgren N, Kasschau KD, Carrington JC, Lundeberg J, Jansson S (2009) Genome-wide profiling of Populus small RNAs. BMC Genomics 10:620
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
Koopman WJM, Li Y, Coart E, van de Weg WE, Vosman B, Roldan-Ruiz I, Smulders MJM (2006) Linked vs. unlinked markers: multilocus microsatellite haplotype-sharing as a tool to estimate gene flow and introgression. Mol Ecol 66:243–256
Lexer C, Widmer A (2008) The genic view of plant speciation: recent progress and emerging questions. Philos Trans R Soc B 363:3023–3036
Lexer C, Fay MF, Joseph J, Nica M, Heinze B (2005) Barrier to gene flow between two ecologically divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): the role of ecology and life history in gene introgression. Mol Ecol 14:1045–1057
Lexer C, Joseph J, van Loo M, Barbará T (2010) Genomic admixture analysis in European Populus spp. reveals unexpected patterns of reproductive isolation and mating. Genetics 186:699–712
Lindtke D, Buerkle CA, Barbará T, Heinze B, Castiglione S, Bartha D, Lexer C (2012) Recombinant hybrids retain heterozygosity at many loci: new insights into the genomics of reproductive isolation in Populus. Mol Ecol 21:5042–5058
Lindtke D, Gompert Z, Lexer C, Buerkle CA (2014) Unexpected ancestry of Populus seedlings from a hybrid zone implies a large role for postzygotic selection in the maintenance of species. Mol Ecol 23:4316–4330
Macaya-Sanz D, Suter L, Joseph J, Barbará T, Alba N, Gonzalez-Martinez SC, Widmer A, Lexer C (2011) Genetic analysis of post-mating reproductive barriers in hybridizing European Populus species. Heredity 107:478–486
Muir G, Schlötterer C (2005) Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Mol Ecol 14:549–561
Pakull B, Groppe K, Mecucci F, Gaudet M, Sabatti M, Fladung M (2011) Genetic mapping of linkage group XIX and identification of sex-linked SSR markers in a Populus tremula x Populus tremuloides cross. Can J Forest Res 41:245–253
Paolucci I, Gaudet M, Jorge V, Beritognolo I, Terzoli S, Kuzminsky E, Muleo R, Mugnozza GS, Sabatti M (2010) Genetic linkage maps of Populus alba L. and comparative mapping analysis of sex determination across Populus species. Tree Genet Genomes 4:25–36
Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24:386–393
Petre B, Major I, Rouhier N, Duplessis S (2011) Genome-wide analysis of eukaryote thaumatin-like proteins (TLPs) with an emphasis on poplar. BMC Plant Biol 11:33
Qvarnström A, Bailey RI (2009) Speciation through evolution of sex-linked genes. Heredity 102:4–15
Rausher MD (2001) Co-evolution and plant resistance to natural enemies. Nature 411:857–864
Roesti M, Gavrilets S, Hendry AP, Salzburger W, Berner D (2014) The genomic signature of parallel adaptation from shared genetic variation. Mol Ecol 23:3944–3956
Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234
Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, Pennacchio CP, Hellsten U, Pennacchio LA, Gunter LE et al (2012) Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol 196:713–725
Smadja CM, Butlin RK (2011) A framework for comparing processes of speciation in the presence of gene flow. Mol Ecol 20:5123–5140
Stahl EA, Bishop JG (2000) Plant-pathogen arms races at the molecular level. Curr Opin Plant Biol 3:299–304
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989
Stirling B, Newcombe G, Vrebalov J, Bosdet I, Bradshaw HD Jr (2001) Suppressed recombination around the MXC3 locus, a major gene for resistance to poplar leaf rust. TAG 103:1129–1137
Stölting KN, Nipper R, Lindtke D, Caseys C, Waeber S, Castiglione S, Lexer C (2013) Genomic scan for single nucleotide polymorphisms reveals patterns of divergence and gene flow between ecologically divergent species. Mol Ecol 22:842–855
Stölting KN, Paris M, Meier C, Heinze B, Castiglione S, Bartha D, Lexer C (2015) Genome-wide patterns of differentiation and spatially varying selection between postglacial recolonization lineages of Populus alba (Salicaceae), a widespread forest tree. New Phytol. doi:10.1111/nph.13392
The Marie Curie SPECIATION Network (2011) What do we need to know about speciation? Trends Ecol Evol 27:27–39
Traw M, Bergelson J (2010) Plant immune system incompatibility and the distribution of enemies in natural hybrid zones. Curr Opin Plant Biol 13:466–471
Tuskan GA, DiFazio SP, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam NH, Ralph SG, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. and Gray). Science 313:1596–1604
Tuskan GA, DiFazio S, Faivre Rampant P, Gaudet M, Harfouche A, Jorge V, Labbé JL, Ranjan P, Sabatti M, Slavov GT, Street N, Tschaplinski TJ, Yin TM (2012) The obscure events contributing to the evolution of an incipient sex chromosome in Populus: a retrospective working hypothesis. Tree Genet Genomes 8:559–571
Whitney KD, Randell RA, Rieseberg LH (2006) Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am Nat 167:794–807
Wu C (2001) The genic view of the process of speciation. J Evol Biol 14:851–865
Yin T, DiFazio SP, Gunter L, Jawdy S, 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
Yin T, DiFazio SP, Gunter LE (2008) Genome structure and emerging evidence of an incipient sex. Genome Res 18:422–430
Zaykin DV, Pudovkin A, Weir BS (2008) Correlation-based inference for linkage disequilibrium with multiple alleles. Genetics 180:533–545
Acknowledgments
This study was supported by grants 31003A_127059 and 31003A_149306 of the Swiss National Science Foundation (SNF) to CL.
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Microsatellite genotype data can be found on dryad doi:10.5061/dryad.2593t.
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Communicated by P. Ingvarsson
This article is part of the Topical Collection on Disease Resistance
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Caseys, C., Stölting, K.N., Barbará, T. et al. Patterns of genetic diversity and differentiation in resistance gene clusters of two hybridizing European Populus species. Tree Genetics & Genomes 11, 81 (2015). https://doi.org/10.1007/s11295-015-0904-8
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DOI: https://doi.org/10.1007/s11295-015-0904-8