Patterns of genetic diversity and differentiation in resistance gene clusters of two hybridizing European Populus species
- 417 Downloads
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.
KeywordsResistance gene cluster NBS-LRR Plant defense Hybridization Sex chromosome Selection
This study was supported by grants 31003A_127059 and 31003A_149306 of the Swiss National Science Foundation (SNF) to CL.
Data archiving statement
Microsatellite genotype data can be found on dryad doi: 10.5061/dryad.2593t.
- Arnold ML (2006) Evolution through genetic exchange. Oxford University Press, OxfordGoogle Scholar
- 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 192:151–163PubMedCrossRefGoogle Scholar
- Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
- 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 4:25–36Google Scholar
- 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 196:713–725PubMedCrossRefGoogle Scholar
- 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 PubMedGoogle Scholar
- The Marie Curie SPECIATION Network (2011) What do we need to know about speciation? Trends Ecol Evol 27:27–39Google Scholar
- 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 8:559–571CrossRefGoogle Scholar