Population structure and genetic bottleneck in sweet cherry estimated with SSRs and the gametophytic self-incompatibility locus

BackgroundDomestication and breeding involve the selection of particular phenotypes, limiting the genomic diversity of the population and creating a bottleneck. These effects can be precisely estimated when the location of domestication is established. Few analyses have focused on understanding the genetic consequences of domestication and breeding in fruit trees. In this study, we aimed to analyse genetic structure and changes in the diversity in sweet cherry Prunus avium L.ResultsThree subgroups were detected in sweet cherry, with one group of landraces genetically very close to the analysed wild cherry population. A limited number of SSR markers displayed deviations from the frequencies expected under neutrality. After the removal of these markers from the analysis, a very limited bottleneck was detected between wild cherries and sweet cherry landraces, with a much more pronounced bottleneck between sweet cherry landraces and modern sweet cherry varieties. The loss of diversity between wild cherries and sweet cherry landraces at the S-locus was more significant than that for microsatellites. Particularly high levels of differentiation were observed for some S-alleles.ConclusionsSeveral domestication events may have happened in sweet cherry or/and intense gene flow from local wild cherry was probably maintained along the evolutionary history of the species. A marked bottleneck due to breeding was detected, with all markers, in the modern sweet cherry gene pool. The microsatellites did not detect the bottleneck due to domestication in the analysed sample. The vegetative propagation specific to some fruit trees may account for the differences in diversity observed at the S-locus. Our study provides insights into domestication events of cherry, however, requires confirmation on a larger sampling scheme for both sweet cherry landraces and wild cherry.

[1]  A. G. Abbott,et al.  Characterization of microsatellite markers in peach [Prunus persica (L.) Batsch] , 2000, Theoretical and Applied Genetics.

[2]  S. Glémin,et al.  Grinding up wheat: a massive loss of nucleotide diversity since domestication. , 2007, Molecular biology and evolution.

[3]  R. Bošković,et al.  Characterisation of novel S-alleles from cherry (Prunus avium L.) , 2008, Tree Genetics & Genomes.

[4]  Randall L. Nelson,et al.  Impacts of genetic bottlenecks on soybean genome diversity , 2006, Proceedings of the National Academy of Sciences.

[5]  J. Goudet FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics , 1995 .

[6]  V. Franklin-Tong Self-Incompatibility in Flowering Plants , 2008 .

[7]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[8]  Steven G. Schroeder,et al.  The Effects of Artificial Selection on the Maize Genome , 2005, Science.

[9]  R. Papa,et al.  Asymmetry of gene flow and differential geographical structure of molecular diversity in wild and domesticated common bean (Phaseolus vulgaris L.) from Mesoamerica , 2002, Theoretical and Applied Genetics.

[10]  J. Doebley,et al.  An Analysis of Genetic Diversity Across the Maize Genome Using Microsatellites , 2005, Genetics.

[11]  F. Kappel,et al.  Inbreeding, Coancestry, and Founding Clones of Sweet Cherries from North America , 2004 .

[12]  A. Iezzoni,et al.  Assessment of genetic diversity of Latvian and Swedish sweet cherry (Prunus avium L.) genetic resources collections by using SSR (microsatellite) markers , 2009 .

[13]  R. Testolin,et al.  Microsatellite DNA in peach (Prunus persica L. Batsch) and its use in fingerprinting and testing the genetic origin of cultivars. , 2000, Genome.

[14]  H. Gregorius,et al.  Detecting local establishment strategies of wild cherry (Prunus avium L.) , 2006, BMC Ecology.

[15]  P. Gouyon,et al.  Genetic differentiation within and among populations of chestnut (Castanea sativa Mill.) and wild cherry (Prunus avium L.) , 1993, Heredity.

[16]  M. Uyenoyama,et al.  On the Evolutionary Modification of Self-Incompatibility: Implications of Partial Clonality for Allelic Diversity and Genealogical Structure , 2008 .

[17]  Thomas Bataillon,et al.  A comparative view of the evolution of grasses under domestication. , 2009, The New phytologist.

[18]  F. Bonhomme,et al.  GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. , 1996 .

[19]  S. Southwick,et al.  Analysis of Sweet Cherry (Prunus avium L.) Cultivars Using SSR and AFLP Markers , 2003 .

[20]  S. Southwick,et al.  Detection of genetic diversity among populations of sweet cherry (Prunus avium L.) by AFLPs , 2001 .

[21]  Maria Hopf,et al.  Domestication of plants in the old world , 1988 .

[22]  D. Lewis,et al.  Structure of the incompatibility gene , 1949, Heredity.

[23]  N. Frascaria-Lacoste,et al.  Heterozygote excess in a self‐incompatible and partially clonal forest tree species —Prunus avium L. , 2006, Molecular ecology.

[24]  S. Stoeckel,et al.  Unequal allelic frequencies at the self‐incompatibility locus within local populations of Prunus avium L.: an effect of population structure? , 2008, Journal of evolutionary biology.

[25]  K. Tobutt,et al.  Determining self‐incompatibility genotypes in Belgian wild cherries , 2005, Molecular ecology.

[26]  B. Courtois,et al.  Phylogeographic Evidence of Crop Neodiversity in Sorghum , 2008, Genetics.

[27]  A. Richman,et al.  Self-incompatibility alleles from Physalis: implications for historical inference from balanced genetic polymorphisms. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Maria Hopf,et al.  Domestication of plants in the Old World. The origin and spread of cultivated plants in West Asia, Europe and the Nile Valley. , 2000 .

[29]  D. Zohary,et al.  Beginnings of Fruit Growing in the Old World , 1975, Science.

[30]  K. Russell,et al.  Characterization of novel microsatellites and development of multiplex PCR for large-scale population studies in wild cherry, Prunus avium , 2004 .

[31]  H. Flachowsky,et al.  Determination of self-incompatible genotypes in sweet cherry (Prunus avium L.) accessions and cultivars of the German Fruit Gene Bank and from private collections , 2007 .

[32]  D. Sargent,et al.  Isolation of S-locus F-box alleles in Prunus avium and their application in a novel method to determine self-incompatibility genotype , 2006, Theoretical and Applied Genetics.

[33]  M. Beaumont,et al.  Evaluating loci for use in the genetic analysis of population structure , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  Marianne Elias,et al.  The evolutionary ecology of clonally propagated domesticated plants. , 2010, The New phytologist.

[35]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[36]  A. Iezzoni,et al.  Construction of an intra-specific sweet cherry (Prunus avium L.) genetic linkage map and synteny analysis with the Prunus reference map , 2008, Tree Genetics & Genomes.

[37]  G. King,et al.  Development of a second generation linkage map for almond using RAPD and SSR markers. , 2000, Genome.

[38]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[39]  J. Cottrell,et al.  Clonal structure and recruitment in British wild cherry (Prunus avium L.) , 2007 .

[40]  J. Cottrell,et al.  Distribution and fine-scale spatial-genetic structure in British wild cherry (Prunus avium L.) , 2007, Heredity.

[41]  K. Tobutt,et al.  Development and characterization of polymorphic microsatellites from Prunus avium‘Napoleon’ , 2003 .

[42]  L. Excoffier,et al.  Detecting loci under selection in a hierarchically structured population , 2009, Heredity.

[43]  F. Ducci,et al.  The distribution of clones in managed and unmanaged populations of wild cherry (Prunus avium) , 1997 .

[44]  L. Bohs,et al.  Historical inferences from the self‐incompatibility locus , 2003 .

[45]  Britta Pollmann,et al.  Morphological and genetic studies of waterlogged Prunus species from the Roman vicus Tasgetium (Eschenz, Switzerland) , 2005 .

[46]  H. Gerlach,et al.  Patterns of random amplified polymorphic DNAs for sweet cherry (Prunus avium L.) cultivar identification , 1997 .

[47]  M. Shriver,et al.  Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle (Bos taurus and Bos indicus). , 1997, Genetics.

[48]  K. Tobutt,et al.  Improved discrimination of self-incompatibility S-RNase alleles in cherry and high throughput genotyping by automated sizing of first intron polymerase chain reaction products , 2006 .

[49]  A. Mohanty,et al.  Chloroplast DNA variation in cultivated and wild Prunus avium L: a comparative study , 2003 .

[50]  R. Testolin,et al.  AC/GT and AG/CT microsatellite repeats in peach [Prunus persica (L) Batsch]: isolation, characterisation and cross-species amplification in Prunus , 1999, Theoretical and Applied Genetics.

[51]  E. Dirlewanger,et al.  Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.) , 2002, Theoretical and Applied Genetics.

[52]  R. Petit,et al.  Identifying Populations for Conservation on the Basis of Genetic Markers , 1998 .

[53]  L. Lehmann,et al.  The population genetics of clonal and partially clonal diploids. , 2003, Genetics.

[54]  M. Navascués,et al.  Genetic diversity and fitness in small populations of partially asexual, self-incompatible plants , 2010, Heredity.

[55]  S. Glémin,et al.  Inbreeding depression in small populations of self-incompatible plants. , 2001, Genetics.

[56]  N. Machon,et al.  Genetic variability in wild cherry populations in France. Effects of colonizing processes , 1997, Theoretical and Applied Genetics.

[57]  G. A. Leng ON POPULATION. , 1963, Singapore medical journal.

[58]  M. Rösch New aspects of agriculture and diet of the early medieval period in central Europe: waterlogged plant material from sites in south-western Germany , 2008 .

[59]  M. Nei,et al.  Estimation of average heterozygosity and genetic distance from a small number of individuals. , 1978, Genetics.

[60]  A. Iezzoni,et al.  Polymorphic DNA Markers in Black Cherry (Prunus serotina) Are Identified Using Sequences from Sweet Cherry, Peach, and Sour Cherry , 2000 .

[61]  D. Sargent,et al.  A cherry map from the inter-specific cross Prunus avium ‘Napoleon’ × P. nipponica based on microsatellite, gene-specific and isoenzyme markers , 2008, Tree Genetics & Genomes.

[62]  O. Tenaillon,et al.  Selection versus demography: a multilocus investigation of the domestication process in maize. , 2004, Molecular biology and evolution.

[63]  R. Šoštarić,et al.  Roman plant remains from Veli Brijun (island of Brioni), Croatia , 2001 .

[64]  Jingchu Luo,et al.  Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. , 2007, Molecular biology and evolution.