Selection against hybrids in mixed populations of Brassica rapa and Brassica napus: model and synthesis.

Pollen of the crop oilseed rape (Brassica napus, AACC) can cross-fertilize ovules of Brassica rapa (AA), which leads to an influx of unpaired C-chromosomes into wild B. rapa populations. The presence of such extra chromosomes is thought to be an indicator of introgression. Backcrosses and F(1) hybrids were found in Danish populations but, surprisingly, only F(1) hybrids were found in the UK and the Netherlands. Here, a model tests how the level of selection and biased vs unbiased transmission affect the population frequency of C-chromosomes. In the biased-transmission scenario the experimental results of the first backcross are extrapolated to estimate survival of gametes with different numbers of C-chromosomes from all crosses in the population. With biased transmission, the frequency of C-chromosomes always rapidly declines to zero. With unbiased transmission, the continued presence of plants with extra C-chromosomes depends on selection in the adult stage and we argue that this is the most realistic option for modeling populations. We suggest that selection in the field against plants with unpaired C-chromosomes is strong in Dutch and UK populations. The model highlights what we do not know and makes suggestions for further research on introgression.

[1]  M. Hochberg,et al.  Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa) , 2004, Theoretical and Applied Genetics.

[2]  C. Damgaard,et al.  Maternal Inheritance of Chloroplasts between Brassica rapa and F1-hybrids Demonstrated by cpDNA Markers Specific to Oilseed Rape and B. rapa , 2005, Molecular Breeding.

[3]  I. Davenport,et al.  A direct regional scale estimate of transgene movement from genetically modified oilseed rape to its wild progenitors , 2000, Molecular ecology.

[4]  D. Levin The Role of Chromosomal Change in Plant Evolution , 2002 .

[5]  A. Légére,et al.  Risks and consequences of gene flow from herbicide-resistant crops: canola (Brassica napus L) as a case study. , 2005, Pest management science.

[6]  T. Mikkelsen,et al.  Transgene expression and fitness of hybrids between GM oilseed rape and Brassica rapa. , 2005, Environmental biosafety research.

[7]  S. Warwick,et al.  Hybridization between transgenic Brassica napus L. and its wild relatives: Brassica rapa L., Raphanus raphanistrum L., Sinapis arvensis L., and Erucastrum gallicum (Willd.) O.E. Schulz , 2003, Theoretical and Applied Genetics.

[8]  J. Allainguillaume,et al.  Spontaneous capture of oilseed rape (Brassica napus) chloroplasts by wild B. rapa: implications for the use of chloroplast transformation for biocontainment , 2009, Current Genetics.

[9]  Nu Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. , 1935 .

[10]  S. Knapp,et al.  Transmission ratio distortion results in asymmetric introgression in Louisiana Iris , 2010, BMC Plant Biology.

[11]  C. N. Stewart,et al.  Growth, productivity, and competitiveness of introgressed weedy Brassica rapa hybrids selected for the presence of Bt cry1Ac and gfp transgenes , 2005, Molecular ecology.

[12]  G. Barker,et al.  Pairing and recombination at meiosis of Brassica rapa (AA) × Brassica napus (AACC) hybrids , 2006, Theoretical and Applied Genetics.

[13]  Abdel H. El-Shaarawi,et al.  Environmental monitoring, assessment and prediction of change , 1993 .

[14]  M. Arnold,et al.  Hybrid fitness across time and habitats. , 2010, Trends in ecology & evolution.

[15]  G. King,et al.  A and C Genome Distinction and Chromosome Identification in Brassica napus by Sequential Fluorescence in Situ Hybridization and Genomic in Situ Hybridization , 2008, Genetics.

[16]  Masahiro Kato,et al.  Fertilization Fitness and Relation to Chromosome Number in Interspecific Progeny between Brassica napus and B. rapa: A Comparative Study using Natural and Resynthesized B. napus , 2001 .

[17]  James A. Birchler,et al.  The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. , 2010, The New phytologist.

[18]  M. Katô,et al.  Destiny of a transgene escape from Brassica napus into Brassica rapa , 2002, Theoretical and Applied Genetics.

[19]  G. Mackay The introgression of S alleles into forage rape, Brassica napus L. from turnip. Brassica campestris L. ssp. Rapifera , 1977, Euphytica.

[20]  C. N. Stewart,et al.  Inheritance of GFP-Bt transgenes from Brassica napus in backcrosses with three wild B. rapa accessions. , 2004, Environmental biosafety research.

[21]  J. Bullock,et al.  Fitness of hybrids between rapeseed (Brassica napus) and wild Brassica rapa in natural habitats , 2006, Molecular ecology.

[22]  Marie-Josée Simard,et al.  Transgenic Brassica napus fields and Brassica rapa weeds in Quebec: sympatry and weed-crop in situ hybridization , 2006 .

[23]  Dirk Reheul,et al.  Quantifying the introgressive hybridisation propensity between transgenic oilseed rape and its wild/weedy relatives , 2009, Environmental monitoring and assessment.

[24]  E. Coen,et al.  Regulatory Genes Control a Key Morphological and Ecological Trait Transferred Between Species , 2008, Science.

[25]  Gang Wu,et al.  Gene transferability from transgenic Brassica napus L. to various subspecies and varieties of Brassica rapa , 2009, Transgenic Research.

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

[27]  A. Richards,et al.  A hybrid swarm between the diploid Dactylorhiza fuchsii (Druce) Soo and the tetraploid D. purpurella (T. & T. A. Steph.) Soo in Durham , 1977 .

[28]  J. Tomiuk,et al.  A- or C-chromosomes, does it matter for the transfer of transgenes from Brassica napus , 2000, Theoretical and Applied Genetics.

[29]  H. Namai,et al.  Pollen fertility and seed set percentage after backcrossing of sesquidiploids (AAC genomes) derived from interspecific hybrid between Brassica campestris L. (AA) and B. oleracea L. (CC) and frequency distribution of aneuploids in the progenies. , 1992 .

[30]  S. Warwick,et al.  Gene Flow, Invasiveness, and Ecological Impact of Genetically Modified Crops , 2009, Annals of the New York Academy of Sciences.

[31]  Danny A. P. Hooftman,et al.  Modelling the long-term consequences of crop-wild relative hybridization: a case study using four generations of hybrids. , 2007 .

[32]  Honor C. Prentice,et al.  Gene Flow and Introgression from Domesticated Plants into Their Wild Relatives , 1999 .

[33]  R. A. Wesselingh,et al.  Hybridization in Annual Plants: Patterns and DynamicsDuring a Four-Year Study in Mixed Rhinanthus Populations , 2010, Folia Geobotanica.

[34]  S. Warwick,et al.  Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population , 2008, Molecular ecology.

[35]  T. Sharbel,et al.  Is the aneuploid chromosome in an apomictic Boechera holboellii a genuine B chromosome? , 2004, Cytogenetic and Genome Research.

[36]  Wei Wei,et al.  Gene flow hampered by low seed size of hybrids between oilseed rape and five wild relatives , 2008, Seed Science Research.

[37]  H. Monod,et al.  Genetic Regulation of Meiotic Cross-Overs between Related Genomes in Brassica napus Haploids and Hybrids[C][W] , 2009, The Plant Cell Online.

[38]  S. Warwick Hybridization between transgenic Brassica napus L. and its wild relatives : Brassica raps L., Raphanus raphanistrum L., Sinapis arvensis L., and Erucastrum gallicum (Willd.) , 2003 .

[39]  M. Chapman,et al.  Introgression of fitness genes across a ploidy barrier. , 2010, The New phytologist.

[40]  T. Sharbel,et al.  EMBRYOLOGY, KARYOLOGY, AND MODES OF REPRODUCTION IN THE NORTH AMERICAN GENUS BOECHERA (BRASSICACEAE): A COMPILATION OF SEVEN DECADES OF RESEARCH1 , 2006 .

[41]  C. N. Stewart,et al.  Bt-transgenic oilseed rape hybridization with its weedy relative, Brassica rapa. , 2002, Environmental biosafety research.

[42]  R. Jørgensen,et al.  Inheritance of oilseed rape (Brassica napus) RAPD markers in a backcross progeny with Brassica campestris , 1996, Theoretical and Applied Genetics.

[43]  M. Vicente,et al.  Gene Flow between Crops and Their Wild Relatives , 2010 .

[44]  Jeremy Sweet,et al.  Hybridization Between Brassica napus and B. rapa on a National Scale in the United Kingdom , 2003, Science.

[45]  C. N. Stewart,et al.  Genetic load and transgenic mitigating genes in transgenic Brassica rapa (field mustard) × Brassica napus (oilseed rape) hybrid populations , 2009, BMC biotechnology.

[46]  S. Luijten,et al.  Baseline study of the distribution and morphology of Brassica napus L. and Brassica rapa L. in the Netherlands , 2010 .

[47]  H. Siegismund,et al.  Progressive introgression between Brassica napus (oilseed rape) and B. rapa , 2003, Heredity.

[48]  R. Shaw,et al.  Fitness of F1 hybrids between weedy Brassica rapa and oilseed rape (B. napus) , 1998, Heredity.

[49]  T. T. Elkington CYTOGENETIC VARIATION IN THE BRITISH FLORA: ORIGINS AND SIGNIFICANCE. , 1984, The New phytologist.

[50]  Lenka Justinova,et al.  The responses of crop - wild Brassica hybrids to simulated herbivory and interspecific competition: implications for transgene introgression. , 2006, Environmental biosafety research.

[51]  G. Ledyard Stebbins,et al.  Chromosomal evolution in higher plants , 1971 .

[52]  D. Persson,et al.  Hybridization between Brassica insularis Moris and B. balearica Pers. , 2008, Hereditas.

[53]  R. Brummitt,et al.  Hybridization and the flora of the British Isles , 1977 .

[54]  Rikke Bagger Jørgensen,et al.  Introgression between oilseed rape (Brassica napus L.) and its weedy relative B. rapa L. in a natural population , 2001, Genetic Resources and Crop Evolution.

[55]  R. Jørgensen,et al.  Fitness of backcross and F2 hybrids between weedy Brassica rapa and oilseed rape (B. napus) , 1998, Heredity.

[56]  R. Jørgensen,et al.  Natural Hybridisation between Oilseed Rape and a Wild Relative: Hybrids among Seeds from Weedy B. Campestris , 2004 .

[57]  K. Marhold,et al.  Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae , 2006, Plant Systematics and Evolution.

[58]  S. Warwick,et al.  Additive transgene expression and genetic introgression in multiple green-fluorescent protein transgenic crop × weed hybrid generations , 2003, Theoretical and Applied Genetics.