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Molecular genetics of growth and development in Populus. II. Segregation distortion due to genetic load

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Abstract

Distortion of expected Mendelian segregation ratios, commonly observed in many plant taxa, has been detected in an experimental three-generation inbred pedigree of Populus founded by interspecific hybridization between P. trichocarpa and P. deltoides. An RFLP linkage map was constructed around a single locus showing severe skewing of segregation ratio against F2 trees carrying the P. trichocarpa allele in homozygous form. Several hypotheses for the mechanism of segregation distortion at this locus were tested, including directional chromosome loss, segregation of a pollen lethal allele, conflicts between genetic factors that isolate the parental species, and inbreeding depression as a result of genetic load. Breeding experiments to produce inbred and outcrossed progenies were combined with PCR-based detection of RFLPs to follow the fate of the deficient allele throughout embryo and seedling development. A recessive lethal allele, lth, inherited from the P. trichocarpa parent, was found to be tightly linked to the RFLP marker locus POP1054 and to cause embryo and seedling mortality. Heterozygotes (lth/+) appear to be phenotypically normal as embryos, seedlings, and young trees.

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Abbreviations

RFLP :

restriction fragment length polymorphism

PCR :

polymerase chain reaction

STS :

sequence-tagged site

SDS :

sodium dodecyl sulfate

References

  • Adams WT, Neale DB, Doerksen AH, Smith DB (1990) Inheritance and linkage of isozyme variants from seed and vegetative bud tissues in coastal Douglas-fir [Pseudotsuga menziesii var ‘menziesii’ var ‘menziesii’ (Mirb.) Franco]. Silvae Genet 39:153–167

    Google Scholar 

  • Beavis WD, Grant D (1991) A linkage map based on information from four F2 populations of maize (Zea mays L.). Theor Appl Genet 82:636–644

    CAS  Google Scholar 

  • Bernatzky R, Tanksley SD (1986) Toward a saturated linkage map in tomato based on isozymes and random cDNA sequences. Genetics 112:887–898

    Google Scholar 

  • Birnboim HG, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    CAS  PubMed  Google Scholar 

  • Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103

    Google Scholar 

  • Bradshaw HD, Stettler RF (1993) Molecular genetics of growth and development in Populus I. Triploidy in hybrid poplars. Theor Appl Genet 86:301–307

    Google Scholar 

  • Cameron DR, Moav RM (1957) Inheritance in Nicotiana tabacum XXVII. Pollen killer, an alien genetic locus inducing abortion of microspores not carrying it. Genetics 42:326–335

    Google Scholar 

  • Cheliak WM, Skroppa T, Pitel JA (1987) Genetics of the polycross. 1. Experimental results from Norway spruce. Theor Appl Genet 73:321–329

    Google Scholar 

  • Devey ME, Jermstad KD, Tauer CG, Neale DB (1991) Inheritance of RFLP loci in a loblolly pine three-generation pedigree. Theor Appl Genet 83:238–242

    Google Scholar 

  • Doebley J, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129:285–295

    CAS  PubMed  Google Scholar 

  • Doebley J, Stec A, Wendel J, Edwards M (1990) Genetic and morphological analysis of a maize-teosinte F2 population: implications for the origin of maize. Proc Natl Acad Sci USA 87:9888–9892

    Google Scholar 

  • Durham RE, Liou PC, Gmitter FG Jr, Moore GA (1992) Linkage of restriction fragment length polymorphisms and isozymes in Citrus. Theor Appl Genet 84:39–48

    Google Scholar 

  • Edwards MD, Stuber CW, Wendel JF (1987) Molecular-marker-facilitated investigations of quantitative-trait loci in maize. I. Numbers, genomic distribution and types of gene action. Genetics 116:113–125

    CAS  PubMed  Google Scholar 

  • Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B, Schach-tschabel U, Kaufmann H, Thompson RD, Bonierbale MW, Ganal MW, Tanksley SD, Salamini F (1991) RFLP maps of potato and their alignment with the homoeologous tomato genome. Theor Appl Genet 83:49–57

    Google Scholar 

  • Gillet E, Gregorius H-R (1992) What can be inferred from open-pollination progenies about the source of observed segregation distortion? A case study in Castanea sativa Mill. Silvae Genet 41:82–87

    Google Scholar 

  • Graner A, Jahoor A, Schondelmaier J, Siedler H, Pillen K, Fischbeck G, Wenzel G, Herrmann RG (1991) Construction of an RFLP map of barley. Theor Appl Genet 83:250–256

    Google Scholar 

  • Grant V (1971) Plant speciation. Columbia University Press, New York

    Google Scholar 

  • Guries RP, Stettler RF (1976) Pre-fertilization barriers to hybridization in the poplars. Silvae Genet 25:37–44

    Google Scholar 

  • Haldane JBS (1919) The combination of linkage values and the calculation of distances between the loci of linked factors. J Genet 8:299–309

    Google Scholar 

  • Hamrick JL, Linhart YB, Mitton JB (1979) Relationships between life history characteristics and electrophoretically detectable genetic variation in plants. Ann Rev Ecol Syst 10:173–200

    Article  Google Scholar 

  • Heilman PE, Stettler RF (1985) Genetic variation and productivity of Populus trichocarpa T. & G. and its hybrids. II. Biomass production in a 4-year plantation. Can J For Res 15:384–388

    Google Scholar 

  • Johnson LPV (1947) A note on the inheritance in F1 and F2 hybrids of Populus alba L. x P. grandidentata Michx. Can J Res Sect C 24:313–317

    Google Scholar 

  • Kang H, Hardner C, Gullberg U (1992) Lethal equivalents in willow, Salix viminalis. Silvae Genet 41:110–117

    Google Scholar 

  • Kasha KJ, Kao KN (1970) High frequency haploid production in barley (Hordeum vulgare L.) Nature 225:874–876

    Google Scholar 

  • Keim P, Paige KN, Whitham TG, Lark KG (1989) Genetic analysis of an interspecific hybrid swarm of Populus: Occurrence of unidirectional introgression. Genetics 123:557–565

    Google Scholar 

  • Keim P, Diers BW, Olson TC, Shoemaker RC (1990) RFLP mapping in soybean: association between marker loci and variation in quantitative traits. Genetics 126:735–742

    Google Scholar 

  • Klekowski (1988) Mutation, developmental selection, and plant evolution. Columbia University Press, New York

    Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    CAS  PubMed  Google Scholar 

  • Landry BS, Kesseli RV, Ferrara B, Michelmore RW (1987) A genetic map of lettuce (Lactuca sativa L.) with restriction fragment length polymorphism, isozyme, disease resistance, and morphological markers. Genetics 116:331–337

    Google Scholar 

  • Ledig FT (1986) Heterozygosity, heterosis, and fitness in outbreeding plants. In: Soule ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Assoc, Sunderland, Mass., pp 77–104

    Google Scholar 

  • Lin SY, Ikehashi S, Yanagihara S, Kawashima A (1992) Segregation distortion via male gametes in hybrids between Indica and Japonica or wide-compatibility varieties of rice (Oryza sativa L.). Theor Appl Genet 84:812–818

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • McCouch SR, Kochert G, Yu Z-H, Wang Z-Y, Khush GS, Coffman WR, Tanksley SD (1988) Molecular mapping of rice chromosomes. Theor Appl Genet 76:815–829

    CAS  Google Scholar 

  • Melchior GH, Seitz FW (1968) Interspezifische Kreuzungssterilitat innerhalb der Pappelsektion Aigeiros. Silvae Genet 17:88–93

    Google Scholar 

  • Morton NE, Crow JF, Muller HJ (1956) An estimate of mutational damage in man from data on consanguineous marriages. Proc Natl Acad Sci USA 42:855–863

    Google Scholar 

  • Ott J (1985) Analysis of human genetic linkage. The Johns Hopkins University Press, Baltimore, Me.

    Google Scholar 

  • Paige KN, Capman WC, Jenetten P (1991) Mitochondrial inheritance patterns across a cottonwood hybrid zone: cytonuclear disequilibria and hybrid zone dynamics. Evolution 45:1360–1369

    CAS  PubMed  Google Scholar 

  • Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD (1988) Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–726

    Article  CAS  PubMed  Google Scholar 

  • Paterson AH, Damon S, Hewitt JD, Zamir D, Rabinowitch HD, Lincoln SE, Lander ES, Tanksley SD (1991) Mendelian factors underlying quantitative traits in tomato: comparison across species, generations, and environments. Genetics 127:181–197

    Google Scholar 

  • Patton DA, Franzmann LH, Meinke DW (1991) Mapping genes essential for embryo development in Arabidopsis thaliana. Mol Gen Genet 227:337–347

    Google Scholar 

  • Reiter RS, Coors JG, Sussman MR, Gabelman WH (1991) Genetic analysis of tolerance to low-phosphorus stress in maize using restriction fragment length polymorphisms. Theor Appl Genet 82:561–568

    Google Scholar 

  • Rychlik W, Rhoads RE (1989) A computer program for choosing optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of DNA. Nucleic Acids Res 17:8543–8551

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5468

    CAS  PubMed  Google Scholar 

  • Sorensen F (1967) Linkage between marker genes and embryonic lethal factors may cause disturbed segregation ratios. Silvae Genet 16:132–134

    Google Scholar 

  • Sorensen F (1969) Embryonic genetic load in coastal Douglas-fir, Pseudotsuga menziesii var ‘menziesii’. Am Nat 103:389–398

    Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Columbia Univ Press, New York

    Google Scholar 

  • Stephens SG (1949) The cytogenetics of speciation in Gossypium. I. Selective elimination of the donor parent genotype in interspecific backcrosses. Genetics 34:627–637

    Google Scholar 

  • Stettler RF, Bawa KS (1971) Experimental induction of haploid parthenogenesis in black cottonwood (Populus trichocarpa T. & G. ex Hook). Silvae Genet 20:15–25

    Google Scholar 

  • Stettler RF, Koster R, Steenackers V (1980) Interspecific crossability studies in poplars. Theor Appl Genet 58:273–282

    Google Scholar 

  • Strauss SH, Conkle MT (1986) Segregation, linkage and diversity of allozymes in knobcone pine. Theor Appl Genet 72:483–493

    Google Scholar 

  • Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular markerbased linkage map of Phaseolus vulgaris L. Genetics 131:733–740

    Google Scholar 

  • Weller JI, Soller M, Brody T (1988) Linkage analysis of quantitative traits in an interspecific cross of tomato (Lycopersicon esculentum x Lycopersicon pimpinellifolium) by means of genetic markers. Genetics 118:329–339

    Google Scholar 

  • Zamir D, Tadmor Y (1986) Unequal segregation of nuclear genes in plants. Bot Gaz 147:355–358

    Article  Google Scholar 

  • Zsuffa L (1975) A summary review of interspecific breeding in the genus Populus. In: Fowler DP, Yeatman CW (eds) Proc 14th Meet Can Tree Improvement Assoc Part 2. Fredericton, New Brunswick, pp 107–123

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Communicated by P. M. A. Tigerstedt

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Bradshaw, H.D., Stettler, R.F. Molecular genetics of growth and development in Populus. II. Segregation distortion due to genetic load. Theoret. Appl. Genetics 89, 551–558 (1994). https://doi.org/10.1007/BF00222447

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  • DOI: https://doi.org/10.1007/BF00222447

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