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Transfer of resistance to potato virus Y (PVY) from Nicotiana africana to Nicotiana tabacum: possible influence of tissue culture on the rate of introgression

Theoretical and Applied Genetics volume 110, pages 678–687 (2005)Cite this article

Abstract

A disomic chromosome addition line of tobacco, Nicotiana tabacum L., was established previously that possesses a single chromosome pair from N. africana [Merxm. and Buttler]. This addition chromosome carries a gene that confers increased resistance to severe strains of potato virus Y (PVY). Methods to increase the probability of gene transfer from alien chromosomes to tobacco (2n=48) are desired. In the research described here, the PVY resistance gene was transferred to a tobacco chromosome from the N. africana addition chromosome in seven independent cases. One introgression event was obtained using conventional backcrossing of the disomic addition line to N. tabacum cv. Petite Havana, while the remaining six events were obtained using a scheme that involved exposure of explants of the addition line to tissue culture. Twenty-six derived 2n=48 individuals heterozygous for PVY resistance were found to exhibit 24 bivalents or 23 bivalents + 2 univalents at metaphase I. Ovular transmission rates for the PVY resistance factor ranged from 25% to 52%, while pollen transmission rates were much lower, ranging from 0 to 39%. Fifty-one random amplified polymorphic DNA (RAPD) markers specific for the intact addition chromosome were identified and used to characterize derived 2n=48/PVY-resistant genotypes. Variability was observed among these plants with respect to the total number of N. africana RAPD markers that were present, which is an indication that crossing over was occurring within each of the seven introgressed chromosome segments. A limited molecular marker-assisted backcrossing experiment allowed for selection of a 2n=48/PVY-resistant individual that possessed only 6 of the 51 original N. africana RAPD markers. In vitro culture is potentially a valuable system for increasing the rate of alien gene transfer in tobacco, and the successful transfer of PVY resistance from N. africana may allow for an increased level and range of resistance to this virus in tobacco.

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References

  • Banks PM, Larkin PJ, Bariana HS, Lagudah ES, Appels R, Waterhouse PM, Brettell RIS, Chen X, Xu HJ, Xin ZY, Qian YT, Zhou XM, Cheng ZM, Zhou GH (1995) The use of cell culture for subchromosomal introgressions of barley yellow dwarf virus resistance from Thinopyrum intermedium to wheat. Genome 38:395–505

    Google Scholar 

  • Benzion G, Phillips RL, Rines HW (1986) Case histories of genetic variability in vitro: oats and maize. In: Vasil IK (ed) Cell culture and somatic cell genetics of plants, vol 3. Academic Press, New York, pp 435–448

  • Burk LG, Durbin RD (1978) The reaction of Nicotiana species to tentoxin. J Hered 69:117–120

    Google Scholar 

  • Burns JA (1982) The chromosomes of Nicotiana africana Merxm.: a recently discovered species. J Hered 73:115–118

    Google Scholar 

  • Campbell KG, Wernsman EA, Fitzmaurice WP, Burns JA (1994) Construction of a designer chromosome in tobacco. Theor Appl Genet 87:837–842

    Article  Google Scholar 

  • Causse MA, Fulton TM, Cho YG, Ahn SN, Chunwongse J, Wu K, Xiao J, Yu Z, Ronald PC, Harrington SE, Second G, McCouch SR, Tanksley SD (1994) Saturated molecular map of the rice genome based on an interspecific backcross population. Genetics 138:1251–1274

    CAS  PubMed  Google Scholar 

  • Chaplin JF, Matzinger DF, Mann TJ (1966) Influence of the homozygous and heterozygous mosaic-resistance factor on quantitative character of flue-cured tobacco. Tob Sci 10:81–84

    Google Scholar 

  • Chen K, Wildman SG (1981) Differentiation of fraction 1 protein in relation to age and distribution of angiosperm groups. Plant Syst Evol 138:89–113

    Google Scholar 

  • Delon R, Fisher CR, Blancard D (1993) Survey on tobacco viruses. CORESTA Inf Bull No 4:72–79

    Google Scholar 

  • Friebe B, Jiang J, Raupp WJ, McIntosh RA, Gill BS (1996) Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status. Euphytica 91:59–87

    Google Scholar 

  • Ganal MW, Tanksley SD (1996) Recombination around the Tm2a and Mi resistance genes in different crosses of Lycopersicon peruvianum . Theor Appl Genet 92:101–108

    Article  CAS  Google Scholar 

  • Gerstel DU, Burns JA, Burk LG (1979) Interspecific hybridizations with an African tobacco, Nicotiana africana Merxm. J Hered 70:342–344

    Google Scholar 

  • Gooding GV, Lapp NA (1980) Distribution, incidence and straits of potato virus Y in North Carolina. Tob Sci 24:91–94

    Google Scholar 

  • Gooding GV, Tolin SA (1973) Strains of potato virus Y affecting flue-cured tobacco in the southeastern United States. Plant Dis Rep 57:200–204

    Google Scholar 

  • Goodspeed TH (1954) The Genus Nicotiana. Chronica Botanica, Waltham, Mass.

    Google Scholar 

  • Hang A, Bregitzer P (1993) Chromosomal variations in immature embryo-derived calli from six barley cultivars. J Hered 84:105–108

    Google Scholar 

  • Hohmann U, Badaeva K, Busch W, Friebe B, Gill BS (1996) Molecular cytogenetic analysis of Agropyron chromatin specifying resistance to barley yellow dwarf virus in wheat. Genome 39:336–347

    Google Scholar 

  • Johnson ES (1999) Identification and marker-assisted selection of a major gene for Phytophthora resistance, its origin, and effect on agronomic characters in tobacco. PhD thesis, North Carolina State University, Raleigh, N.C.

  • Johnson SS, Phillips RL, Rines HW (1987) Possible role of heterochromatin in chromosome breakage induced by tissue culture in oats (Avena sativa L). Genome 29:439–446

    Google Scholar 

  • Johnson ES, Miklas PN, Stavely JR, Martinez-Cruzado JC (1995) Coupling-phase and repulsion-phase RAPDs for marker-assisted selection of PI 181996 rust resistance in common bean. Theor Appl Genet 90:659–664

    Article  Google Scholar 

  • Jorgensen RB, Anderson B (1989) Karyotype analysis of regenerated plants from callus cultures of interspecific hybrids of cultivated barley (Hordeum vulgare L). Theor Appl Genet 77:343–352

    Article  Google Scholar 

  • Kaeppler SM, Phillips RL, Olhoft P (1998) Molecular basis of heritable tissue culture-induced variation in plants. In: Jain SM, Brar DS, Ahloowalia BS (eds) Somaclonal variation and induced mutations in crop improvement. Current plant science and biotechnology in agriculture, vol 32. Kluwer, Dordrecht, pp 465–484

  • Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–2000

    Article  CAS  PubMed  Google Scholar 

  • Knott DR (1987) Transferring alien genes to wheat. In: Heyne EG (ed) Wheat and wheat improvement, 2nd edn. American Society of Agronomy, Madison, Wis. pp 462–471

    Google Scholar 

  • Koelle G (1961) Genetische analyse einer Y-virus (Rippenbraun) resistenten Mutante der Tabaksorte Virgin A. Zuchter 31:71–72

    Article  Google Scholar 

  • Lapitan NLV, Sears RG, Gill BS (1984) Translocations and other karyotypic structural changes in wheat x rye hybrids regenerated from tissue culture. Theor Appl Genet 68:547–554

    Article  Google Scholar 

  • Larkin PJ, Snowcroft WR (1981) Somaclonal variation—a source of variability from cell cultures for plant improvement. Theor Appl Genet 60: 197–214

    Google Scholar 

  • Larkin PJ, Banks PM, Bhati R, Brettell RIS, Davies PA, Ryan SA, Snowcroft WR, Spindler LH, Tanner GJ (1989) From somatic variation to variant plants: mechanisms and applications. Genome 31:705–711

    Google Scholar 

  • Lee M, Phillips RL (1987) Genomic rearrangements in maize induced by tissue culture. Genome 29:122–128

    Google Scholar 

  • Lee M, Phillips RL (1988) The chromosomal basis of somaclonal variation. Annu Rev Physiol Plant Mol Biol 39:413–437

    Article  Google Scholar 

  • Legg PD, Litton CC, Collins GB (1981) Effects of the Nicotiana debneyi black root rot resistance factor on agronomic and chemical traits in burley tobacco. Theor Appl Genet 60:365–368

    Article  Google Scholar 

  • Lewis RS, Wernsman EA (2001) Efforts to initiate construction of a disease resistance package on a designer chromosome in tobacco. Crop Sci 41:1420–1427

    Google Scholar 

  • Liharska T, Koornneef M, van Wordragen M, van Kammen A, Zabel P (1996) Tomato chromosome 6: effect of alien chromosomal segments on recombination frequencies. Genome 39:485–491

    Google Scholar 

  • Lin TY, Kao YY, Lin S, Lin RF, Chen CM, Huang CH, Wang CK, Lin YZ, Chen CC (2001) A genetic linkage map of Nicotiana plumbaginifolia / Nicotiana longiflora based on RFLP and RAPD markers. Theor Appl Genet 103:905–911

    Article  Google Scholar 

  • Linger LR, Wolff ML, Wernsman EA (2000) Comparison of transgenic versus interspecific sources of TMV resistance conferred by the N gene. In: 39th Tobacco Workers’ Conf. Williamsburg, Virginia

  • Lucas GB (1975) Diseases of tobacco, 3rd edn. Biological Consulting Assoc, Raleigh, N.C.

    Google Scholar 

  • Lucas GB, Gooding GV Jr, Sasser JN, Gerstel DU (1980) Reaction of Nicotiana africana to black shank, granville wilt, root knot, tobacco mosaic virus, and potato virus Y. Tob Sci 24:141–142

    Google Scholar 

  • McCoy TJ, Phillips RL, Rines HW (1982) Cytogenetic analysis of plants regenerated from oat (Avena sativa) tissue cultures; high frequency of partial chromosome loss. Can J Genet Cytol 24:37–50

    Google Scholar 

  • Merxmuller H, Buttler KP (1975) Nicotiana in der afrikanischen Namib-ein pflanzengeographisches und phylogenetisches. Ratsel Mitt Bot Munchen 12:91–104

    Google Scholar 

  • Messeguer R, Ganal MW, de Vicente MC, Young ND, Bolkan H, Tanksley SD (1991) High resolution RFLP map around the root-knot nematode resistance gene (Mi ) in tomato. Theor Appl Genet 82:529–536

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Paterson AH, de Verna JW, Lanini B, Tanksley SD (1990) Fine mapping of quantitative trait loci using selected overlapping recombinant chromosomes in an interspecific cross of tomato. Genetics 124:735–742

    CAS  PubMed  Google Scholar 

  • Peschke VM, Phillips RL (1992) Genetic implications of somaclonal variation in plants. Adv Genet 30:41–75

    Google Scholar 

  • Phillips RL, Kaeppler SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proc Natl Acad Sci USA 91:5222–5226

    CAS  PubMed  Google Scholar 

  • Reed SM (1991) Cytogenetic evolution and aneuploidy in Nicotiana. In: Tsuchiya T, Gupta PK (eds) Chromosome engineering in plants: genetics, breeding, evolution, part B. Elsevier, Amsterdam, pp 483–505

    Google Scholar 

  • Riley R, Chapman V, Johnson R (1968) The incorporation of alien disease resistance in wheat by genetic interference with the regulation of meiotic chromosome synapsis. Genet Res 12:198–219

    Google Scholar 

  • Sears ER (1981) Transfer of alien genetic material to wheat. In: Evans LT, Peacock WP (eds) Wheat science—today and tomorrow. Cambridge University Press, Cambridge, pp 75–89

    Google Scholar 

  • Sears ER (1993) Use of radiation to transfer alien segments to wheat. Crop Sci 33:897–901

    Google Scholar 

  • Wernsman EA (1992a) Sources of resistance to virus diseases. CORESTA Inf Bull 1992-3/4, pp 113–119

  • Wernsman EA (1992b) Varied roles for the haploid sporophyte in plant improvement. In: Stalker HT, Murphy JP (eds) Plant breeding in the 1990s. Proc Symposium Plant Breed 1990s. CAB Int, Wallingford, pp 461–484

  • Witherspoon WD (1987) Utilization of the haploid sporophyte as the selection unit in tobacco breeding. PhD thesis, North Carolina State University, Raleigh, N.C.

  • Witherspoon WD, Wernsman EA, Gooding GV Jr, Rufty RC (1991) Characterization of a gametoclonal variant controlling virus resistance in tobacco. Theor Appl Genet 81:1–5

    Google Scholar 

  • Young ND, Tanksley SD (1989) RFLP analysis of the size of chromosomal segments retained around the Tm-2 locus during backcross breeding. Theor Appl Genet 77:353–359

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported in part through a CORESTA study grant provided to the author.

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  1. Department of Crop Science, North Carolina State University, 7620, Raleigh, NC, 27695, USA

    R. S. Lewis

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  1. R. S. Lewis
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Correspondence to R. S. Lewis.

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Communicated by P.S. Heslop-Harrison

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Lewis, R.S. Transfer of resistance to potato virus Y (PVY) from Nicotiana africana to Nicotiana tabacum: possible influence of tissue culture on the rate of introgression. Theor Appl Genet 110, 678–687 (2005). https://doi.org/10.1007/s00122-004-1893-4

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  • DOI: https://doi.org/10.1007/s00122-004-1893-4

Keywords

  • Addition Chromosome
  • BC1F1 Plant
  • Disomic Addition Line
  • BC1F1 Family
  • Introgression Event