Abstract
Hybrid lethality was identified in interspecific hybrids between two cotton species, Gossypium hirsutum and G. barbadense cv. Coastland R4-4 (R4-4). Genetic analysis indicated that the lethal symptom was controlled by two dominant complementary genes, one from G. hirsutum and another from R4-4. Microsatellite mapping identified the location of the causal gene in G. hirsutum as chromosome D8, while the R4-4 gene was placed on chromosome D11. Our data indicate that these genes conform to the Dobzhansky–Muller model, and are novel for the induction of hybrid lethality in Gossypium. Following the genetic nomenclature, we propose that the two novel Dobzhansky–Muller genes from G. hirsutum and from R4-4 be named Le 3 and Le 4 , respectively. Given what we know about their inheritance patterns, their genotypes should be Le 3 Le 3 le 4 le 4 in G. hirsutum, and le 3 le 3 Le 4 Le 4 in R4-4. Data from this study supported previous information in that expression of the lethal symptom might be affected by the dosage of causal alleles and the environment in which plants are growing.
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References
Bakker EG, Toomajian C, Kreitman M, Bergelson J (2006) A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell 18:1803–1818
Barbash DA, Siino DF, Tarone AM, Roote J (2003) A rapidly evolving MYB related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA 100:5302–5307
Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a common barrier to gene flow in plants. Nat Rev Genet 8:382–393
Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky–Muller-type incompatibility syndrome in plants. PLoS Biol 5(9):1962–1972
Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA (2006) Two Dobzhansky–Muller genes interact to cause hybrid lethality in Drosophila. Science 314:1292–1295
Caldwell RM, Compton LE (1943) Complementary lethal genes in wheat causing a progressive lethal necrosis of seedlings. J Hered 34:67–70
Christie P, MacNair MR (1984) Complementary lethal factors in two North American populations of the yellow monkey flower. J Hered 75:510–511
Chu Y, Oka H (1972) The distribution and effects of genes causing F1 weakness in Oryza breviligulata and O glaberrima. Genetics 70:163–173
Chu CG, Faris JD, Friesen TL, Xu SS (2006) Molecular mapping of hybrid necrosis genes Ne1 and Ne2 in hexaploid wheat using microsatellite markers. Theor Appl Genet 112:1374–1381
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Inc, Sunderland, MA
Dobzhansky TH (1937) Genetics and the origin of species. Columbia University Press, New York
Gerstel DU (1954) A new lethal combination in interspecific cotton hybrids. Genetics 39:628–639
Guo WZ, Cai CP, Wang CB, Han ZG, Song XL, Wang K, Niu XW, Wang C, Lu KY, Shi B, Zhang TZ (2007) A microsatellite-based, gene-rich linkage map reveals genome structure, function, and evolution in Gossypium. Genetics 176:527–541
Hollingshead LA (1930) A lethal factor in Crepis effective only in an interspecific hybrid. Genetics 15:114–140
Hudson RR, Kreitman MK, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159
Hutchinson JB (1932) The genetics of cotton. VII. ‘Crumpled’, a new dominant in Asiatic cottons produced by complementary factors. J Genet 25:281–291
Hutchinson J (1959) The application of genetics to cotton improvement. Cambridge University Press, London
Ichitani K, Fukuta Y, Taura S, Sato M (2001) Chromosomal location of Hwc2, one of the complementary hybrid weakness genes, in rice. Plant Breed 120:523–525
Ichitani K, Namigoshi K, Sato M, Taura S, Aoki M (2007) Fine mapping and allelic dosage effect of Hwc1, a complementary hybrid weakness gene in rice. Theor Appl Genet 114:1407–1415
Jenkins JG (1953) Coastland-A new long staple cotton for the Southeast. Georgia Coastal Plain Exp Stn Bull 53
Kerr T (1960) The potentials of barbadense cottons. In: Proceedings of the 12th cotton improvement conference, Memphis, pp 57–60
Kohel RJ (1973) Genetic nomenclature in cotton. Hered 64:291–295
Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175
Lee JA (1981a) Genetics of D3 complementary lethality in Gossypium hirsutum and G. barbadense. J Hered 72:299–300
Lee JA (1981b) A new linkage relationship in cotton. Crop Sci 21:346–347
Mallet J (2006) What does Drosophila genetics tell us about speciation? Trends Ecol Evol 21:386–393
Manabe T, Marubashi W, Onozawa Y (1989) Temperature-dependent conditional lethality in interspecific hybrids between Nicotiana suaveolens Lehm. and N. tabacum L. In: Proceedings of the 6th International Congress of the Society for the Advancement of Breeding Researches in Asia and Oceania (SABRAO), Philippine Rice Research Institute, Philippines. pp 459–462
Marubashi W, Tezuka T (2006) Hybrid lethality in interspecific hybrids between Nicotiana tabacum and N. suaveolens: evidence that the Q chromosome causes hybrid lethality based on Q-chromosome-specific DNA markers. Theor Appl Genet 112:1172–1178
Masuda Y, Yamada T, Kuboyama T, Marubashi W (2007) Identification and characterization of genes involved in hybrid lethality in hybrid tobacco cells (Nicotiana suaveolens × N. tabacum) using suppression subtractive hybridization. Plant Cell Rep 26:1595–1604
Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York
McNaughton IH, Harper JL (1960) The comparative biology of closely related species living in the same area. II. Aberrant morphology and a virus-like syndrome in hybrids between Papaver rhoeas L. and P. dubium L. New Phytol 59:27–41
Michelmore RW, Paran IP, Kesseli RV (1991) Identification of markers linked to disease resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832
Mino M, Maekawa K, Ogawa K, Yamagishi H, Inoue M (2002) Cell death processes during expression of hybrid lethality in interspecific F1 hybrid between Nicotiana gossei Domin and Nicotiana tabacum. Plant Physiol 130:1776–1787
Moyle LC, Graham EB (2005) Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum. Genetics 169:355–373
Muller HJ (1942) Isolating mechanisms, evolution, and temperature. Biol Symp 6:71–125
Orr HA (2005) The genetic basis of reproductive isolation: insights from Drosophila. Proc Natl Acad Sci USA 102(1):6522–6526
Orr HA, Presgraves DC (2000) Speciation by postzygotic isolation: forces, genes and molecules. BioEssays 22:1085–1094
Paterson AH, Brubaker C, Wendel JF (1993) A rapid method for extraction of cotton (Gossypium spp.) genomic DNA suitable for RFLP or PCR analysis. Plant Mol Biol Rep 11:122–127
Philips LL (1977) Interspecific incompatibility in Gossypium. IV. Temperature-conditional lethality in hybrids of G. klotzschianum. Am J Bot 64:914–915
Philips LL, Merritt JF (1972) Interspecific compatibility in Gossypium. I. Stem histogenesis of G. hirsutum × G. gossypioides. Am J Bot 59:203–208
Phillips LL (1976) Interspecific incompatibility in Gossypium. III. The genetics of tumorigenesis in hybrids of G. gossypioides. Can J Genet Cytol 18:365–369
Phillips LL, Reid RK (1975) Interspecific compatibility in Gossypium. II. Light and electron microscopic studies of cell necrosis and tumorigenesis in hybrid of G. klotzschianum. Am J Bot 62:790–796
Presgraves DC (2002) Patterns of postzygotic isolation in Lepidoptera. Evolution 56:1168–1183
Presgraves DC, Stephan W (2007) Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96. Mol Biol Evol 24:306–314
Presgraves DC, Balagopalan L, Abmayr SM, Orr HA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423:715–719
Price TD, Bouvier MM (2002) The evolution of F1 postzygotic incompatibilities in birds. Evolution 56:2083–2089
Provine WB (1991) Alfred Henry Sturtevant and crosses between Drosophila melanogaster and Drosophila simulans. Genetics 129:1–5
Rooney WL, Stelly DM (1990) Genetic effects on the timing of Le daw 2 induced necrosis of cotton. Crop Sci 30:70–74
Samora PJ, Stelly DM, Kohel RJ (1994) Localization and mapping of the Le 1 and Gl 2 loci of cotton (Gossypium hirsutum L.). J Hered 85:152–156
Sasa MM, Chippendale PT, Johnson NA (1998) Patterns of postzygotic isolation in frogs. Evolution 52:1811–1820
Sato YI, Hayashi J (1983) Distribution of the complementary genes causing Fl weakness in the common rice and its wild relatives I. L-2-a gene in Asian native cultivars. Jpn J Genet 58:411–418
Saunders AR (1952) Complementary lethal genes in the cowpea. S Afr J Sci 48:195–197
Savant AC (1956) Semilethal complementary factors in a tomato species hybrid. Evolution 10:93–96
Seelanan T, Schnabel A, Wendel JF (1997) Congruence and consensus in the cotton tribe. Syst Bot 22:259–290
Shii CT, Mok MC, Temple SR, Mok DWS (1980) Expression of developmental abnormalities of Phaseolus vulgaris L. Interaction between temperature and allelic dosage. J Hered 71:219–222
Silow RA (1941) The comparative genetics of Gossypium anomalum and the cultivated Asiatic cottons. J Genet 42:259–358
Singh SP, Gutiérrez JA (1984) Geographical distribution of the DL1 and DL2 genes causing hybrid dwarfism in Phaseolus vulgaris L., their association with seed size, and their significance to breeding. Euphytica 33:337–345
Small RL, Wendel JF (2002) Differential evolutionary dynamics of duplicated paralogous Adh loci in allotetraploid cotton (Gossypium). Mol Biol Evol 19:597–607
Small RL, Ryburn JA, Cronn RC, Seelanan T, Wendel JF (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear Adh sequences for phylogeny reconstruction in a recently diverged plant group. Am J Bot 85:1301–1315
Small RL, Ryburn JA, Wendel JF (1999) Low levels of nucleotide diversity at homoeologous Adh loci in allotetraploid cotton (Gossypium L.). Mol Biol Evol 16:491–501
Stebbins GL (1966) Reproductive isolation and the origin of species. In: Processes of organic evolution. Prentice-Hall, New Jersey. pp 85–112
Stelly DM (1990) Localization of the Le2 Locus of cotton (Gossypium hirsutum L.). J Hered 81:193–197
Stephens SG (1946) The genetics of Corky. PartI. The new world alleles and their possible role as an interspecific isolating mechanism. J Genet 47:150–161
Stephens SG (1975) Some observations on photoperiodism and the development of annual forms of domesticated cottons. Econ Bot 30:409–418
Stephens SG (1976) The origin of Sea Island cotton. Agric History 50:391–399
Tsunewaki K (1970) Necrosis and chlorosis genes in common wheat and its ancestral species. Seiken Ziho 22:67–75
Valkonen JPT, Watanabe KN (1999) Autonomous cell death, temperature sensitivity and the genetic control associated with resistance to cucumber mosaic virus (CMV) in diploid potatoes (Solanum spp.). Theor Appl Genet 99:996–1005
Van Ooijen JW, Voorrips RE (2001) JoinMapR Version 3.0: software for the calculation of genetic linkage maps. Centre for Plant Breeding and Reproduction Research (CPRO-DLO). Wageningen, The Netherlands
Wang K, Song XL, Han ZG, Guo WZ, Yu JZ, Sun J, Pan JJ, Kohel RJ, Zhang TZ (2006) Complete assignment of the chromosomes of Gossypium hirsutum L. by translocation and fluorescence in situ hybridization mapping. Theor Appl Genet 113:73–80
Wiebe GA (1934) Complementary factors in barley giving a lethal progeny. J Hered 25:272–274
Yamada T, Marubashi W (2003) Overproduced ethylene causes programmed cell death leading to temperature-sensitive lethality in hybrid seedlings from the cross Nicotiana suaveolens × N. tabacum. Planta 217:690–698
Yamada T, Marubashi W, Niwa M (2000) Apoptotic cell death induces temperature-sensitive lethality in hybrid seedlings and calli derived from the cross of Nicotiana suaveolens × N. tabacum. Planta 211:614–622
Yamada T, Marubashi W, Niwa M (2001) Facile induction of apoptosis into plant cells associated with temperature-sensitive lethality shown on interspecific hybrid from the cross Nicotiana suaveolens × N. tabacum. Plant Cell Physiol 42:204–213
Zhang J, Wu YT, Guo WZ, Zhang TZ (2000) Fast screening of microsatellite markers in cotton with PAGE/silver staining. Cotton Sci 12:267–269
Zhang J, Guo WZ, Zhang TZ (2002) Molecular linkage map of allotetraploid cotton (Gossypium hirsutum L. × Gossypium barbadense L.) with a haploid population. Theor Appl Genet 105:1166–1174
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This study is supported by grants from the National Nature Science Foundation of China (30730067), Natural Science Foundation in Jiangsu province (BK 2008036) and the 111 Project (B08025).
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Song, L., Guo, W. & Zhang, T. Interaction of novel Dobzhansky–Muller type genes for the induction of hybrid lethality between Gossypium hirsutum and G. barbadense cv. Coastland R4-4. Theor Appl Genet 119, 33–41 (2009). https://doi.org/10.1007/s00122-009-1014-5
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DOI: https://doi.org/10.1007/s00122-009-1014-5