Abstract
Gametocidal (Gc) genes, introduced into common wheat from related Aegilops species, are selfish genetic elements that ensure their preferential transmission by inducing chromosomal breaks. Here we report the production and characterization of a knock-out mutation of the Gc2 gene transferred to wheat as a wheat-Aegilops sharonensis T4B-4Ssh#l translocation chromosome. In hemizygous Gc2/- condition, gametophytes lacking Gc2 suffer chromosomal fragmentation and produce nonfunctional gametes, which leads to sporophytic semisterility and exclusive transmission of the Gc2-carrier chromosome. We have identified one putative ethyl methylsulfonate (EMS)-induced Gc2 mutant that restores spike fertility and shows Mendelian segregation. Progeny screening mapped the mutation to the Gc2-carrier chromosome T4B-4Ssh#l. C-banding and fluorescence in situ hybridization analyses showed that the loss of Gc2 function in the mutant is not due to a terminal deficiency. Analysis of first and second pollen mitoses in Gc2 mut/-plants and C-banding analysis of testcross progenies showed that no chromosomal breakage occurs in the mutant. No gametophytic chromosomal breakage was observed in heterozygous Gc2 mut/Gc2 plants, which had fully fertile spikes. These results suggest that Gc2 encodes two agents, one causing chromosomal breaks in gametophytes lacking Gc2 and another that protects the Gc2 carrier from breakage. The EMS-induced Gc2 mutant appears to be a knock-out of the gene encoding the ‘breaking’ agent. These data are a first crucial step toward the molecular understanding of Gc2 action.
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References
Anamthawat-Jonsson K, Heslop-Harrison JS (1993) Isolation and characterization of a genome-specific DNA sequence in Triticeae species. Mol Gen Genet 240:151–158
De Las Hedras JI, King IP, Parker JS (2001) 5-azacytidine induces chromosomal breakage in the root tips of wheat carrying the cuckoo chromosome 4S1 from Aegilops sharonensis. Heredity 87:474–479
Endo TR (1978) On the Aegilops chromosomes having gametocidal action on common wheat. In: Ramanujam S (ed) Proceedings of the 5th International Wheat Genetics Symposium, New Delhi, India, pp 306–314
Endo TR (1979) Selective gametocidal action of a chromosome of Aegilops cylindrica in a cultivar of common wheat. Wheat Inf Serv 50:24–28
Endo TR (1982) Gametocidal chromosomes of three Aegilops species in wheat. Can J Genet Cytol 24:201–206
Endo TR (1985) Two types of gametocidal chromosomes of Aegilops sharonensis and Ae. longissima. Jpn J Genet 60:125–135
Endo TR (1988) Induction of chromosomal structural changes by a chromosome of Aegilops cylindrica L. in common wheat. J Hered 79:366–370
Endo TR (1990) Gametocidal chromosomes and their induction of chromosome mutations in wheat. Jpn J Genet 65:135–152
Endo TR (1996) Allocation of a gametocidal chromosome of Aegilops cylindrica to wheat homoeologous group 2. Genes Genet Syst 71:243–246
Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307
Endo TR, Katayama Y (1978) Finding of a selectively retained chromosome of Aegilops caudata L. in common wheat. Wheat Inf Serv 47/48:32–35
Endo TR, Tsunewaki K (1975) Sterility of common wheat with Aegilops triuncialis cytoplasm. J Hered 66:13–18
Faris JD, Laddomada B, Gill BS (1998) Molecular mapping of segregation distortion loci in Aegilops tauschii. Genetics 149:319–327
Finch RA, Miller TE, Bennett MD (1984) “Cuckoo” Aegilops addition chromosome in wheat ensures its transmission by causing chromosome breaks in meiospores lacking it. Chromosoma 90:84–88
Friebe B, Gill BS (1995) Chromosome banding and genome analysis in diploid and cultivated polyploid wheats. In: Jauhar PP (ed) Methods of genome analysis in plants. CRC Press, Boca Raton, New York, London, Tokyo, pp 39–60
Friebe B, Tuleen NA, Jiang J, Gill BS (1993) Standard karyotype of Triticum longissimum and its cytogenetic relationship with T. aestivum. Genome 36:731–742
Friebe B, Tuleen NA, Gill BS (1999) Development and identification of a complete set of Triticum aestivum-Aegilops geniculata chromosome addition lines. Genome 42:374–380
Friebe B, Kynast RG, Gill BS (2000a) Gametocidal factor-induced structural rearrangements in rye chromosomes added to common wheat. Chromosome Res 8:501–511
Friebe B, Qi LL, Nasuda S, Zhang P, Tuleen NA, Gill BS (2000b) Development of a complete set of Triticum aestivum-Aegilops speltoides chromosome addition lines. Theor Appl Genet 101:51–58
Gill BS, Friebe B, Endo TR (1991) Standard karyotype and nomenclature system for description of chromosome bands and structural aberrations in wheat (Triticum aestivum). Genome 34:830–839
Hermann BG, Koschorz B, Wertz K, McLaughlin KJ, Kispert A (1999) A protein kinase encoded by the t complex responder gene causes non-mendelian inheritance. Nature 402:141–146
King IP, Laurie DA (1993) Chromosome damage in early embryo and endosperm development in crosses involving the preferentially transmitted 4S1 chromosome of Aegilops sharonensis. Heredity 70:52–59
Koebner R, Hadfield J (2001) Large-scale mutagenesis directed at specific chromosomes in wheat. Genome 44:45–49
Kota RS, Dvorak J (1988) Genomic instability in wheat induced by chromosome 6B S of Triticum speltoides. Genetics 120:1085–1094
Krieg DR (1963) Ethyl-methanesulfonate-induced reversions of the bacteriophage T4rII mutants. Genetics 48:561–580
Loegering WG, Sears ER (1963) Distorted inheritance of stem-rust resistance in timstein wheat caused by a pollen killer gene. Can J Genet Cytol 5:67–72
Lyttle TW (1991) Segregation distorter. Annu Rev Genet 25:511–557
Lyttle TW (1993) Cheaters sometimes prosper: distortion of Mendelian segregation by meiotic drive. Trends Genet 9:205–210
Maan SS (1975) Exclusive preferential transmission of an alien chromosome in wheat. Crop Sci 15:287–292
Maguire MP (1963) High transmission frequency of a Tripsacum chromosome in corn. Genetics 4:1185–1194
McCallum CM, Comai L, Greene EA, Henikoff S (2000a) Targeting induced local lesions in genomes (TILLING) for plant functional genomics. Plant Physiol 123:439–442
McCallum CM, Comai L, Greene EA, Henikoff S (2000b) Targeted screening for induced mutations. Nat Biotechnol 18:445–447
Merrill C, Bayraktaroglu L, Kusano A, Ganetzky B (1999) Truncated RanGAP encoded by the Segregation Distorter locus of Drosophila. Science 283:1742–1745
Miller TE, Hutchinson J, Chapman V (1982) Investigation of a preferentially transmitted Aegilops sharonensis chromosome in wheat. Theor Appl Genet 61:27–33
Morris R, Sears ER (1967) The cytogenetics of wheat and its relatives. In: Quisenberry KS, Reitz LP (eds) Wheat and wheat improvement. American Society Agronomy No. 13, Madison, Wisconsin, USA, pp 19–87
Naito T, Kusano K, Kobayashi I (1995) Selfish behavior of restriction-modification systems. Science 267:897–899
Nasuda S (1999) Molecular cytogenetic analysis of gametocidal genes in wheat. Ph.D thesis, Department of Plant Pathology, Kansas State University, Manhattan, Kansas, USA
Nasuda S, Friebe B, Gill BS (1998) Gametocidal genes induce chromosome breakage in the interphase prior to the first mitotic cell division of the male gametophyte in wheat. Genetics 149:1115–1124
Rick CM (1966) Abortion of male and female gametes in the tomato determined by allelic interaction. Genetics 53:85–96
Sandler L, Novitsky E (1957) Meiotic drive as an evolutionary force. Am Nat 91:105–110
Sandler L, Hiraizumi Y, Sandler I (1959) Meiotic drive in natural populations of Drosophila melanogaster L. I. The cytogenetic basis of distortion. Genetics 44:233–250
Sano Y (1990) The genetic nature of gamete eliminator in rice. Genetics 125:183–190
Sears ER (1972) The nature of mutation in hexaploid wheat. Symp Biol Hung 12:73–82
Shi F, Endo TR (1999) Genetic induction of structural changes in barley chromosomes added to common wheat by a gametocidal chromosome derived from Aegilops cylindrica. Genes Genet Syst 74:49–54
Shi F, Endo TR (2000) Genetic induction of chromosomal rearrangements in barley chromosome 7H added to common wheat. Chromosoma 109:358–363
Silver LM (1993) The peculiar journey of a selfish chromosome: t-haplotypes and meiotic drive. Trends Genet 9:250–254
Tsujimoto H (1994) Two new sources of gametocidal genes from Aegilops longissima and Ae. sharonensis. Wheat Inf Serv 79:42–46
Tsujimoto H (1995) Gametocidal genes in wheat and its relatives. IV. Functional relationships between six gametocidal genes. Genome 38:283–289
Tsujimoto H, Noda K (1989) Structure of chromosome 5 A of wheat speltoid mutants induced by the gametocidal genes of Aegilops speltoides. Genome 32:1085–1090
Tsujimoto H, Tsunewaki K (1983) Genetic analyses of a gametocidal gene originated from Aegilops aucherri. In: Sakamoto S (ed) Proceedings 6th International Wheat Genetics Symposium, Kyoto, Japan, pp 1077–1081
Tsujimoto H, Tsunewaki K (1985a) Hybrid dysgenesis in common wheat caused by gametocidal genes. Jpn J Genet 60:565–578
Tsujimoto H, Tsunewaki K (1985b) Gametocidal genes in wheat and its relatives. II. Suppressor of chromosome 3C gametocidal gene of Aegilops triuncialis. Can J Genet Cytol 27:178–185
Tsunewaki K (1980) Genetic diversity of the cytoplasms in Triticum and Aegilops. Japanese Society for the Promotion of Science, Tokyo, Japan
Tsunewaki K (1993) Genome-plasmon interactions in wheat. Jpn J Genet 68:1–34
Williams D, Miller JD, Klindworth DL (1992) Induced mutations of a genetic suppressor of resistance to wheat stem rust. Crop Sci 32:612–616
Wilson GG, Murray NE (1991) Restriction-modification systems. Annu Rev Genet 25:585–627
Zhang P, Friebe B, Lukaszewski AJ, Gill BS (2001) The centromere structure in Robertsonian wheat-rye translocation chromosomes indicates that centric breakage-fusion can occur at different positions within the primary constriction. Chromosoma 110:335–344
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Published online: 21 March 2003
Edited by: D. Schweizer
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Friebe, B., Zhang, P., Gill, B.S. et al. Characterization of a knock-out mutation at the Gc2 locus in wheat. Chromosoma 111, 509–517 (2003). https://doi.org/10.1007/s00412-003-0234-8
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DOI: https://doi.org/10.1007/s00412-003-0234-8
Keywords
- Common Wheat
- Pollen Mitosis
- Testcross Progeny
- Selfish Genetic Element
- Gametocidal Chromosome