Abstract
Since the dawn of wheat cytogenetics, chromosome 3B has been known to harbor a gene(s) that, when removed, causes chromosome desynapsis and gametic sterility. The lack of natural genetic diversity for this gene(s) has prevented any attempt to fine map and further characterize it. Here, gamma radiation treatment was used to create artificial diversity for this locus. A total of 696 radiation hybrid lines were genotyped with a custom mini array of 140 DArT markers, selected to evenly span the whole 3B chromosome. The resulting map spanned 2,852 centi Ray with a calculated resolution of 0.384 Mb. Phenotyping for the occurrence of meiotic desynapsis was conducted by measuring the level of gametic sterility as seeds produced per spikelet and pollen viability at booting. Composite interval mapping revealed a single QTL with LOD of 16.2 and r 2 of 25.6 % between markers wmc326 and wPt-8983 on the long arm of chromosome 3B. By independent analysis, the location of the QTL was confirmed to be within the deletion bin 3BL7-0.63-1.00 and to correspond to a single gene located ~1.4 Mb away from wPt-8983. The meiotic behavior of lines lacking this gene was characterized cytogenetically to reveal striking similarities with mutants for the dy locus, located on the syntenic chromosome 3 of maize. This represents the first example to date of employing radiation hybrids for QTL analysis. The success achieved by this approach provides an ideal starting point for the final cloning of this interesting gene involved in meiosis of cereals.
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Abbreviations
- 3B-RH:
-
Radiation hybrids for chromosome 3B
- cR:
-
Centi Rays
- CS:
-
Chinese Spring
- DArT:
-
Diversity Arrays Technology
- Gy:
-
Gray
- H 2 :
-
Broad sense heritability
- LDN:
-
Langdon
- LDN 3D (3B):
-
Langdon substitution line 3D for 3B
- M1 :
-
Mutant generation 1
- MS:
-
Mean sum of squares
- MSg:
-
Mean sum of squares for the genotype
- MSge:
-
Mean sum of squares for the genotype by environment
- PV:
-
Pollen viability
- QTL:
-
Quantitative trait loci
- RH0 or RH1 :
-
Radiation hybrid generation 0 or 1
- SpS:
-
Seeds per spikelet
- SSR:
-
Single sequence repeat
References
Akbari M, Wenzl P, Caig V et al (2006) Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor Appl Genet 113:1409–1420
Al-Kaff N, Knight E, Bertin I, Foote T, Hart N, Griffiths S, Moore G (2008) Detailed dissection of the chromosomal region containing the Ph1 locus in wheat Triticum aestivum: with deletion mutants and expression profiling. Ann Bot 101:863–872
Baskaran R (2010) Emerging role of radiation induced bystander effects: cell communications and carcinogenesis. Genome Integr 1:13
Beadle GW (1930) Genetic and cytological studies of a Mendelian asynaptic in Zea mays. Cornell Agric Exp Stn Mem 129:1–23
Bolot S, Abrouk M, Masood-Quraishi U et al (2009) The ‘inner circle’ of the cereal genomes. Curr Opin Plant Biol 12:119–125
Bourne GH, Danielli JF (1979) International review of cytology, vol 58. Academic Press Inc, London
Brenchley R, Spannagl M, Pfeifer M et al (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491(7426):705–710
Cande ZW, Freeling M (2011) Inna Golubovskaya: the life of a geneticist studying meiosis. Genetics 188(3):491–498
Caryl AP, Gareth HJ, Franklin FCH (2003) Dissecting plant meiosis using Arabidopsis thaliana mutants. J Exp Botany 54(380):25–38
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Cox DR, Burmeister M, Price ER, Kim S, Myers RM (1990) Radiation hybrid mapping: a somatic cell genetic method for construction of high-resolution maps of mammalian chromosomes. Science 250:245–250
de Boer E, Heyting C (2006) The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115:220–234
de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) Carthagene: multi population integrated genetic and radiated hybrid mapping. Bioinformatics 21:1703–1704
Devos KM, Sorrells ME, Anderson JA et al (1999) Chromosome aberrations in wheat nullisomic-tetrasomic and ditelosomic lines. Cereal Res Commun 27(3):231–239
Dolezel J, Simkova H, Kubalakova M et al (2009) Chromosome genomics in the Triticeae. In: Feuillet C, Muehlbauer GJ (eds) Genetics and genomics of the Triticeae. Springer, New York, pp 285–316
Elkonin LA, Tsvetova MI (2012) Heritable effect of plant water availability conditions on restoration of male fertility in the “9E” CMS-inducing cytoplasm of sorghum. Front Plant Sci 3:91
Endo TR, Gill BS (1996) The deletion stock of common wheat. J Hered 87(4):295–307
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Addison Wesley Longman Limited, Edinburgh Gate
Faraut T (2009) Contribution of radiation hybrids to genome mapping in domestic animals. Cytogenet Genome Res 126:21–33
Faris JD, Gill BS (2003) Genomic targeting and high-resolution mapping of the domestication gene Q in wheat. Genome 45:706–719
Franckowiak JD, Lundqvist U (2008) Table of barley genetic stock description. Barley Genetics Newsl 38:134–164
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
Gill KS, Gill BS, Endo TR, Boyko EV (1996) Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat. Genetics 143:1001–1012
Goss SJ, Harris H (1975) New method for mapping genes in human chromosomes. Nature 255:680–684
Guidet F, Rogowsky P, Taylor C, Song W, Langridge P (1991) Cloning and characterisation of a new rye-specific repeated sequence. Genome 34:81–87
Hallauer AR, Miranda JB (1988) Quantitative research in maize breeding. Iowa State University Press, Ames
Hassold T, Sherman S, Hunt P (2009) Counting cross-overs: characterizing meiotic recombination in mammals. Hum Mol Genet 9(16):2409–2419
Henderson AS (1970) The time and place of meiotic crossing-over. Annu Rev Genet 4:295–324
Hernandez-Soriano JM, Ramage RT (1973) Desynaptic genes. Barley Genetics Newsl 4:123–125
Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19(20):2488–2500
Hossain KG, Riera-Lizarazu O, Kalavacharla V, Vales MI, Maan SS, Kianian SF (2004) Radiation hybrid mapping of the species cytoplasm-specific (scs ae) gene in wheat. Genetics 168:415–423
Huang BE, George AW, Forrest KL, Kilian A, Hayden MJ, Morell MK, Cavanagh CR (2012) A multiparent advanced generation inter-cross population for genetic analysis in wheat. Plant Biotechnol J 10:826–839
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Joppa LR, Williams ND (1977) D-genome substitution monosomics of durum wheat. Crop Sci 17:772–776
Joppa LR, Williams ND (1988) Langdon durum disomic substitution lines and aneuploid analysis in tetraploid wheat. Genome 30:222–228
Joppa LR, Williams ND (1993) The Langdon durum disomic-substitutions: development, characteristics, and uses. Agron Abstr, p 68
Kalavacharla V, Hossain K, Gu Y et al (2006) High-resolution radiation hybrid map of wheat chromosome 1D. Genetics 173:1089–1099
Kim N (2001) Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet 35:673–745
Kumar A, Bassi FM, Paux E et al (2012a) DNA repair and crossing over favor similar chromosome regions as discovered in radiation hybrids of Triticum. BMC Genomics 13:339
Kumar A, Simons K, Iqbal M et al (2012b) Physical mapping resources for large plant genomes: radiation hybrids for wheat D-genome progenitor Aegilops tauschii. BMC Genomics 13:597
Kynast RG, Okagaki RJ, Rines HW, Phillips RL (2002) Maize individualized chromosome and derived radiation hybrid lines and their use in functional genomics. Funct Integr Genomic 2:60–69
Li HW, Pao WK, Li CH (1945) Desynapsis in the common wheat. Am J Bot 32(2):92–101
Martini G, Bozzini A (1966) Radiation induced asynaptic muattions in durum wheat (Triticum durum Desf.). Chromosoma 20:251–266
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Apples R, Xia XC (2011) Catalogue of gene symbols for wheat: 2011 supplement. Annu Wheat Newsl 57
Michalak de Jimenez MK, Bassi FM, Ghavami F et al (2013) A radiation hybrid map of chromosome 1D reveals synteny conservation at a wheat speciation locus. Funct Integr Genomics 13:19–32
Murphy SP, Bass HW (2012) The maize (Zea mays) desynaptic (dy) mutation defines a pathway for meiotic chromosome segregation, linking nuclear morphology, telomere distribution and synapsis. J Cell Sci 125(15):3681–3690
Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556
Paux E, Roger D, Badaeva E, Gay G, Bernard M, Sourdille P, Feuillet C (2006) Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J 48:463–474
Paux E, Sourdille P, Salse J et al (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104
Paux E, Faure S, Choulet F et al (2010) Insertion site-based polymorphism markers open new perspectives for genome saturation and marker-assisted selection in wheat. Plant Biotechnol J 8:196–210
Pawlowski WP, Golubovskaya IN, Cande WZ (2003) Altered nuclear distribution of recombination protein RAD51 in maize mutants suggests the involvement of RAD51 in meiotic homology recognition. Plant Cell 15:1807–1816
Peterson R, Slovin JP, Chen C (2010) A simplified method for differential staining of aborted and non-aborted pollen grains. Int J Plant Biol 1:e13
Qiao H, Chen JK, Reynolds A, Hoog C, Paddy M, Hunter N (2012) Interplay between synaptonemal complex, homologous recombination, and centromeres during mammalian meiosis. PLoS Genet 8(6):e1002790
Raman H, Zhang K, Cakir M et al (2005) Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 8:781–791
Ross KJ, Fransz P, Jones GH (1996) A light microscope atlas of meiosis in Arabidopsis thaliana. Chromosom Res 4:507–516
Rustenholz C, Choulet F, Laugier C et al (2011) A 3,000-loci transcript map of chromosome 3B unravels the structural and functional features of gene islands in hexaploid wheat. Plant Physiol 157:1596–1608
Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, dynamics. Science 326:1112–1115
Schramm S, Fraune J, Naumann R et al (2011) A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility. PLoS Genet 7(5):e1002088
Sears ER (1954) The aneuploids of common wheat. Missouri Agr Exp Stn Res Bull 572:1–58
Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114
Song QJ, Shi JR, Singh S et al (2005) Development and mapping of microsatellite (SSR) markers in wheat. Theor Appl Genet 110:550–560
Sutka J, Galiba G, Vagujfalvi A, Gill BS, Snape JW (1999) Physical mapping of Vrn-A1 and genes on chromosome 5A of wheat using deletion line. Theor Appl Genet 99:199–202
Tanaka A, Shikazono N, Hase Y (2010) Studies on biological effects of ion beams on lethality, molecular nature of mutation, mutation rate, and spectrum of mutation phenotype for mutation breeding in higher plants. J Radiat Res 51:223–233
The International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768
Tiwari VK, Riera-Lizarazu O, Gunn HL et al (2012) Endosperm tolerance of paternal aneuploidy allows radiation-hybrid mapping of the wheat D-genome and a measure of γ ray-induced chromosome breaks. PLoS ONE 7(11):e48815
Tsilo TJ, Hareland GA, Chao S, Anderson JA (2011) Genetic mapping and QTL analysis of flour color and milling yield related traits using recombinant inbred lines in hard red spring wheat. Crop Sci 51:237–246
Wang S, Basten CJ, Zeng ZB (2011) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh
Watanabe N, Koval SF (2003) Mapping of chlorine mutant genes on the long arm of homoeologous group 7 chromosomes in common wheat with partial deletion lines. Euphytica 129:259–265
Wenzl P, Suchánková P, Carling J et al (2010) Isolated chromosomes as a new and efficient source of DArT markers for the saturation of genetic maps. Theor Appl Genet 121:465–474
Xu SJ, Joppa LR (1995) Mechanisms and inheritance of first division restitution in hybrids of wheat, rye, and Aegilops squarrosa. Genome 38:607–615
Xu SJ, Joppa LR (2000) Hexaploid triticales from hybrids of Langdon durum D-genome substitutions with rye. Plant Breed 119:223–226
Zhirov EG, Bessarab KS, Gubanova MA (1974) Genetic studies on partial desynapsis in soft wheat. Soviet Genetics 9(1):10–18
Zhou C, Dong W, Han L et al (2012) Construction of whole genome radiation hybrid panels and map of chromosome 5A of wheat using asymmetric somatic hybridization. PLoS ONE 7(7):e40214
Acknowledgments
The authors wish to thank Professor Wojtek Pawlowski (Cornell University, NY) for in-depth revision and insightful comments on this manuscript, Justin Hegstad and Allen Peckrul for their qualified technical help. This work was supported by funding from the National Science Foundation, Plant Genome Research Program (NSF-PGRP) grant No. IOS-0822100 to SFK. F.M.B was partially supported by Program Master and Back Regione Autonoma della Sardegna and Monsanto Beachell-Borlaug International Scholarship.
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Bassi, F.M., Kumar, A., Zhang, Q. et al. Radiation hybrid QTL mapping of Tdes2 involved in the first meiotic division of wheat. Theor Appl Genet 126, 1977–1990 (2013). https://doi.org/10.1007/s00122-013-2111-z
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DOI: https://doi.org/10.1007/s00122-013-2111-z