Cytogenetic mapping with centromeric bacterial artificial chromosomes contigs shows that this recombination-poor region comprises more than half of barley chromosome 3H

Plant Journal

Volumn 84, Issue 2, 2015, Pages 385-394

  Aliyeva Schnorr, Lala ^a   Beier, Sebastian ^a   Karafiátová, Miroslava ^b   Schmutzer, Thomas ^a   Scholz, Uwe ^a   Doležel, Jaroslav ^b   Stein, Nils ^a   Houben, Andreas ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

BAC FISH; centromere; chromatin; pachytene chromosomes; physical map; posttranslational histone modifications; recombination

Indexed keywords

DNA SEQUENCES; FACSIMILE; FLUORESCENCE; FLUORESCENCE MICROSCOPY; PLANTS (BOTANY); PROBES;

BACTERIAL ARTIFICIAL CHROMOSOMES; CENTROMERE; CHROMATIN; FLUORESCENCE IN SITU HYBRIDIZATION; MEIOTIC RECOMBINATIONS; METAPHASE CHROMOSOMES; POST-TRANSLATIONAL HISTONE MODIFICATIONS; RECOMBINATION;

CHROMOSOMES;

CHROMOSOMAL MAPPING; GENETICS; HORDEUM; PLANT CHROMOSOME;

CHROMOSOME MAPPING; CHROMOSOMES, PLANT; HORDEUM;

EID: 84943626821     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13006     Document Type: Article

References (73)

1. Ariyadasa, R., Mascher, M., Nussbaumer, T., et al. (2014) A sequence-ready physical map of barley anchored genetically by two million single-nucleotide polymorphisms. Plant Physiol. 164, 412-423.
2. Ashida, T., Nasuda, S., Sato, K., and, Endo, T.R., (2007) Dissection of barley chromosome 5H in common wheat. Genes Genet. Syst. 82, 123-133.
3. Baddeley, D., Jayasinghe, I.D., Cremer, C., Cannell, M.B., and, Soeller, C., (2009) Light-induced dark states of organic fluorochromes enable 30 nm resolution imaging in standard media. Biophys. J. 96, L22-L24.
4. Choulet, F., Alberti, A., Theil, S., et al. (2014) Structural and functional partitioning of bread wheat chromosome 3B. Science, 345, 1249721.
5. Close, T.J., Bhat, P.R., Lonardi, S., et al. (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genom. 10, 582.
6. Colmsee, C., Beier, S., Himmelbach, A., Schmutzer, T., Stein, N., Scholz, U., and, Mascher, M., (2015) BARLEX-the barley draft genome explorer. Mol. Plant, 8, 964-966.
7. Comadran, J., Kilian, B., Russell, J., et al. (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat. Genet. 44, 1388-1392.
8. Devaux, P., Kilian, A., and, Kleinhofs, A., (1993) Anther culture and Hordeum bulbosum-derived barley doubled haploids: mutations and methylation. Mol Genet. Genomics, 241, 674-679.
9. Doležel, J., Binarova, P., and, Lucretti, S., (1989) Analysis of nuclear-DNA content in plant-cells by flow-cytometry. Biol Plant. 31, 113-120.
10. Dvorak, J., and, Chen, K.C., (1984) Distribution of nonstructural variation between wheat cultivars along chromosome arm-6 bp-evidence from the linkage map and physical map of the arm. Genetics, 106, 325-333.
11. Fransz, P., Armstrong, S., Alonso-Blanco, C., Fischer, T.C., Torres-Ruiz, R.A., and, Jones, G., (1998) Cytogenetics for the model system Arabidopsis thaliana. Plant J. 13, 867-876.
12. Fuchs, J., Demidov, D., Houben, A., and, Schubert, I., (2006) Chromosomal histone modification patterns-from conservation to diversity. Trends Plant Sci. 11, 199-208.
13. Fukui, K., Kamisugi, Y., and, Sakai, F., (1994) Physical mapping of 5S rDNA loci by direct-cloned biotinylated probes in barley chromosomes. Genome, 37, 105-111.
14. Gernand, D., Demidov, D., and, Houben, A., (2003) The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes. Cytogenet. Genome Res. 101, 172-176.
15. Gill, K.S., and, Gill, B.S., (1994) Mapping in the realm of polyploidy-the wheat model. BioEssays, 16, 841-846.
16. Hasterok, R., Marasek, A., Donnison, I.S., Armstead, I., Thomas, A., King, I.P., Wolny, E., Idziak, D., Draper, J., and, Jenkins, G., (2006) Alignment of the genomes of Brachypodium distachyon and temperate cereals and grasses using bacterial artificial chromosome landing with fluorescence in situ hybridization. Genetics, 173, 349-362.
17. Higgins, J.D., Perry, R.M., Barakate, A., Ramsay, L., Waugh, R., Halpin, C., Armstrong, S.J., and, Franklin, F.C., (2012) Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell, 24, 4096-4109.
18. Higgins, J.D., Osman, K., Jones, G.H., and, Franklin, F.C., (2014) Factors underlying restricted crossover localization in barley meiosis. Annu. Rev. Genet. 48, 29-47.
19. Holm, G., (1960) An inversion in barley. Hereditas, 46, 274-278.
20. Houben, A., Belyaev, N.D., Turner, B.M., and, Schubert, I., (1996) Differential immunostaining of plant chromosomes by antibodies recognizing acetylated histone H4 variants. Chromosome Res. 4, 191-194.
21. Houben, A., Demidov, D., Gernand, D., Meister, A., Leach, C.R., and, Schubert, I., (2003) Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J. 33, 967-973.
22. Houben, A., Schroeder-Reiter, E., Nagaki, K., Nasuda, S., Wanner, G., Murata, M., and, Endo, T.R., (2007) CENH3 interacts with the centromeric retrotransposon cereba and GC-rich satellites and locates to centromeric substructures in barley. Chromosoma, 116, 275-283.
23. Hudakova, S., Michalek, W., Presting, G.G., ten Hoopen, R., dos Santos, K., Jasencakova, Z., and, Schubert, I., (2001) Sequence organization of barley centromeres. Nucleic Acids Res. 29, 5029-5035.
24. International Barley Genome Sequencing Consortium, Mayer, K.F., Waugh, R., Brown, J.W., Schulman, A., Langridge, P., Platzer, M., Fincher, G.B., Muehlbauer, G.J., Sato, K., Close, T.J., Wise, R.P., and, Stein, N., (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature, 491, 711-716.
25. Jenuwein, T., (2001) Re-SET-ting heterochromatin by histone methyltransferases. Trends Cell Biol. 11, 266-273.
26. Jenuwein, T., and, Allis, C.D., (2001) Translating the histone code. Science, 293, 1074-1080.
27. Jia, Q., Zhang, J., Westcott, S., Zhang, X.Q., Bellgard, M., Lance, R., and, Li, C., (2009) GA-20 oxidase as a candidate for the semidwarf gene sdw1/denso in barley. Funct. Integr. Genomics 9, 255-262.
28. Jiang, J., Gill, B.S., Wang, G.L., Ronald, P.C., and, Ward, D.C., (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc. Natl Acad. Sci. USA, 92, 4487-4491.
29. de Jong, J.H., Fransz, P., and, Zabel, P., (1999) High resolution FISH in plants-techniques and applications. Trends Plant Sci. 4, 258-263.
30. Joshi, G.P., Nasuda, S., and, Endo, T.R., (2011) Dissection and cytological mapping of barley chromosome 2H in the genetic background of common wheat. Genes Genet. Syst. 86, 231-248.
31. Karafiátová, M., Bartos, J., Kopecky, D., Ma, L., Sato, K., Houben, A., Stein, N., and, Doležel, J., (2013) Mapping nonrecombining regions in barley using multicolor FISH. Chromosome Res. 21, 739-751.
32. Kato, A., Lamb, J.C., and, Birchler, J.A., (2004) Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc. Natl Acad. Sci. USA, 101, 13554-13559.
33. Kato, A., Albert, P.S., Vega, J.M., and, Birchler, J.A., (2006) Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech. Histochem. 81, 71-78.
34. Kim, J.S., Childs, K.L., Islam-Faridi, M.N., Menz, M.A., Klein, R.R., Klein, P.E., Price, H.J., Mullet, J.E., and, Stelly, D.M., (2002) Integrated karyotyping of sorghum by in situ hybridization of landed BACs. Genome, 45, 402-412.
35. Komatsuda, T., and, Mano, Y., (2002) Molecular mapping of the intermedium spike-c (int-c) and non-brittle rachis 1 (btr1) loci in barley (Hordeum vulgare L.). Theor. Appl. Genet. 105, 85-90.
36. Künzel, G., and, Waugh, R., (2002) Integration of microsatellite markers into the translocation-based physical RFLP map of barley chromosome 3H. Theor. Appl. Genet. 105, 660-665.
37. Künzel, G., Korzun, L., and, Meister, A., (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics, 154, 397-412.
38. Lamb, J.C., Danilova, T., Bauer, M.J., Meyer, J.M., Holland, J.J., Jensen, M.D., and, Birchler, J.A., (2007) Single-gene detection and karyotyping using small-target fluorescence in situ hybridization on maize somatic chromosomes. Genetics, 175, 1047-1058.
39. Litt, M.D., Simpson, M., Gaszner, M., Allis, C.D., and, Felsenfeld, G., (2001) Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science, 293, 2453-2455.
40. Lysák, M.A., Číhalíková, J., Kubaláková, M., Šimková, H., Künzel, G., and, Doležel, J., (1999) Flow karyotyping and sorting of mitotic chromosomes of barley (Hordeum vulgare L.). Chromosome Res. 7, 431-444.
41. Ma, L., Vu, G.T.H., Schubert, V., Watanabe, K., Stein, N., Houben, A., and, Schubert, I., (2010) Synteny between Brachypodium distachyon and Hordeum vulgare as revealed by FISH. Chromosome Res. 18, 841-850.
42. Marthe, F., and, Künzel, G., (1994) Localization of translocation breakpoints in somatic metaphase chromosomes of barley. Theor. Appl. Genet. 89, 240-248.
43. Mayer, K.F., Martis, M., Hedley, P.E., et al. (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell, 23, 1249-1263.
44. Miller, J.T., Dong, F., Jackson, S.A., Song, J., and, Jiang, J., (1998) Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics, 150, 1615-1623.
45. Nasuda, S., Kikkawa, Y., Ashida, T., Islam, A.K., Sato, K., and, Endo, T.R., (2005) Chromosomal assignment and deletion mapping of barley EST markers. Genes Genet. Syst. 80, 357-366.
46. Oliver, C., Pradillo, M., Corredor, E., and, Cunado, N., (2013) The dynamics of histone H3 modifications is species-specific in plant meiosis. Planta, 238, 23-33.
47. Plath, K., Fang, J., Mlynarczyk-Evans, S.K., Cao, R., Worringer, K.A., Wang, H., de la Cruz, C.C., Otte, A.P., Panning, B., and, Zhang, Y., (2003) Role of Histone H3 Lysine 27 Methylation in X Inactivation. Science, 300, 131-135.
48. Poland, J.A., Brown, P.J., Sorrells, M.E., and, Jannink, J.L., (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE, 7, e32253.
49. Poursarebani, N., Ariyadasa, R., Zhou, R., et al. (2013) Conserved synteny-based anchoring of the barley genome physical map. Funct. Integr. Genomics, 13, 339-350.
50. Qi, X., and, Lindhout, P., (1997) Development of AFLP markers in barley. Mol. Gen. Genet. 254, 330-336.
51. Rostoks, N., Park, Y.J., Ramakrishna, W., et al. (2002) Genomic sequencing reveals gene content, genomic organization, and recombination relationships in barley. Funct. Integr. Genomics, 2, 51-59.
52. Sakai, K., Nasuda, S., Sato, K., and, Endo, T.R., (2009) Dissection of barley chromosome 3H in common wheat and a comparison of 3H physical and genetic maps. Genes Genet. Syst. 84, 25-34.
53. Sakata, M., Nasuda, S., and, Endo, T.R., (2010) Dissection of barley chromosome 4H in common wheat by the gametocidal system and cytological mapping of chromosome 4H with EST markers. Genes Genet. Syst. 85, 19-29.
54. Sanei, M., Pickering, R., Kumke, K., Nasuda, S., and, Houben, A., (2011) Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc. Natl Acad. Sci. USA, 108, E498-E505.
55. Schmutzer, T., Ma, L., Pousarebani, N., Bull, F., Stein, N., Houben, A., and, Scholz, U., (2014) Kmasker-a tool for in silico prediction of single-copy FISH probes for the large-genome species Hordeum vulgare. Cytogenet. Genome Res. 142, 66-78.
56. Serizawa, N., Nasuda, S., Shi, F., Endo, T.R., Prodanovic, S., Schubert, I., and, Künzel, G., (2001) Deletion-based physical mapping of barley chromosome 7H. Theor. Appl. Genet. 103, 827-834.
57. Shearer, L.A., Anderson, L.K., de Jong, H., Smit, S., Goicoechea, J.L., Roe, B.A., Hua, A., Giovannoni, J.J., and, Stack, S.M., (2014) Fluorescence in situ hybridization and optical mapping to correct scaffold arrangement in the tomato genome. G3 (Bethesda), 4, 1395-1405.
58. Siedler, H., and, Graner, A., (1991) Construction of physical maps of the Hor1 locus of two barley cultivars by pulsed field gel electrophoresis. Mol. Gen. Genet. 226, 177-181.
59. Sorokin, A., Marthe, F., Houben, A., Pich, U., Graner, A., and, Künzel, G., (1994) Polymerase chain reaction mediated localization of RFLP clones to microisolated translocation chromosomes of barley. Genome, 37, 550-555.
60. Stein, N., Prasad, M., Scholz, U., et al. (2007) A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor. Appl. Genet. 114, 823-839.
61. Steuernagel, B., Taudien, S., Gundlach, H., et al. (2009) De novo 454 sequencing of barcoded BAC pools for comprehensive gene survey and genome analysis in the complex genome of barley. BMC Genom. 10, 547.
62. Stevison, L.S., Hoehn, K.B., and, Noor, M.A., (2011) Effects of inversions on within- and between-species recombination and divergence. Genome Biol. Evol. 3, 830-841.
63. Strahl, B.D., Ohba, R., Cook, R.G., and, Allis, C.D., (1999) Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc. Natl Acad. Sci. USA, 96, 14967-14972.
64. Suprunova, T., Krugman, T., Distelfeld, A., Fahima, T., Nevo, E., and, Korol, A., (2007) Identification of a novel gene (Hsdr4) involved in water-stress tolerance in wild barley. Plant Mol. Biol. 64, 17-34.
65. Szinay, D., Chang, S.B., Khrustaleva, L., Peters, S., Schijlen, E., Bai, Y., Stiekema, W.J., van Ham, R.C., de Jong, H., and, Klein Lankhorst, R.M., (2008) High-resolution chromosome mapping of BACs using multi-colour FISH and pooled-BAC FISH as a backbone for sequencing tomato chromosome 6. Plant J. 56, 627-637.
66. Tanksley, S.D., Ganal, M.W., Prince, J.P., et al. (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics, 132, 1141-1160.
67. Vrána, J., Kubaláková, M., Číhalíková, J., Valárik, M., and, Doležel, J., (2015) Preparation of sub-genomic fractions enriched for particular chromosomes in polyploid wheat. Biol. Plant. 59, 445-455.
68. Wang, M.L., Atkinson, M.D., Chinoy, C.N., Devos, K.M., and, Gale, M.D., (1992) Comparative Rflp-based genetic maps of barley chromosome-5 (1H) and rye chromosome-1R. Theor. Appl. Genet. 84, 339-344.
69. Wang, F., Stewart, J.M., and, Zhang, J., (2007) Molecular markers linked to the Rf2 fertility restorer gene in cotton. Genome, 50, 818-824.
70. Wicker, T., Krattinger, S.G., Lagudah, E.S., et al. (2009a) Analysis of intraspecies diversity in wheat and barley genomes identifies breakpoints of ancient haplotypes and provides insight into the structure of diploid and hexaploid Triticeae gene pools. Plant Physiol. 149, 258-270.
71. Wicker, T., Taudien, S., Houben, A., Keller, B., Graner, A., Platzer, M., and, Stein, N., (2009b) A whole-genome snapshot of 454 sequences exposes the composition of the barley genome and provides evidence for parallel evolution of genome size in wheat and barley. Plant J. 59, 712-722.
72. Yan, G., and, Chen, X., (2007) Molecular mapping of the rps1.a recessive gene for resistance to stripe rust in BBA 2890 barley. Phytopathology, 97, 668-673.
73. Yang, L., Koo, D.H., Li, Y., Zhang, X., Luan, F., Havey, M.J., Jiang, J., and, Weng, Y., (2012) Chromosome rearrangements during domestication of cucumber as revealed by high-density genetic mapping and draft genome assembly. Plant J. 71, 895-906.