Abstract
PCR-based Landmark Unique Gene (PLUG) markers are EST-PCR markers developed based on the orthologous gene conservation between rice and wheat, and on the intron polymorphisms among the three orthologous genes derived from the A, B and D genomes of wheat. We designed a total of 960 primer sets from wheat ESTs that showed high similarity with 951 single-copy rice genes. When genomic DNA of Chinese Spring wheat was used as a template, 872 primer sets amplified one to five distinct products. Out of these 872 PLUG markers, 531 were assigned to one or more chromosomes by nullisomic-tetrasomic analysis. For each wheat chromosome, the number of loci detected ranged from 32 for chromosome 6A to 73 for chromosome 7D, with an average of 48 loci per chromosome. Several novel synteny perturbations were identified using deletion bin-mapping of markers. Furthermore, we demonstrated that PLUG markers can be used as probes to simultaneously identify BAC clones that contain homoeologous regions from all three genomes.
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Akhunov ED, Akhunova AR, Linkiewicz AM, Dubcovsky J, Hummel D, Lazo G, Chao S, Anderson OD, David J, Qi L, Echalier B, Gill BS, Miftahudin, Gustafson JP, La Rota M, Sorrells ME, Zhang D, Nguyen HT, Kalavacharla V, Hossain K, Kianian SF, Peng J, Lapitan NL, Wennerlind EJ, Nduati V, Anderson JA, Sidhu D, Gill KS, McGuire PE, Qualset CO, Dvorak J (2003) Synteny perturbations between wheat homoeologous chromosomes caused by locus duplications and deletions correlate with recombination rates. Proc Natl Acad Sci USA 100:10836–10841
Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733
Campanella JJ, Olajide AF, Magnus V, Ludwig-Muller J (2004) A novel auxin conjugate hydrolase from wheat with substrate specificity for longer side-chain auxin amide conjugates. Plant Physiol 135:2230–2240
Carollo V, Matthews DE, Lazo GR, Blake TK, Hummel DD, Lui N, Hane DL, Anderson OD (2005) GrainGenes 2.0. an improved resource for the small-grains community. Plant Physiol 139:643–651
Chantret N, Salse J, Sabot F, Bellec A, Laubin B, Dubois I, Dossat C, Sourdille P, Joudrier P, Gautier MF, Cattolico L, Beckert M, Aubourg S, Weissenbach J, Caboche M, Leroy P, Bernard M, Chalhoub B (2008) Contrasted microcolinearity and gene evolution within a homoeologous region of wheat and barley species. J Mol Evol 66:138–150
Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307
Faris JD, Fellers JP, Brooks SA, Gill BS (2003) A bacterial artificial chromosome contig spanning the major domestication locus Q in wheat and identification of a candidate gene. Genetics 164:311–321
Feldman M, Levy AA (2005) Allopolyploidy––a shaping force in the evolution of wheat genomes. Cytogenet Genome Res 109:250–258
Feltus FA, Singh HP, Lohithaswa HC, Schulze SR, Silva TD, Paterson AH (2006) A comparative genomics strategy for targeted discovery of single-nucleotide polymorphisms and conserved-noncoding sequences in orphan crops. Plant Physiol 140:1183–1191
Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc Natl Acad Sci USA 100:15253–15258
Florea L, Hartzell G, Zhang Z, Rubin GM, Miller W (1998) A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Res 8:967–974
Fredslund J, Madsen LH, Hougaard BK, Nielsen AM, Bertioli D, Sandal N, Stougaard J, Schauser L (2006) A general pipeline for the development of anchor markers for comparative genomics in plants. BMC Genomics 7:207
Fu D, Szucs P, Yan L, Helguera M, Skinner JS, von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletions within the first intron in VRN–1 are associated with spring growth habit in barley and wheat. Mol Genet Genomics 273:54–65
Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–1974
Gao S, Gu YQ, Wu J, Coleman-Derr D, Huo N, Crossman C, Jia J, Zuo Q, Ren Z, Anderson OD, Kong X (2007) Rapid evolution and complex structural organization in genomic regions harboring multiple prolamin genes in the polyploid wheat genome. Plant Mol Biol 65:189–203
Gu YQ, Salse J, Coleman-Derr D, Dupin A, Crossman C, Lazo GR, Huo N, Belcram H, Ravel C, Charmet G, Charles M, Anderson OD, Chalhoub B (2006) Types and rates of sequence evolution at the high-molecular-weight glutenin locus in hexaploid wheat and its ancestral genomes. Genetics 174:1493–1504
Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 31:5654–5666
Hossain KG, Kalavacharla V, Lazo GR, Hegstad J, Wentz MJ, Kianian PM, Simons K, Gehlhar S, Rust JL, Syamala RR, Obeori K, Bhamidimarri S, Karunadharma P, Chao S, Anderson OD, Qi LL, Echalier B, Gill BS, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Akhunov ED, Dvorak J, Miftahudin, Ross K, Gustafson JP, Radhawa HS, Dilbirligi M, Gill KS, Peng JH, Lapitan NL, Greene RA, Bermudez-Kandianis CE, Sorrells ME, Feril O, Pathan MS, Nguyen HT, Gonzalez-Hernandez JL, Conley EJ, Anderson JA, Choi DW, Fenton D, Close TJ, McGuire PE, Qualset CO, Kianian SF (2004) A chromosome bin map of 2148 expressed sequence tag loci of wheat homoeologous group 7. Genetics 168:687–699
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Ishikawa G, Yonemaru J, Saito M, Nakamura T (2007) PCR-based landmark unique gene (PLUG) markers effectively assign homoeologous wheat genes to A, B and D genomes. BMC Genomics 8:135
Itoh T, Tanaka T, Barrero RA, Yamasaki C, Fujii Y, Hilton PB, Antonio BA, Aono H, Apweiler R, Bruskiewich R, Bureau T, Burr F, Costa de Oliveira A, Fuks G, Habara T, Haberer G, Han B, Harada E, Hiraki AT, Hirochika H, Hoen D, Hokari H, Hosokawa S, Hsing YI, Ikawa H, Ikeo K, Imanishi T, Ito Y, Jaiswal P, Kanno M, Kawahara Y, Kawamura T, Kawashima H, Khurana JP, Kikuchi S, Komatsu S, Koyanagi KO, Kubooka H, Lieberherr D, Lin YC, Lonsdale D, Matsumoto T, Matsuya A, McCombie WR, Messing J, Miyao A, Mulder N, Nagamura Y, Nam J, Namiki N, Numa H, Nurimoto S, O’Donovan C, Ohyanagi H, Okido T, Oota S, Osato N, Palmer LE, Quetier F, Raghuvanshi S, Saichi N, Sakai H, Sakai Y, Sakata K, Sakurai T, Sato F, Sato Y, Schoof H, Seki M, Shibata M, Shimizu Y, Shinozaki K, Shinso Y, Singh NK, Smith-White B, Takeda J, Tanino M, Tatusova T, Thongjuea S, Todokoro F, Tsugane M, Tyagi AK, Vanavichit A, Wang A, Wing RA, Yamaguchi K, Yamamoto M, Yamamoto N, Yu Y, Zhang H, Zhao Q, Higo K, Burr B, Gojobori T, Sasaki T (2007) Curated genome annotation of Oryza sativa ssp. japonica and comparative genome analysis with Arabidopsis thaliana. Genome Res 17:175–183
La Rota M, Sorrells ME (2004) Comparative DNA sequence analysis of mapped wheat ESTs reveals the complexity of genome relationships between rice and wheat. Funct Integr Genomics 4:34–46
Marshall DR, Langridge P, Appels R (2001) Wheat breeding in the new century: applying molecular genetic analyses of key quality and agronomic traits. Aust J Agric Res 52:1043–1423
Nelson JC, Sorrells ME, Van Deynze AE, Lu YH, Atkinson M, Bernard M, Leroy P, Faris JD, Anderson JA (1995) Molecular mapping of wheat: major genes and rearrangements in homoeologous groups 4, 5, and 7. Genetics 141:721–731
Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217
Qi L, Echalier B, Friebe B, Gill BS (2003) Molecular characterization of a set of wheat deletion stocks for use in chromosome bin mapping of ESTs. Funct Integr Genomics 3:39–55
Salse J, Bolot S, Throude M, Jouffe V, Piegu B, Quraishi UM, Calcagno T, Cooke R, Delseny M, Feuillet C (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20:11–24
See DR, Brooks S, Nelson JC, Brown-Guedira G, Friebe B, Gill BS (2006) Gene evolution at the ends of wheat chromosomes. Proc Natl Acad Sci USA 103:4162–4167
Sorrells ME, La Rota M, Bermudez-Kandianis CE, Greene RA, Kantety R, Munkvold JD, Miftahudin, Mahmoud A, Ma X, Gustafson PJ, Qi LL, Echalier B, Gill BS, Matthews DE, Lazo GR, Chao S, Anderson OD, Edwards H, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dvorak J, Zhang D, Nguyen HT, Peng J, Lapitan NL, Gonzalez-Hernandez JL, Anderson JA, Hossain K, Kalavacharla V, Kianian SF, Choi DW, Close TJ, Dilbirligi M, Gill KS, Steber C, Walker-Simmons MK, McGuire PE, Qualset CO (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827
Stein N, Prasad M, Scholz U, Thiel T, Zhang H, Wolf M, Kota R, Varshney RK, Perovic D, Grosse I, Graner A (2007) A 1, 000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor Appl Genet 114:823–839
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Town CD, Cheung F, Maiti R, Crabtree J, Hass BJ, Wortman JR, Hine EE, Althoff R, Arbogast TS, Tallon LJ, Vigouroux M, Trick M, Bancroft I (2006) Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 18:1348–1359
Tsuchida M, Fukushima T, Nasuda S, Masoudi-Nejad A, Ishikawa G, Nakamura T, Endo TR (2008) Dissection of rye chromosome 1R in common wheat. Genes Genet Syst 83:43–53
Wei H, Fu Y, Arora R (2005) Intron-flanking EST-PCR markers: from genetic marker development to gene structure analysis in Rhododendron. Theor Appl Genet 111:1347–1356
Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Edgar R, Federhen S, Geer LY, Helmberg W, Kapustin Y, Kenton DL, Khovayko O, Lipman DJ, Madden TL, Maglott DR, Ostell J, Pruitt KD, Schuler GD, Schriml LM, Sequeira E, Sherry ST, Sirotkin K, Souvorov A, Starchenko G, Suzek TO, Tatusov R, Tatusova TA, Wagner L, Yaschenko E (2006) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 34:D173–D180
Wicker T, Yahiaoui N, Keller B (2007) Contrasting rates of evolution in Pm3 loci from three wheat species and rice. Genetics 177:1207–1216
Wu J, Maehara T, Shimokawa T, Yamamoto S, Harada C, Takazaki Y, Ono N, Mukai Y, Koike K, Yazaki J, Fujii F, Shomura A, Ando T, Kono I, Waki K, Yamamoto K, Yano M, Matsumoto T, Sasaki T (2002) A comprehensive rice transcript map containing 6591 expressed sequence tag sites. Plant Cell 14:525–535
Wu F, Mueller LA, Crouzillat D, Petiard V, Tanksley SD (2006) Combining bioinformatics and phylogenetics to identify large sets of single copy, orthologous genes (COSII) for comparative, evolutionary and systematic studies: A test case in the euasterid plant clade. Genetics 174:1407–1420
Yahiaoui N, Srichumpa P, Dudler R, Keller B (2004) Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J 37:528–538
Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268
Yuan Q, Ouyang S, Wang A, Zhu W, Maiti R, Lin H, Hamilton J, Haas B, Sultana R, Cheung F, Wortman J, Buell CR (2005) The institute for genomic research Osa1 rice genome annotation database. Plant Physiol 138:18–26
Acknowledgments
We thank Dr. Patricia Vrinten for helpful discussions and useful comments on the manuscript. We also thank Drs. Izumi Kono, Tsuyu Ando, Satoshi Katagiri and Wataru Karasawa at STAFF institute for performing the deletion-bin mapping and BAC clones screening, and Drs. Tsuyoshi Tanaka and Takeshi Itoh at National Institute of Agrobiological Sciences for establishing links among the RAP-DB and PLUG web sites. This work was partially supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Green Technology Project DM-1305).
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122_2008_916_MOESM1_ESM.xls
Supplementary material 1 PLUG primer sequences, wheat ESTs and rice genes, and summary of PCR and mapping results. In the ‘no. of products’ column, ‘m’ indicates the primer set amplified multiple non-specific products. S, H and T in the ‘detection’ column indicate that the product from the specific genome can be distinguished by size polymorphism of the PCR product, or of the HaeIII-digested or TaqI-digested product, respectively. Asterisks in the last columns indicate markers correspond to the probes used in the NSF deletion-bin mapping project (http://wheat.pw.usda.gov/NSF/). (XLS 289 kb)
122_2008_916_MOESM2_ESM.xls
Supplementary material 2 Aneuploid lines of Chinese Spring used in this study. The NBRP-Wheat strain ID designation is shown. Lines used in this study, and those used by Qi et al. (2003) are indicated, and updated FL values based on each study are given. (XLS 69 kb)
122_2008_916_MOESM3_ESM.pdf
Supplementary material 3 Gel-documentation for the nullisomic-tetrasomic analysis of the 154 PLUG markers used in deletion-bin mapping. Rose, yellow and blue asterisks in the photos indicate that the band is derived from the A, B or D genome, respectively. PCR products and restriction enzyme-digested PCR products were separated on 1% and 4% agarose gels, respectively. (PDF 4469 kb)
122_2008_916_MOESM4_ESM.pdf
Supplementary material 4 Comparative maps of wheat and rice orthologous chromosomes. Arrows beside the rice chromosomes indicate centromere positions. The C-banding patterns and deletion breakpoints of Chinese Spring chromosomes were taken from Endo and Gill (1996). (PDF 72 kb)
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Ishikawa, G., Nakamura, T., Ashida, T. et al. Localization of anchor loci representing five hundred annotated rice genes to wheat chromosomes using PLUG markers. Theor Appl Genet 118, 499–514 (2009). https://doi.org/10.1007/s00122-008-0916-y
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DOI: https://doi.org/10.1007/s00122-008-0916-y