Abstract
The small annual grass Brachypodium distachyon (Brachypodium) is rapidly emerging as a powerful model system to study questions unique to the grasses. Many Brachypodium resources have been developed including a whole genome sequence, highly efficient transformation and a large germplasm collection. We developed a genetic linkage map of Brachypodium using single nucleotide polymorphism (SNP) markers and an F2 mapping population of 476 individuals. SNPs were identified by targeted resequencing of single copy genomic sequences. Using the Illumina GoldenGate Genotyping platform we placed 558 markers into five linkage groups corresponding to the five chromosomes of Brachypodium. The unusually long total genetic map length, 1,598 centiMorgans (cM), indicates that the Brachypodium mapping population has a high recombination rate. By comparing the genetic map to genome features we found that the recombination rate was positively correlated with gene density and negatively correlated with repetitive regions and sites of ancestral chromosome fusions that retained centromeric repeat sequences. A comparison of adjacent genome regions with high versus low recombination rates revealed a positive correlation between interspecific synteny and recombination rate.
Similar content being viewed by others
Abbreviations
- BAC:
-
Bacterial artificial chromosome
- BES:
-
BAC end sequence
- Bp:
-
Base pair
- cM:
-
centiMorgans
- kb:
-
Kilobase
- LTR:
-
Long terminal repeat
- SNP:
-
Single nucleotide polymorphism
- OPA:
-
Oligo pool array
- UTR:
-
Untranslated region
References
Allerdings E, Ralph J, Steinhart H, Bunzel M (2006) Isolation and structural identification of complex feruloylated heteroxylan side-chains from maize bran. Phytochemistry 67(12):1276–1286
Anderson LK, Lai A, Stack SM, Rizzon C, Gaut BS (2006) Uneven distribution of expressed sequence tag loci on maize pachytene chromosomes. Genome Res 16(1):115
Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Blas AL, Yu Q, Chen C, Veatch O, Moore PH, Paull RE, Ming R (2009) Enrichment of a papaya high-density genetic map with AFLP markers. Genome 52(8):716
Bowers JE, Abbey C, Anderson S, Chang C, Draye X, Hoppe AH, Jessup R, Lemke C, Lennington J, Li Z, Lin YR, Liu SC, Luo L, Marler BS, Ming R, Mitchell SE, Qiang D, Reischmann K, Schulze SR, Skinner DN, Wang YW, Kresovich S, Schertz KF, Paterson AH (2003) A high-density genetic recombination map of sequence-tagged sites for Sorghum, as a framework for comparative structural and evolutionary genomics of tropical grains and grasses. Genetics 165(1):367
Bowers JE, Arias MA, Asher R, Avise JA, Ball RT, Brewer GA, Buss RW, Chen AH, Edwards TM, Estill JC, Exum HE, Goff VH, Herrick KL, Steele CLJ, Karunakaran S, Lafayette GK, Lemke C, Marler BS, Masters SL, McMillan JM, Nelson LK, Newsome GA, Nwakanma CC, Odeh RN, Phelps CA, Rarick EA, Rogers CJ, Ryan SP, Slaughter KA, Soderlund CA, Tang H, Wing RA, Paterson AH (2005) Comparative physical mapping links conservation of microsynteny to chromosome structure and recombination in grasses. Proc Natl Acad Sci USA 102(37):13206
Butler H, Ragoussis J (2008) BeadArray-Based genotyping. Methods Mol Biol 439:53–74
Chan EKF, Rowe HC, Kliebenstein DJ (2010) Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping. Genetics 185(3):991–1007. doi:10.1534/genetics.109.108522
Choi IY, Hyten DL, Matukumalli LK, Song Q, Chaky JM, Quigley CV, Chase K, Lark KG, Reiter RS, Yoon MS, Hwang EY, Yi SI, Young ND, Shoemaker RC, Van Tassell CP, Specht JE, Cregan PB (2007) A soybean transcript map: Gene distribution, haplotype and single-nucleotide polymorphism analysis. Genetics 176(1):685
Cogan NOI, Ponting RC, Vecchies AC, Drayton MC, George J, Dracatos PM, Dobrowolski MP, Sawbridge TI, Smith KF, Spangenberg GC, Forster JW (2006) Gene-associated single nucleotide polymorphism discovery in perennial ryegrass (Lolium perenne L.). Mol Genet Genomics 276(2):101
Draper J, Mur LAJ, Jenkins G, Ghosh-Biswas GC, Bablak P, Hasterok R, Routledge APM (2001) Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol 127(4):1539–1555
Drouaud J, Camilleri C, Bourguignon PY, Canaguier A, Berard A, Vezon D, Giancola S, Brunel D, Colot V, Prum B, Quesneville H, Mezard C (2006) Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination “hot spots”. Genome Res 16(1):106
Dubcovsky J, Luo MC, Zhong GY, Bransteitter R, Desai A, Kilian A, Kleinhofs A, Dvořák J (1996) Genetic map of diploid wheat, Triticum monococcum L., and its comparison with maps of Hordeum vulgare L. Genetics 143(2):983
Dvorak J, Yang ZL, You FM, Luo MC (2004) Deletion polymorphism in wheat chromosome regions with contrasting recombination rates. Genetics 168(3):1665
Feltus FA, Wan J, Schulze SR, Estill JC, Jiang N, Paterson AH (2004) An SNP resource for rice genetics and breeding based on subspecies indica and japonica genome alignments. Genome Res 14(9):1812–1819
Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X, Jia P, Zhang Y, Zhao Q, Ying K, Yu S, Tang Y, Weng Q, Zhang L, Lu Y, Mu J, Lu Y, Zhang LS, Yu Z, Fan D, Liu X, Lu T, Li C, Wu Y, Sun T, Lei H, Li T, Hu H, Guan J, Wu M, Zhang R, Zhou B, Chen Z, Chen L, Jin Z, Wang R, Yin H, Cai Z, Ren S, Lv G, Gu W, Zhu G, Tu Y, Jia J, Zhang Y, Chen J, Kang H, Chen X, Shao C, Sun Y, Hu Q, Zhang X, Zhang W, Wang L, Ding C, Sheng H, Gu J, Chen S, Ni L, Zhu F, Chen W, Lan L, Lai Y, Cheng Z, Gu M, Jiang J, Li J, Hong G, Xue Y, Han B (2002) Sequence and analysis of rice chromosome 4. Nature 420(6913):316
Garvin DF, Gu YQ, Hasterok R, Hazen SP, Jenkins G, Mockler TC, Mur LAJ, Vogel JP (2008) Development of genetic and genomic research resources for Brachypodium distachyon, a new model system for grass crop research. Crop Sci 48:S-69–S-84
Garvin DF, McKenzie N, Vogel JP, Mockler TC, Blankenheim ZJ, Wright J, Cheema JJS, Dicks J, Huo N, Hayden DM, Gu Y, Tobias C, Chang JH, Chu A, Trick M, Michael TP, Bevan MW, Snape JW (2010) An SSR-based genetic linkage map of the model grass Brachypodium distachyon. Genome 53(1):1–13
Groenen MAM, Wahlberg P, Foglio M, Cheng HH, Megens HJ, Crooijmans RPMA, Besnier F, Lathrop M, Muir WM, Wong GKS, Gut I, Andersson L (2009) A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Res 19(3):510
Gu YQ, Ma Y, Huo N, Vogel JP, You FM, Lazo GR, Nelson WM, Soderlund C, Dvorak J, Anderson OD, Luo MC (2009) A BAC-based physical map of Brachypodium distachyon and its comparative analysis with rice and wheat. BMC Genomics 10:496
Harushima Y, Yano M, Shomura A, Sato M, Shimano T, Kuboki Y, Yamamoto T, Lin SY, Antonio BA, Parco A, Kajiya H, Huang N, Yamamoto K, Nagamura Y, Kurata N, Khush GS, Sasaki T (1998) A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148(1):479
Hasterok R, Marasek A, Donnison IS, Armstead I, Thomas A, King IP, Wolny E, Idziak D, Draper J, 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(1):349–362
Huo N, Gu Y, Lazo G, Vogel J, Coleman-Derr D, Luo M, Thilmony R, Garvin D, Anderson O (2006) Construction and characterization of two BAC libraries from Brachypodium distachyon, a new model for grass genomics. Genome 49:1099–1108
Huo N, Lazo GR, Vogel JP, You FM, Ma Y, Hayden DM, Coleman-Derr D, Hill TA, Dvorak J, Anderson OD, Luo M-C, Gu YQ (2008) The nuclear genome of Brachypodium distachyon: analysis of BAC end sequences. Funct Integr Genomics 8(2):135–147
Huo N, Vogel JP, Lazo GR, You FM, Ma Y, McMahon S, Dvorak J, Anderson OD, Luo MC, Gu YQ (2009) Structural characterization of Brachypodium genome and its syntenic relationship with rice and wheat. Plant Mol Biol 70(1–2):47
International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Jensen-Seaman MI, Furey TS, Payseur BA, Lu Y, Roskin KM, Chen CF, Thomas MA, Haussler D, Jacob HJ (2004) Comparative recombination rates in the rat, mouse, and human genomes. Genome Res 14(4):528
Kim S, Plagnol V, Hu TT, Toomajian C, Clark RM, Ossowski S, Ecker JR, Weigel D, Nordborg M (2007) Recombination and linkage disequilibrium in Arabidopsis thaliana. Nat Genet 39(9):1151–1155
Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Lister C, Dean C (1993) Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J 4:745–750
Luo MC, Deal KR, Akhunov ED, Akhunova AR, Anderson OD, Anderson JA, Blake N, Clegg MT, Coleman-Derr D, Conley EJ, Crossman CC, Dubcovsky J, Gill BS, Gu YQ, Hadam J, Heo HY, Huo N, Lazo G, Ma Y, Matthews DE, McGuire PE, Morrell PL, Qualset CO, Renfro J, Tabanao D, Talbert LE, Tian C, Toleno DM, Warburton ML, You FM, Zhang W, Dvorak J (2009) Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae. Proc Natl Acad Sci USA 106(37):15780
Mace ES, Rami JF, Bouchet S, Klein PE, Klein RR, Kilian A, Wenzl P, Xia L, Halloran K, Jordan DR (2009) A consensus genetic map of sorghum that integrates multiple component maps and high-throughput Diversity Array Technology (DArT) markers. BMC Plant Biol 9
Myers S, Bottolo L, Freeman C, McVean G, Donnelly P (2005) Genetics: a fine-scale map of recombination rates and hotspots across the human genome. Science 310(5746):321–324
Nasu S, Suzuki J, Ohta R, Hasegawa K, Yui R, Kitazawa N, Monna L, Minobe Y (2002) Search for and analysis of single nucleotide polymorphisms (SNPS) in rice (Oryza sativa, Oryza rufipogon) and establishment of SNP markers. DNA Res 9(5):163–171
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob Ur R, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556
Ponting RC, Drayton MC, Cogan NOI, Dobrowolski MP, Spangenberg GC, Smith KF, Forster JW (2007) SNP discovery, validation, haplotype structure and linkage disequilibrium in full-length herbage nutritive quality genes of perennial ryegrass (Lolium perenne L.). Mol Genet Genomics 278(5):585–597
Sharp PJ, Kreis M, Shewry PR, Gale MD (1988) Location of β-amylase sequence in wheat and its relatives. Theor Appl Genet 75:286–290
Tian Z, Rizzon C, Du J, Zhu L, Bennetzen JL, Jackson SA, Gaut BS, Ma J (2009) Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res 19(12):2221–2230
Vain P, Worland B, Thole V, McKenzie N, Alves SC, Opanowicz M, Fish LJ, Bevan MW, Snape JW (2008) Agrobacterium-mediated transformation of the temperate grass Brachypodium distachyon (genotype Bd21) for T-DNA insertional mutagenesis. Plant Biotechnol J 6:236–245
Van Ooijen JW (2006) JoinMap®4, software for the calculation of genetic linkage maps in experimental population. Kyazma B.V., Wageningen, the Netherlands
Vogel JP, Bragg JN (2009) Brachypodium distachyon, a new model for the Triticeae. In: Feuillet C, Muehlbauer G (eds) Genetics and genomics of the Triticeae, vol 7. Plant genetics and genomics: crops and models. Springer, New York, pp 427–449
Vogel J, Hill T (2008) High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep 27(3):471–478
Vogel J, Gu Y, Twigg P, Lazo G, Laudencia-Chingcuanco D, Hayden D, Donze T, Vivian L, Stamova B, Coleman-Derr D (2006) EST sequencing and phylogenetic analysis of the model grass Brachypodium distachyon. Theor Appl Genet 113:186–195
Vogel JP, Tuna M, Budak H, Huo N, Gu YQ, Steinwand MA (2009) Development of SSR markers and analysis of diversity in Turkish populations of Brachypodium distachyon. BMC Plant Biology 9:Art. No.: 88
Wright SI, Agrawal N, Bureau TE (2003) Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res 13(8):1897–1903
Wu J, Mizuno H, Hayashi-Tsugane M, Ito Y, Chiden Y, Fujisawa M, Katagiri S, Saji S, Yoshiki S, Karasawa W, Yoshihara R, Hayashi A, Kobayashi H, Ito K, Hamada M, Okamoto M, Ikeno M, Ichikawa Y, Katayose Y, Yano M, Matsumoto T, Sasaki T (2003) Physical maps and recombination frequency of six rice chromosomes. Plant J 36(5):720–730
You FM, Huo N, Gu YQ, Luo MC, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinform 9:253
Acknowledgments
We would like to thank Haiming Xu (Zhejiang University) for QGA station analysis, Alan Schulman for LTR locations, and Edward Buckler for suggestions on presenting cumulative features (Fig. 4). This work was funded by an NSF 06-555 Plant Genome Research program grant and by USDA CRIS projects 5325-21000-013-00 and 3640-21000-021-00D.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Schulman.
Electronic supplementary material
Below is the link to the electronic supplementary material.
122_2011_1598_MOESM1_ESM.xls
Online Resource 1: This file contains an excel spreadsheet with all the SNPs identified, their flanking sequence and their designability rank score used to predict their performance in the Illumina GoldeGate genotyping system. (XLS 748 kb)
122_2011_1598_MOESM3_ESM.xls
Online Resource 3: This file contains an excel spreadsheet with all the mapped SNP markers, genomic coordinates, genetic distance, SNP score and marker sequence. (XLS 178 kb)
122_2011_1598_MOESM4_ESM.xls
Online Resource 4: This file contains an excel spreadsheet with all the genomic features for the paired low and high recombination intervals. (XLS 38 kb)
Rights and permissions
About this article
Cite this article
Huo, N., Garvin, D.F., You, F.M. et al. Comparison of a high-density genetic linkage map to genome features in the model grass Brachypodium distachyon . Theor Appl Genet 123, 455–464 (2011). https://doi.org/10.1007/s00122-011-1598-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-011-1598-4