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Theoretical and Applied Genetics

, Volume 127, Issue 9, pp 1975–1989 | Cite as

Comparative analysis of the radish genome based on a conserved ortholog set (COS) of Brassica

  • Young-Min Jeong
  • Won-Hyong Chung
  • Hee Chung
  • Namshin Kim
  • Beom-Seok Park
  • Ki-Byung Lim
  • Hee-Ju YuEmail author
  • Jeong-Hwan MunEmail author
Original Paper

Abstract

Key message

This manuscript provides a Brassica conserved ortholog set (COS) that can be used as diagnostic cross-species markers as well as tools for genetic mapping and genome comparison of the Brassicaceae.

Abstract

A conserved ortholog set (COS) is a collection of genes that are conserved in both sequence and copy number between closely related genomes. COS is a useful resource for developing gene-based markers and is suitable for comparative genome mapping. We developed a COS for Brassica based on proteome comparisons of Arabidopsis thaliana, B. rapa, and B. oleracea to establish a basis for comparative genome analysis of crop species in the Brassicaceae. A total of 1,194 conserved orthologous single-copy genes were identified from the genomes based on whole-genome BLASTP analysis. Gene ontology analysis showed that most of them encoded proteins with unknown function and chloroplast-related genes were enriched. In addition, 152 Brassica COS primer sets were applied to 16 crop and wild species of the Brassicaceae and 57.9–92.8 % of them were successfully amplified across the species representing that a Brassica COS can be used as diagnostic cross-species markers of diverse Brassica species. We constructed a genetic map of Raphanus sativus by analyzing the segregation of 322 COS genes in an F2 population (93 individuals) of Korean cultivars (WK10039 × WK10024). Comparative genome analysis based on the COS genes showed conserved genome structures between R. sativus and B. rapa with lineage-specific rearrangement and fractionation of triplicated subgenome blocks indicating close evolutionary relationship and differentiation of the genomes. The Brassica COS developed in this study will play an important role in genetic, genomic, and breeding studies of crop Brassicaceae species.

Keywords

Brassica Species Restriction Fragment Length Polymorphism Marker Ancestral Karyotype Polyploidy Event Comparative Genome Mapping 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by grants from the Next-Generation Biogreen21 program (PJ008019), Rural Development Administration, Korea to HJY and 2013 Research Fund of Myongji University to JHM. We thank Dr. Shengyi Liu (Oil Crops Research Institute of CAAS, China) for kindly providing sequence information of Brassica oleracea, Sin-Gi Park (National Academy of Agricultural Science of RDA, Korea) for bioinformatics support, and Dr. Suhyoung Park (National Institute of Horticultural and Herbal Science of RDA, Korea) for providing plant material.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The authors declare that the experiments complied with current laws of the country in which they were performed.

Supplementary material

122_2014_2354_MOESM1_ESM.pptx (5.1 mb)
Supplementary material 1 (PPTX 5273 kb)
122_2014_2354_MOESM2_ESM.docx (51 kb)
Supplementary material 2 (DOCX 51 kb)

References

  1. Al-Shehbaz I, Beilstein M, Kellogg E (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Syst Evol 259:89–120CrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCentralPubMedCrossRefGoogle Scholar
  3. Arias T, Beilstein M, Tang M, McKain M, Pires J (2014) Diversification times among Brassica (Brassicaceae) crops suggest hybrid formation after 20 million years of divergence. Am J Bot 101:86–91PubMedCrossRefGoogle Scholar
  4. Beilstein M, Al-Shehbaz I, Kellogg E (2006) Brassicaceae phylogeny and trichome evolution. Am J Bot 93:607–619PubMedCrossRefGoogle Scholar
  5. Beilstein M, Nagalingum N, Clements M, Manchester S, Mathews S (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci USA 107:18724–18728PubMedCentralPubMedCrossRefGoogle Scholar
  6. Bushakra JM, Sargent DJ, Cabrera A, Crowhurst R, Girona EL, Velasco R, Symonds VV, Knaap E, Troggio M, Gardiner SE, Chagné D (2011) Rosaceae conserved orthologous set (RosCOS) markers as a tool to assess genome synteny between Malus and Fragaria. Tree Genet Genomes 8:643–658CrossRefGoogle Scholar
  7. Cabrera A, Kozik A, Howad W, Arus P, Iezzoni AF, van der Knaap E (2009) Development and bin mapping of a Rosaceae conserved ortholog set (COS) of markers. BMC Genom 10:562CrossRefGoogle Scholar
  8. Chapman MA, Chang J, Weisman D, Kesseli RV, Burke JM (2007) Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae). Theor Appl Genet 115:747–755PubMedCrossRefGoogle Scholar
  9. Cheng F, Wu J, Fang L, Wang X (2012) Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Front Plant Sci 3:198PubMedCentralPubMedGoogle Scholar
  10. Cheng F, Mandakova T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the Mesohexaploid Brassica rapa. Plant Cell 25:1541–1554PubMedCentralPubMedCrossRefGoogle Scholar
  11. Dassanayake M, Oh DH, Haas JS, Hernandez A, Hong H, Ali S, Yun DJ, Bressan RA, Zhu JK, Bohnert HJ, Cheeseman JM (2011) The genome of the extremophile crucifer Thellungiella parvula. Nat Genet 43:913–918PubMedCentralPubMedCrossRefGoogle Scholar
  12. Economic Research Service USDA (2008) Vegetables and melons outlook. http://www.ers.usda.gov/Publications/VGS/Tables/World.pdf
  13. Fulton TM, Van der Hoeven R, Eannetta NT, Tanksley SD (2002) Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467PubMedCentralPubMedCrossRefGoogle Scholar
  14. Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11:725–736PubMedGoogle Scholar
  15. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, Haberer G, Hollister JD, Ossowski S, Ottilar RP, Salamov AA, Schneeberger K, Spannagl M, Wang X, Yang L, Nasrallah ME, Bergelson J, Carrington JC, Gaut BS, Schmutz J, Mayer KF, Van de Peer Y, Grigoriev IV, Nordborg M, Weigel D, Guo YL (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43:476–481PubMedCentralPubMedCrossRefGoogle Scholar
  16. Huang S, Deng L, Guan M, Li J, Lu K, Wang H, Fu D, Mason A, Liu S, Hua W (2013) Identification of genome-wide single nucleotide polymorphisms in allopolyploid crop Brassica napus. BMC Genom 14:717CrossRefGoogle Scholar
  17. Kim B, Yu H, Park S, Shin J, Oh M, Kim N, Mun J (2012) Identification and profiling of novel microRNAs in the Brassica rapa genome based on small RNA deep sequencing. BMC Plant Biol 12:218PubMedCentralPubMedCrossRefGoogle Scholar
  18. Krutovsky KV, Troggio M, Brown GR, Jermstad KD, Neale DB (2004) Comparative mapping in the Pinaceae. Genetics 168:447–461PubMedCentralPubMedCrossRefGoogle Scholar
  19. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645PubMedCentralPubMedCrossRefGoogle Scholar
  20. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25PubMedCentralPubMedCrossRefGoogle Scholar
  21. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948PubMedCrossRefGoogle Scholar
  22. Li F, Hasegawa Y, Saito M, Shirasawa S, Fukushima A, Ito T, Fujii H, Kishitani S, Kitashiba H, Nishio T (2011) Extensive chromosome homoeology among Brassiceae species were revealed by comparative genetic mapping with high-density EST-based SNP markers in radish (Raphanus sativus L.). DNA Res 18:401–411PubMedCentralPubMedCrossRefGoogle Scholar
  23. Liewlaksaneeyanawin C, Zhuang J, Tang M, Farzaneh N, Lueng G, Cullis C, Findlay S, Ritland CE, Bohlmann J, Ritland K (2008) Identification of COS markers in the Pinaceae. Tree Genet Genomes 5:247–255CrossRefGoogle Scholar
  24. Lü N, Yamane K, Ohnishi O (2008) Genetic diversity of cultivated and wild radish and phylogenetic relationships among Raphanus and Brassica species revealed by the analysis of trnK/matK sequence. Breed Sci 58:15–22CrossRefGoogle Scholar
  25. Lysak M, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I (2006) Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci USA 103:5224–5229PubMedCentralPubMedCrossRefGoogle Scholar
  26. Mun J-H, Kwon S, Yang T, Seol Y, Jin M, Kim J, Lim M, Kim J, Baek S, Choi B, Yu H, Kim D, Kim N, Lim K, Lee S, Hahn J, Lim Y, Bancroft I, Park B (2009) Genome-wide comparative analysis of the Brassica rapa gene space reveals genome shrinkage and differential loss of duplicated genes after whole genome triplication. Genome Biol 10:R111PubMedCentralPubMedCrossRefGoogle Scholar
  27. Nelson MN, Parkin IA, Lydiate DJ (2011) The mosaic of ancestral karyotype blocks in the Sinapis alba L. genome. Genome 54:33–41PubMedCrossRefGoogle Scholar
  28. Panjabi P, Jagannath A, Bisht NC, Padmaja KL, Sharma S, Gupta V, Pradhan AK, Pental D (2008) Comparative mapping of Brassica juncea and Arabidopsis thaliana using intron polymorphism (IP) markers: homoeologous relationships, diversification and evolution of the A, B and C Brassica genomes. BMC Genom 9:113CrossRefGoogle Scholar
  29. Quraishi UM, Abrouk M, Bolot S, Pont C, Throude M, Guilhot N, Confolent C, Bortolini F, Praud S, Murigneux A, Charmet G, Salse J (2009) Genomics in cereals: from genome-wide conserved orthologous set (COS) sequences to candidate genes for trait dissection. Funct Integr Genomics 9:473–484PubMedCrossRefGoogle Scholar
  30. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  31. Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542PubMedCrossRefGoogle Scholar
  32. Shirasawa K, Oyama M, Hirakawa H, Sato S, Tabata S, Fujioka T, Kimizuka-Takagi C, Sasamoto S, Watanabe A, Kato M, Kishida Y, Kohara M, Takahashi C, Tsuruoka H, Wada T, Sakai T, Isobe S (2011) An EST-SSR linkage map of Raphanus sativus and comparative genomics of the Brassicaceae. DNA Res 18:221–232PubMedCentralPubMedCrossRefGoogle Scholar
  33. Slotte T, Hazzouri K, Ågren J, Koenig D, Maumus F, Guo Y, Steige K, Platts A, Escobar J, Newman L, Wang W, Mandáková T, Vello E, Smith L, Henz S, Steffen J, Takuno S, Brandvain Y, Coop G, Andolfatto P, Hu T, Blanchette M, Clark R, Quesneville H, Nordborg M, Gaut B, Lysak M, Jenkins J, Grimwood J, Chapman J, Prochnik S, Shu S, Rokhsar D, Schmutz J, Weigel D, Wright S (2013) The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat Genet 45:831–835PubMedCrossRefGoogle Scholar
  34. Song KM, Osborn TC, Williams PH (1988) Brassica taxonomy based on nuclear restriction fragment length polymorphisms (RFLPs): 2. Preliminary analysis of subspecies within B. rapa (syn. campestris) and B. oleracea. Theor Appl Genet 76:593–600PubMedGoogle Scholar
  35. Song K, Osborn TC, Williams PH (1990) Brassica taxonomy based on nuclear restriction fragment length polymorphisms (RFLPs): 3. Genome relationships in Brassica and related genera and the origin of B. oleracea and B. rapa (syn. campestris). Theor Appl Genet 79:497–506PubMedGoogle Scholar
  36. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815Google Scholar
  37. The Brassica rapa Genome Sequencing Project Consortium (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039Google Scholar
  38. Thormann CE, Ferreira ME, Camargo LE, Tivang JG, Osborn TC (1994) Comparison of RFLP and RAPD markers to estimating genetic relationships within and among cruciferous species. Theor Appl Genet 88:973–980PubMedGoogle Scholar
  39. Timms L, Jimenez R, Chase M, Lavelle D, McHale L, Kozik A, Lai Z, Heesacker A, Knapp S, Rieseberg L, Michelmore R, Kesseli R (2006) Analyses of synteny between Arabidopsis thaliana and species in the Asteraceae reveal a complex network of small syntenic segments and major chromosomal rearrangements. Genetics 173:2227–2235PubMedCentralPubMedCrossRefGoogle Scholar
  40. van Ooijen JW (2006) JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B. V, WageningenGoogle Scholar
  41. Warwick S, Black L (1991) Molecular systematics of Brassica and allied genera (Subtribe Brassicinae, Brassiceae)—chloroplast genome and cytodeme congruence. Theor Appl Genet 82:81–92PubMedGoogle Scholar
  42. Warwick S, Black L (1997) Phylogenetic implications of chloroplast DNA restriction site variation in subtribes Raphaninae and Cakilinae (Brassicaceae, tribe Brassiceae). Canadian J Bot 75:960–973CrossRefGoogle Scholar
  43. 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 174:1407–1420PubMedCentralPubMedCrossRefGoogle Scholar
  44. Wu F, Eannetta NT, Xu Y, Durrett R, Mazourek M, Jahn MM, Tanksley SD (2009a) A COSII genetic map of the pepper genome provides a detailed picture of synteny with tomato and new insights into recent chromosome evolution in the genus Capsicum. Theor Appl Genet 118:1279–1293PubMedCrossRefGoogle Scholar
  45. Wu F, Eannetta NT, Xu Y, Tanksley SD (2009b) A detailed synteny map of the eggplant genome based on conserved ortholog set II (COSII) markers. Theor Appl Genet 118:927–935PubMedCrossRefGoogle Scholar
  46. Wu F, Eannetta NT, Xu Y, Plieske J, Ganal M, Pozzi C, Bakaher N, Tanksley SD (2010) COSII genetic maps of two diploid Nicotiana species provide a detailed picture of synteny with tomato and insights into chromosome evolution in tetraploid N. tabacum. Theor Appl Genet 120:809–827PubMedCrossRefGoogle Scholar
  47. Wu HJ, Zhang Z, Wang JY, Oh DH, Dassanayake M, Liu B, Huang Q, Sun HX, Xia R, Wu Y, Wang YN, Yang Z, Liu Y, Zhang W, Zhang H, Chu J, Yan C, Fang S, Zhang J, Wang Y, Zhang F, Wang G, Lee SY, Cheeseman JM, Yang B, Li B, Min J, Yang L, Wang J, Chu C, Chen SY, Bohnert HJ, Zhu JK, Wang XJ, Xie Q (2012) Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc Natl Acad Sci USA 109:12219–12224PubMedCentralPubMedCrossRefGoogle Scholar
  48. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591PubMedCrossRefGoogle Scholar
  49. Yang YW, Lai KN, Tai PY, Ma DP, Li WH (1999) Molecular phylogenetic studies of Brassica, Rrippa, Arabidopsis and allied genera based on the internal transcribed spacer region of 18S–25S rDNA. Mol Phylogenet Evol 13:455–462PubMedCrossRefGoogle Scholar
  50. Yang YW, Tai PY, Chen Y, Li WH (2002) A study of the phylogeny of Brassica rapa, B. nigra, Raphanus sativus, and their related genera using noncoding regions of chloroplast DNA. Mol Phylogene Evol 23:268–275CrossRefGoogle Scholar
  51. Yang R, Jarvis DE, Chen H, Beilstein MA, Grimwood J, Jenkins J, Shu S, Prochnik S, Xin M, Ma C, Schmutz J, Wing RA, Mitchell-Olds T, Schumaker KS, Wang X (2013) The reference genome of the halophytic plant Eutrema salsugineum. Front Plant Sci 4:46PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Young-Min Jeong
    • 1
  • Won-Hyong Chung
    • 2
  • Hee Chung
    • 1
  • Namshin Kim
    • 2
  • Beom-Seok Park
    • 3
  • Ki-Byung Lim
    • 4
  • Hee-Ju Yu
    • 1
    Email author
  • Jeong-Hwan Mun
    • 5
    Email author
  1. 1.Department of Life ScienceThe Catholic University of KoreaBucheonKorea
  2. 2.Korean Bioinformation CenterKorea Research Institute of Bioscience and BiotechnologyDaejonKorea
  3. 3.The Agricultural Genome CenterNational Academy of Agricultural Science Rural Development AdministrationSuwonKorea
  4. 4.Department of Horticultural ScienceKyungpook National UniversityDaeguKorea
  5. 5.Department of Bioscience and BioinformaticsMyongji UniversityYonginKorea

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