SpringerLink
Log in

Identification of candidate domestication regions in the radish genome based on high-depth resequencing analysis of 17 genotypes

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

This study provides high-quality variation data of diverse radish genotypes. Genome-wide SNP comparison along with RNA-seq analysis identified candidate genes related to domestication that have potential as trait-related markers for genetics and breeding of radish.

Abstract

Radish (Raphanus sativus L.) is an annual root vegetable crop that also encompasses diverse wild species. Radish has a long history of domestication, but the origins and selective sweep of cultivated radishes remain controversial. Here, we present comprehensive whole-genome resequencing analysis of radish to explore genomic variation between the radish genotypes and to identify genetic bottlenecks due to domestication in Asian cultivars. High-depth resequencing and multi-sample genoty** analysis of ten cultivated and seven wild accessions obtained 4.0 million high-quality homozygous single-nucleotide polymorphisms (SNPs)/insertions or deletions. Variation analysis revealed that Asian cultivated radish types are closely related to wild Asian accessions, but are distinct from European/American cultivated radishes, supporting the notion that Asian cultivars were domesticated from wild Asian genotypes. SNP comparison between Asian genotypes identified 153 candidate domestication regions (CDRs) containing 512 genes. Network analysis of the genes in CDRs functioning in plant signaling pathways and biochemical processes identified group of genes related to root architecture, cell wall, sugar metabolism, and glucosinolate biosynthesis. Expression profiling of the genes during root development suggested that domestication-related selective advantages included a main taproot with few branched lateral roots, reduced cell wall rigidity and favorable taste. Overall, this study provides evolutionary insights into domestication-related genetic selection in radish as well as identification of gene candidates with the potential to act as trait-related markers for background selection of elite lines in molecular breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abbo S, Pinhasi van-Oss R, Gopher A, Saranga Y, Ofner I, Peleg Z (2014) Plant domestication versus crop evolution: a conceptual framework for cereals and grain legumes. Trends Plant Sci 19:351–360

    Article  CAS  PubMed  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baute G, Kane N, Grassa C, Lai Z, Rieseberg L (2015) Genome scans reveal candidate domestication and improvement genes in cultivated sunflower, as well as post-domestication introgression with wild relatives. New Phytol 206:830–838

    Article  CAS  PubMed  Google Scholar 

  • Becker B (1962) Rettich und Radies. Handb Pflanzenzücht 6:23–78

    Google Scholar 

  • Browning S, Browning B (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084–1097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruex A, Kainkaryam R, Wieckowski Y, Kang Y, Bernhardt C, **a Y, Zheng X, Wang J, Lee M, Benfey P, Woolf P, Schiefelbein J (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet 8:e1002446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bus A, Hecht J, Huettel B, Reinhardt R, Stich B (2012) High-throughput polymorphism detection and genoty** in Brassica napus using next-generation RAD sequencing. BMC Genom 13:281

    Article  CAS  Google Scholar 

  • Cao K, Zheng Z, Wang L, Liu X, Zhu G, Fang W, Cheng S, Zeng P, Chen C, Wang X, **e M, Zhong X, Wang X, Zhao P, Bian C, Zhu Y, Zhang J, Ma G, Chen C, Li Y, Hao F, Li Y, Huang G, Li Y, Li H, Guo J, Xu X, Wang J (2014) Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol 15:415

    PubMed  PubMed Central  Google Scholar 

  • Chen H, Patterson N, Reich D (2010) Population differentiation as a test for selective sweeps. Genome Res 20:393–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung W-H, Jeong N, Kim J, Lee W, Lee Y-G, Lee S-H, Yoon W, Kim J-H, Choi I-Y, Choi H-K, Moon J-K, Kim N, Jeong S-C (2014) Population structure and domestication revealed by high-depth resequencing of Korean cultivated and wild soybean genomes. DNA Res 21:153–167

    Article  CAS  PubMed  Google Scholar 

  • Cingolani P, Platts A, Wang IL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6:80–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellstrand N, Marshall D (1985) The impact of domestication on distribution of allozyme variation within and among cultivars of radish, Raphanus sativus L. Theor Appl Genet 69:393–398

    Article  CAS  PubMed  Google Scholar 

  • Firon N, LaBonte D, Villordon A, Kfir Y, Solis J, Lapis E, Perlman T, Doron-Faigenboim A, Hetzroni A, Althan L, Nadir L (2013) Transcriptional profiling of sweet potato (Ipomoea batatas) roots indicates down-regulation of lignin biosynthesis and up-regulation of starch biosynthesis at an early stage of storage root formation. BMC Genom 14:460

    Article  CAS  Google Scholar 

  • George R, Evans D (1981) A classification of winter radish cultivars. Euphytica 30:483–492

    Article  Google Scholar 

  • Guevara D, El-Kereamy A, Yaish M, Mei-Bi Y, Rothstein S (2014) Functional characterization of the rice UDP-glucose 4-epimerase 1, OsUGE1: a potential role in cell wall carbohydrate partitioning during limiting nitrogen conditions. PLoS One 9:e96158

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Zhong R, Wr Morrison, Ye Z (2003) The Arabidopsis RHD3 gene is required for cell wall biosynthesis and actin organization. Planta 217:912–921

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Lu T, Han B (2013) Resequencing rice genomes: an emerging new era of rice genomics. Trends Genet 29:225–232

    Article  PubMed  Google Scholar 

  • Hufford M, Xu X, van Heerwaarden J, Pyhäjärvi T, Chia J, Cartwright R, Elshire R, Glaubitz J, Guill K, Kaeppler S, Lai J, Morrell P, Shannon L, Song C, Springer N, Swanson-Wagner R, Tiffin P, Wang J, Zhang G, Doebley J, McMullen M, Ware D, Buckler E, Yang S, Ross-Ibarra J (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 44:808–811

    Article  CAS  PubMed  Google Scholar 

  • Iorizzo M, Senalik D, Ellison S, Grzebelus D, Cavagnaro P, Allender C, Brunet J, Spooner D, Van Deynze A, Simon P (2013) Genetic structure and domestication of carrot (Daucus carota subsp. sativus) (Apiaceae). Am J Bot 100:930–938

    Article  PubMed  Google Scholar 

  • Jang G, Lee J, Rastogi K, Park S, Oh S, Lee J (2015) Cytokinin-dependent secondary growth determines root biomass in radish (Raphanus sativus L.). J Exp Bot 66:4607–4619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong Y-M, Kim N, Ahn B, Oh M, Chung W-H, Chung H, Jeong S, Lim K-B, Hwang Y-J, Kim G-B, Baek S, Choi S-B, Hyung D-J, Lee S-W, Sohn S-H, Kwon S-J, ** M, Seol Y-J, Chae W, Choi K, Park B-S, Yu H-J, Mun J-H (2016) Elucidating the triplicated ancestral genome structure of radish based on chromosome-level comparison with the Brassica genomes. Theor Appl Genet 129:1357–1372

    Article  CAS  PubMed  Google Scholar 

  • Kaneko Y, Matsuzawa Y (1993) Radish (Raphanus sativus L.). Pergamon Press Ltd., Oxford

    Google Scholar 

  • Kerk N, Ceserani T, Tausta S, Sussex I, Nelson T (2003) Laser capture microdissection of cells from plant tissues. Plant Physiol 132:27–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitashiba H, Li F, Hirakawa H, Kawanabe T, Zou Z, Hasegawa Y, Tonosaki K, Shirasawa S, Fukushima A, Yokoi S, Takahata Y, Kakizaki T, Ishida M, Okamoto S, Sakamoto K, Shirasawa K, Tabata S, Nishio T (2014) Draft sequences of the radish (Raphanus sativus L.) genome. DNA Res 21:481–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloosterman B, Vorst O, Hall R, Visser R, Bachem C (2005) Tuber on a chip: differential gene expression during potato tuber development. Plant Biotechnol J 3:505–519

    Article  CAS  PubMed  Google Scholar 

  • Kopta T, Pokluda R (2013) Yields, quality and nutritional parameters of radish (Raphanus sativus) cultivars when grown in organically in Czech Republic. Hort Sci 40:16–21

    CAS  Google Scholar 

  • Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Zeng R, Liao H (2016) Improving crop nutrient efficiency through root architecture modifications. J Integr Plant Biol 58:193–202

    Article  PubMed  Google Scholar 

  • Maldonado Dos Santos J, Valliyodan B, Joshi T, Khan S, Liu Y, Wang J, Vuong T, Oliveira M, Marcelino-Guimarães F, Xu D, Nguyen H, Abdelnoor R (2016) Evaluation of genetic variation among Brazilian soybean cultivars through genome resequencing. BMC Genom 17:110

    Article  Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo M (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsui Y, Shimomura M, Komatsu K, Namiki N, Shibata-Hatta M, Imai M, Katayose Y, Mukai Y, Kanamori H, Kurita K, Kagami T, Wakatsuki A, Ohyanagi H, Ikawa H, Minaka N, Nakagawa K, Shiwa Y, Sasaki T (2015) The radish genome and comprehensive gene expression profile of tuberous root formation and development. Sci Rep 5:10835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moghe G, Hufnagel D, Tang H, **ao Y, Dworkin I, Town C, Conner J, Shiu S (2014) Consequences of whole-genome triplication as revealed by comparative genomic analyses of the wild radish Raphanus raphanistrum and three other Brassicaceae species. Plant Cell 26:1925–1937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mun J-H, Chung H, Chung W-H, Oh M, Jeong Y-M, Kim N, Ahn B, Park B-S, Park S, Lim K-B, Hwang Y-J, Yu H-J (2015) Construction of a reference genetic map of Raphanus sativus based on genoty** by whole-genome resequencing. Theor Appl Genet 128:259–272

    Article  CAS  PubMed  Google Scholar 

  • Olsen K, Wendel J (2013) A bountiful harvest: genomic insights into crop domestication phenotypes. Annu Rev Plant Biol 64:47–70

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Park S, Yu H-J, Mun J-H, Lee S (2010) Genome-wide discovery of DNA polymorphism in Brassica rapa. Mol Genet Genomics 283:135–145

    Article  CAS  PubMed  Google Scholar 

  • Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540

    Article  CAS  PubMed  Google Scholar 

  • Patel R, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ralph P, Coop G (2010) Parallel adaptation: one or many waves of advance of an advantageous allele? Genetics 186:647–668

    Article  PubMed  PubMed Central  Google Scholar 

  • Remans T, Nacry P, Pervent M, Girin T, Tillard P, Lepetit M, Gojon A (2006) A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol 140:909–921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rong J, Lammers Y, Strasburg J, Schidlo N, Ariyurek Y, de Jong T, Klinkhamer P, Smulders M, Vrieling K (2014) New insights into domestication of carrot from root transcriptome analyses. BMC Genom 15:895

    Article  Google Scholar 

  • Rouhier H, Usuda H (2001) Spatial and temporal distribution of sucrose synthase in the radish hypocotyl in relation to thickening growth. Plant Cell Physiol 42:583–593

    Article  CAS  PubMed  Google Scholar 

  • Ruzin S (1999) Plant microtechnique and microscopy. Oxford University Press, New York

    Google Scholar 

  • Seifert G, Barber C, Wells B, Dolan L, Roberts K (2002) Galactose biosynthesis in Arabidopsis: genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers. Curr Biol 12:1840–1845

    Article  CAS  PubMed  Google Scholar 

  • Sergeeva L, Keurentjes J, Bentsink L, Vonk J, van der Plas L, Koornneef M, Vreugdenhil D (2006) Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. Proc Natl Acad Sci USA 103:2994–2999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sirju-Charran G, Wickham L (1988) The development of alternative storage sink sites in sweet potato Ipomoea batatas. Ann Bot 61:99–102

    Google Scholar 

  • Sturm A, Tang G (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407

    Article  PubMed  Google Scholar 

  • Sun P, **ao X, Duan L, Guo Y, Qi J, Liao D, Zhao C, Liu Y, Zhou L, Li X (2015) Dynamic transcriptional profiling provides insights into tuberous root development in Rehmannia glutinosa. Front Plant Sci 6:396

    PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ting F, Wren M (1980) Storage organ development in radish (Raphanus sativus L.). 1. A comparison of development in seedlings and rooted cuttings of two contrasting varieties. Ann Bot 46:267–276

    Google Scholar 

  • Usuda H, Demura T, Shimogawara K, Fukuda H (1999) Development of sink capacity of the “storage root” in a radish cultivar with a high ratio of “storage root” to shoot. Plant Cell Physiol 40:369–377

    Article  CAS  Google Scholar 

  • Warwick S (2011) Brassicaceae in Agriculture. In: Schmidt R, Bancroft I (eds) Genetics and Genomics of the Brassicaceae. Springer, Gatersleben, pp 33–66

    Chapter  Google Scholar 

  • Xu M, **e W, Huang M (2012a) Overexpression of PeRHD3 alters the root architecture in Populus. Biochem Biophys Res Commun 424:239–244

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Liu X, Ge S, Jensen J, Hu F, Li X, Dong Y, Gutenkunst R, Fang L, Huang L, Li J, He W, Zhang G, Zheng X, Zhang F, Li Y, Yu C, Kristiansen K, Zhang X, Wang J, Wright M, McCouch S, Nielsen R, Wang J, Wang W (2012b) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105–111

    Article  CAS  Google Scholar 

  • Yamagishi H (2004) Assessment of cytoplasmic polymorphisms by PCR-RFLP of the mitochondrial orfB region in wild and cultivated radishes (Raphanus). Plant Breed 123:141–144

    Article  CAS  Google Scholar 

  • Yamagishi H, Terachi T (2003) Multiple origins of cultivated radishes as evidenced by a comparison of the structural variations in mitochondrial DNA of Raphanus. Genome 46:89–94

    Article  CAS  PubMed  Google Scholar 

  • Yamane K, Lu N, Ohnishi O (2005) Chloroplast DNA variations of cultivated radish and its wild relatives. Plant Sci 168:627–634

    Article  CAS  Google Scholar 

  • Yamane K, Lu N, Ohnishi O (2009) Multiple origins and high genetic diversity of cultivated radish inferred from polymorphism in chloroplast simple sequence repeats. Breed Sci 59:55–65

    Article  CAS  Google Scholar 

  • Zheng D, Han X, An Y, Guo H, **a X, Yin W (2013) The nitrate transporter NRT2.1 functions in the ethylene response to nitrate deficiency in Arabidopsis. Plant Cell Environ 36:1328–1337

    Article  CAS  PubMed  Google Scholar 

  • Zhou Z, Jiang Y, Wang Z, Gou Z, Lyu J, Li W, Yu Y, Shu L, Zhao Y, Ma Y, Fang C, Shen Y, Liu T, Li C, Li Q, Wu M, Wang M, Wu Y, Dong Y, Wan W, Wang X, Ding Z, Gao Y, **ang H, Zhu B, Lee S, Wang W, Tian Z (2015) Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol 33:408–414

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Next-Generation Biogreen21 program (PJ01108601 to JHM and PJ01108602 to HJY) and the National Academy of Agricultural Science (PJ009795 to JHM), Rural Development Administration, Korea. We appreciate Genebank Information Center, RDA, Korea and National Institute of Agricultural Sciences, Japan for providing seeds of radish accessions.

Author information

Author notes

    Authors and Affiliations

    1. Epigenomics Research Center of Genome Institute, Daejeon, 34141, Korea

      Namshin Kim, Seongmun Jeong, Won-Jun Lim, Kyoung Hyoun Kim, Won Park & Jae-Yoon Kim

    2. Department of Life Science, The Catholic University of Korea, Bucheon, 14662, Korea

      Young-Min Jeong, Bomi Yim, Young Joon Lee & Hee-Ju Yu

    3. Department of Functional Genomics, Korea University of Science and Technology, Daejeon, 34141, Korea

      Namshin Kim, Won-Jun Lim, Kyoung Hyoun Kim, Won Park & Jae-Yoon Kim

    4. Department of Bioscience and Bioinformatics, Myongji University, Yongin, 17058, Korea

      Goon-Bo Kim, Seunghoon Baek, Young-Eun Kwon, Ara Cho, Sang-Bong Choi & Jeong-Hwan Mun

    5. Korean Bioinformation Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, 34141, Korea

      Jiwoong Kim

    6. Department of Genetic Engineering, Dong-A University, Busan, 49315, Korea

      **-Hyun Kim

    7. Breeding Research Institute, Dongbu Farm Hannong Co. Ltd., Ansung, 17503, Korea

      Byung-Moon Chun & Young-Pyo Lee

    8. Department of Genomics, National Academy of Agricultural Science, Rural Development Administration, Wanju, 54874, Korea

      Beom-Seok Park

    Authors
    1. Namshin Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Young-Min Jeong
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Seongmun Jeong
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Goon-Bo Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Seunghoon Baek
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Young-Eun Kwon
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Ara Cho
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Sang-Bong Choi
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Jiwoong Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Won-Jun Lim
      View author publications

      You can also search for this author in PubMed Google Scholar

    11. Kyoung Hyoun Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    12. Won Park
      View author publications

      You can also search for this author in PubMed Google Scholar

    13. Jae-Yoon Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    14. **-Hyun Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    15. Bomi Yim
      View author publications

      You can also search for this author in PubMed Google Scholar

    16. Young Joon Lee
      View author publications

      You can also search for this author in PubMed Google Scholar

    17. Byung-Moon Chun
      View author publications

      You can also search for this author in PubMed Google Scholar

    18. Young-Pyo Lee
      View author publications

      You can also search for this author in PubMed Google Scholar

    19. Beom-Seok Park
      View author publications

      You can also search for this author in PubMed Google Scholar

    20. Hee-Ju Yu
      View author publications

      You can also search for this author in PubMed Google Scholar

    21. Jeong-Hwan Mun
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Hee-Ju Yu or Jeong-Hwan Mun.

    Ethics declarations

    Ethical standards

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

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Additional information

    Communicated by I. AP Parkin.

    N. Kim and Y.-M. Jeong contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 2820 kb)

    Supplementary material 2 (DOCX 206 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Kim, N., Jeong, YM., Jeong, S. et al. Identification of candidate domestication regions in the radish genome based on high-depth resequencing analysis of 17 genotypes. Theor Appl Genet 129, 1797–1814 (2016). https://doi.org/10.1007/s00122-016-2741-z

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00122-016-2741-z

    Keywords

    Search

    Navigation