Skip to main content
SpringerLink
Log in

Insights into the genetic relationships among plants of Beta section Beta using SNP markers

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

Abstract

Key message

Using a much higher number of SNP markers and larger sample sizes than all the previous studies, we characterized the genetic relationships among wild and cultivated plants of section Beta.

Abstract

We analyzed the genetic variation of Beta section Beta, which includes wild taxa (Beta macrocarpa, B. patula, B. vulgaris subsp. adanensis and B. vulgaris subsp. maritima) and cultivars (fodder beet, sugar beet, garden beet, leaf beet, and swiss chards), using 9724 single nucleotide polymorphism markers. The analyses conducted at the individual level without a priori groups confirmed the strong differentiation of B. macrocarpa and B. vulgaris subsp. adanensis from the other taxa. B. vulgaris subsp. maritima showed a complex genetic structure partly following a geographical pattern, which confounded the differences between this taxon and the cultivated varieties. Cultivated varieties were structured into three main groups: garden beets, fodder and sugar beets, and leaf beets and swiss chards. The genetic structure described here will be helpful to correctly estimate linkage disequilibrium and to test for statistical associations between genetic markers and environmental variables.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abe J, Tsuda C (1987) Genetic analysis for isozyme variation in the section Vulgares, genus Beta. Jpn J Breed 37:253–261

    Article  Google Scholar 

  • Abe J, Yoshikawa H, Tsuda C (1986) Reproductive barriers in sugar beet (Beta vulgaris) and its wild relatives of the section Vulgares, the genus Beta. J Fac Agric Hokkaido Univ Jpn 63:40–48

    Google Scholar 

  • Adetunji I, Willems G, Tschoep H et al (2014) Genetic diversity and linkage disequilibrium analysis in elite sugar beet breeding lines and wild beet accessions. Theor Appl Genet 127:559–571. doi:10.1007/s00122-013-2239-x

    Article  CAS  PubMed  Google Scholar 

  • Andrello M, Henry K, Devaux P et al (2016) Taxonomic, spatial and adaptive genetic variation of Beta section Beta. Theor Appl Genet 129:257–271. doi:10.1007/s00122-015-2625-7

    Article  CAS  PubMed  Google Scholar 

  • Arnaud J-F, Viard F, Delescluse M, Cuguen J (2003) Evidence for gene flow via seed dispersal from crop to wild relatives in Beta vulgaris (Chenopodiaceae): consequences for the release of genetically modified crop species with weedy lineages. Proc R Soc Lond B Biol Sci 270:1565–1571

    Article  Google Scholar 

  • Arnaud J-F, Fénart S, Godé C et al (2009) Fine-scale geographical structure of genetic diversity in inland wild beet populations. Mol Ecol 18:3201–3215. doi:10.1111/j.1365-294X.2009.04279.x

    Article  PubMed  Google Scholar 

  • Bauchet G, Munos S, Sauvage C et al (2014) Genes involved in floral meristem in tomato exhibit drastically reduced genetic diversity and signature of selection. BMC Plant Biol 14:1

    Article  Google Scholar 

  • Biancardi E, Panella LW, Lewellen RT (2012) Beta maritima. The origin of beets. Springer, New York

    Book  Google Scholar 

  • Bonavent J-F, Bessone L, Geny A et al (1989) A possible origin for the sugar beet cytoplasmic male sterility source Owen. Genome 32:322–327. doi:10.1139/g89-448

    Article  CAS  Google Scholar 

  • Buttler KP (1977) Variation in wild populations of annual beet (Beta, Chenopodiaceae). Plant Syst Evol 128:123–136

    Article  Google Scholar 

  • Campbell LG (2010) Registration of seven sugarbeet germplasms selected from crosses between cultivated sugarbeet and wild species. J Plant Regist 4:149. doi:10.3198/jpr2009.11.0673crg

    Article  Google Scholar 

  • Cheng D, Kitazaki K, Xu D et al (2009) The distribution of normal and male-sterile cytoplasms in Chinese sugar-beet germplasm. Euphytica 165:345–351. doi:10.1007/s10681-008-9796-0

    Article  Google Scholar 

  • Cheng D, Yoshida Y, Kitazaki K et al (2011) Mitochondrial genome diversity in Beta vulgaris L. ssp. vulgaris (leaf and garden beet groups) and its implications concerning the dissemination of the crop. Genet Resour Crop Evol 58:553–560. doi:10.1007/s10722-010-9598-9

    Article  Google Scholar 

  • Curk F, Ancillo G, Ollitrault F et al (2015) Nuclear species-diagnostic SNP markers mined from 454 amplicon sequencing reveal admixture genomic structure of modern citrus varieties. PLoS One 10:e0125628

    Article  PubMed  PubMed Central  Google Scholar 

  • Desplanque B, Boudry P, Broomberg K et al (1999) Genetic diversity and gene flow between wild, cultivated and weedy forms of Beta vulgaris L. (Chenopodiaceae), assessed by RFLP and microsatellite markers. Theor Appl Genet 98:1194–1201

    Article  CAS  Google Scholar 

  • Dohm JC, Minoche AE, Holtgräwe D et al (2014) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546–549. doi:10.1038/nature12817

    Article  CAS  PubMed  Google Scholar 

  • Draycott AP (ed) (2006) Sugar beet. Blackwell, Oxford

    Google Scholar 

  • Ecke W, Michaelis G (1990) Comparison of chloroplast and mitochondrial DNA from five morphologically distinct Beta vulgaris cultivars: sugar beet, fodder beet, beet root, foliage beet, and Swiss chard. TAG Theor Appl Genet Theor Angew Genet 79:440–442. doi:10.1007/BF00226149

    CAS  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839. doi:10.1007/BF00221895

    Article  PubMed  Google Scholar 

  • Excoffier L, Dupanloup I, Huerta-Sánchez E et al (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9:e1003905. doi:10.1371/journal.pgen.1003905

    Article  PubMed  PubMed Central  Google Scholar 

  • Fénart S, Arnaud J-F, De Cauwer I, Cuguen J (2008) Nuclear and cytoplasmic genetic diversity in weed beet and sugar beet accessions compared to wild relatives: new insights into the genetic relationships within the Beta vulgaris complex species. Theor Appl Genet 116:1063–1077. doi:10.1007/s00122-008-0735-1

    Article  PubMed  Google Scholar 

  • Fievet V, Touzet P, Arnaud J-F, Cuguen J (2007) Spatial analysis of nuclear and cytoplasmic DNA diversity in wild sea beet (Beta vulgaris ssp. maritima) populations: do marine currents shape the genetic structure? Mol Ecol 16:1847–1864. doi:10.1111/j.1365-294X.2006.03208.x

    Article  PubMed  Google Scholar 

  • Fischer HE (1989) Origin of the “Weisse Schlesische Rübe” (white Silesian beet) and resynthesis of sugar beet. Euphytica 41:75–80. doi:10.1007/BF00022414

    Article  Google Scholar 

  • Frese L (2010) Conservation and Access to Sugarbeet Germplasm. Sugar Tech 12:207–219. doi:10.1007/s12355-010-0054-0

    Article  Google Scholar 

  • Frese L, Nachtigall M, Enders M, Pinheiro De Carvalho MAA (2012) Beta patula (Aiton): Genetic diversity analysis. In: Maxted N (ed) \Agrobiodiversity conservation: securing the diversity of crop wild relatives and landraces. CABI, Wallingford

    Google Scholar 

  • Fritzsche K, Metzlaff M, Melzer R, Hagemann R (1987) Comparative restriction endonuclease analysis and molecular cloning of plastid DNAs from wild species and cultivated varieties of the genus Beta (L.). Theor Appl Genet 74:589–594. doi:10.1007/BF00288857

    Article  CAS  PubMed  Google Scholar 

  • Hammer K, Stanarius A, Kühne T (1990) Differential occurrence of beet cryptic viruses—a new tool for germplasm characterization and evolutionary studies in beets? Euphytica 45:23–27. doi:10.1007/BF00032145

    Google Scholar 

  • Hjerdin A, Sall T, Nilsson NO et al (1994) Genetic variation among wild and cultivated beets of the section Beta as revealed by RFLP analysis. J Sugar Beet Res 31:59–67

    Article  Google Scholar 

  • Hoban S, Kelley JL, Lotterhos KE et al (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat 188:379–397. doi:10.1086/688018

    Article  PubMed  PubMed Central  Google Scholar 

  • Hyten DL, Song Q, Zhu Y et al (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci 103:16666–16671. doi:10.1073/pnas.0604379103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics. doi:10.1093/bioinformatics/btr521

    PubMed  PubMed Central  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones PD, Lister DH, Jaggard KW, Pidgeon JD (2003) Future climate impact on the productivity of sugar beet (Beta vulgaris L.) in Europe. Clim Change 58:93–108

    Article  Google Scholar 

  • Jung C, Pillen K, Frese L et al (1993) Phylogenetic relationships between cultivated and wild species of the genus Beta revealed by DNA “fingerprinting”. Theor Appl Genet 86:449–457. doi:10.1007/BF00838560

    Article  CAS  PubMed  Google Scholar 

  • Kadereit G, Hohmann S, Kadereit JW (2006) A synopsis of Chenopodiaceae subfam. Betoideae and notes on the taxonomy of Beta. Willdenowia 36:9–19. doi:10.3372/wi.36.36101

    Article  Google Scholar 

  • Kilian B, Graner A (2012) NGS technologies for analyzing germplasm diversity in genebanks. Brief Funct Genom 11:38–50. doi:10.1093/bfgp/elr046

    Article  CAS  Google Scholar 

  • Kishima Y, Mikami T, Hirai A et al (1987) Beta chloroplast genomes: analysis of fraction I protein and chloroplast DNA variation. Theor Appl Genet. doi:10.1007/BF00262497

    PubMed  Google Scholar 

  • Letschert JPW (1993) Beta section Beta: biogeographical patterns of variation, and taxonomy. Wagening Agric Univ Pap 93(1):1–155

    Google Scholar 

  • Leys M, Petit EJ, El-Bahloul Y et al (2014) Spatial genetic structure in Beta vulgaris subsp. maritima and Beta macrocarpa reveals the effect of contrasting mating system, influence of marine currents, and footprints of postglacial recolonization routes. Ecol Evol 4:1828–1852. doi:10.1002/ece3.1061

    Article  PubMed  PubMed Central  Google Scholar 

  • Litwiniec A, Gośka M, Choińska B et al (2016) Evaluation of rhizomania-resistance segregating sequences and overall genetic diversity pattern among selected accessions of Beta and Patellifolia. Potential implications of breeding for genetic bottlenecks in terms of rhizomania resistance. Euphytica 207:685–706. doi:10.1007/s10681-015-1570-5

    Article  CAS  Google Scholar 

  • Lu Y, Yan J, Guimarães CT et al (2009) Molecular characterization of global maize breeding germplasm based on genome-wide single nucleotide polymorphisms. Theor Appl Genet 120:93–115. doi:10.1007/s00122-009-1162-7

    Article  CAS  PubMed  Google Scholar 

  • Mangin B, Siberchicot A, Nicolas S et al (2012) Novel measures of linkage disequilibrium that correct the bias due to population structure and relatedness. Heredity 108:285–291. doi:10.1038/hdy.2011.73

    Article  CAS  PubMed  Google Scholar 

  • Mangin B, Sandron F, Henry K et al (2015) Breeding patterns and cultivated beets origins by genetic diversity and linkage disequilibrium analyses. Theor Appl Genet 128:2255–2271. doi:10.1007/s00122-015-2582-1

    Article  PubMed  Google Scholar 

  • Mason AS, Zhang J, Tollenaere R et al (2015) High-throughput genotyping for species identification and diversity assessment in germplasm collections. Mol Ecol Resour 15:1091–1101. doi:10.1111/1755-0998.12379

    Article  CAS  PubMed  Google Scholar 

  • Maxted N, Ford-Lloyd BV, Jury S et al (2006) Towards a definition of a crop wild relative. Biodivers Conserv 15:2673–2685. doi:10.1007/s10531-005-5409-6

    Article  Google Scholar 

  • McGrath JM, Derrico CA, Yu Y (1999) Genetic diversity in selected, historical US sugarbeet germplasm and Beta vulgaris ssp. maritima. Theor Appl Genet 98:968–976

    Article  Google Scholar 

  • Mikami T, Kishima Y, Sugiura M, Kinoshita T (1984) Chloroplast DNA diversity in the cytoplasms of sugar beet and its related species. Plant Sci Lett 36:231–235. doi:10.1016/0304-4211(84)90174-3

    Article  CAS  Google Scholar 

  • Mikami T, Yamamoto MP, Matsuhira H et al (2011) Molecular basis of cytoplasmic male sterility in beets: an overview. Plant Genet Resour 9:284–287. doi:10.1017/S1479262111000177

    Article  Google Scholar 

  • Mita G, Dani M, Casciari P et al (1991) Assessment of the degree of genetic variation in beet based on RFLP analysis and the taxonomy of Beta. Euphytica 55:1–6. doi:10.1007/BF00022552

    Article  CAS  Google Scholar 

  • Monteiro F, Romeiras MM, Batista D, Duarte MC (2013) Biodiversity assessment of sugar beet species and its wild relatives: linking ecological data with new genetic approaches. Am J Plant Sci 04:21–34. doi:10.4236/ajps.2013.48A003

    Article  Google Scholar 

  • Morin PA, Luikart G, Wayne RK, The SNP workshop group (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19:208–216. doi:10.1016/j.tree.2004.01.009

    Article  Google Scholar 

  • Nagamine T, Catty JP, Ford-Lloyd BV (1989) Phenotypic polymorphism and allele differentiation of isozymes in fodder beet, multigerm sugar beet and monogerm sugar beet. Theor Appl Genet 77:711–720

    Article  CAS  PubMed  Google Scholar 

  • Ober ES, Clark CJA, Bloa ML et al (2004) Assessing the genetic resources to improve drought tolerance in sugar beet: agronomic traits of diverse genotypes under droughted and irrigated conditions. Field Crops Res 90:213–234. doi:10.1016/j.fcr.2004.03.004

    Article  Google Scholar 

  • Rong J, Lammers Y, Strasburg JL et al (2014) New insights into domestication of carrot from root transcriptome analyses. BMC Genom 15:1

    Google Scholar 

  • Saccomani M, Stevanato P, Trebbi D et al (2009) Molecular and morpho-physiological characterization of sea, ruderal and cultivated beets. Euphytica 169:19–29. doi:10.1007/s10681-009-9888-5

    Article  Google Scholar 

  • Santoni S, Bervillé A (1992a) Characterization of the nuclear ribosomal DNA units and phylogeny of Beta L. wild forms and cultivated beets. Theor Appl Genet 83:533–542

    Article  CAS  PubMed  Google Scholar 

  • Santoni S, Bervillé A (1992b) Two different satellite DNAs in Beta vulgaris L.: evolution, quantification and distribution in the genus. Theor Appl Genet 84:1009–1016

    CAS  PubMed  Google Scholar 

  • Santoni S, Bervillé A (1992c) Evidence for gene exchanges between sugar beet (Beta vulgaris L.) and wild beets: consequences for transgenic sugar beets. Plant Mol Biol 20:578–580

    Article  CAS  PubMed  Google Scholar 

  • Santoni S, Faivre-Rampant P, Moreau E, Bervillé A (1991) Rapid control of purity for the cytoplasm of male-sterile seed stocks by means of a dot hybridization assay. Mol Cell Probes 5:1–9

    Article  CAS  PubMed  Google Scholar 

  • Schiffels S, Durbin R (2014) Inferring human population size and separation history from multiple genome sequences. Nat Genet 46:919–925. doi:10.1038/ng.3015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoville SD, Bonin A, François O et al (2012) Adaptive genetic variation on the landscape: methods and cases. Annu Rev Ecol Evol Syst 43:23–43. doi:10.1146/annurev-ecolsys-110411-160248

    Article  Google Scholar 

  • Senda M, Onodera Y, Mikami T (1998) Cytoplasmic diversity in leaf beet cultivars as revealed by mitochondrial DNA analysis. Hereditas 128:127–132

    Article  CAS  PubMed  Google Scholar 

  • Shen Y, Ford-Lloyd BV, Newbury J (1998) Genetic relationships within the genus Beta determined using both PCR-based marker and DNA sequencing techniques. Heredity 80:624–632

    Article  CAS  PubMed  Google Scholar 

  • Shun ZF, Chu SY, Frese L (2000) Study on the relationship between Chinese and East Mediterranean Beta vulgaris L. subsp. vulgaris (leaf beet group) accessions. In: Maggioni L, Frese L, Germeier C, Lipman E (eds) Report of a working group on Beta. International Plant Genetic Resources Institute, Rome, pp 65–69

    Google Scholar 

  • Stevanato P, Trebbi D, Biancardi E et al (2013) Evaluation of genetic diversity and root traits of sea beet accessions of the Adriatic Sea coast. Euphytica 189:135–146. doi:10.1007/s10681-012-0775-0

    Article  Google Scholar 

  • Thermo Fisher Scientific Inc. (2017) AxiomTM Genotyping Solution Data Analysis Guide. http://tools.thermofisher.com/content/sfs/manuals/axiom_genotyping_solution_analysis_guide.pdf. Accessed 23 March 2017

  • Tian H-L, Wang F-G, Zhao J-R et al (2015) Development of maizeSNP3072, a high-throughput compatible SNP array, for DNA fingerprinting identification of Chinese maize varieties. Mol Breed. doi:10.1007/s11032-015-0335-0

    PubMed  PubMed Central  Google Scholar 

  • van Geyt JPC, Lange W, Oleo M, De Bock TSM (1990) Natural variation within the genus Beta and its possible use for breeding sugar beet : a review. Euphytica 49:57–76

    Article  Google Scholar 

  • Viard F, Arnaud J-F, Delescluse M, Cuguen J (2004) Tracing back seed and pollen flow within the crop-wild Beta vulgaris complex: genetic distinctiveness vs. hot spots of hybridization over a regional scale. Mol Ecol 13:1357–1364. doi:10.1111/j.1365-294X.2004.02150.x

    Article  CAS  PubMed  Google Scholar 

  • Villain S (2007) Histoire évolutive de la section Beta: mise en évidence des phénomènes d’hybridation et de spéciation au sein de la Section dans le bassin Méditerranéen. Ph.D., Université Lille 1-Sciences et Technologies

  • Wang M, Goldman IL (1999) Genetic distance and diversity in table beet and sugar beet accessions measured by randomly amplified polymorphic DNA. J Am Soc Hortic Sci 124:630–635

    CAS  Google Scholar 

  • Warschefsky E, Penmetsa RV, Cook DR, von Wettberg EJB (2014) Back to the wilds: tapping evolutionary adaptations for resilient crops through systematic hybridization with crop wild relatives. Am J Bot 101:1791–1800. doi:10.3732/ajb.1400116

    Article  PubMed  Google Scholar 

  • Weihe A, Dudareva NA, Veprev SG et al (1991) Molecular characterization of mitochondrial DNA of different subtypes of male-sterile cytoplasms of the sugar beet Beta vulgaris L. Theor Appl Genet 82:11–16. doi:10.1007/BF00231271

    Article  CAS  PubMed  Google Scholar 

  • Winkler LR, Michael Bonman J, Chao S et al (2016) Population structure and genotype–phenotype associations in a collection of oat landraces and historic cultivars. Front Plant Sci. doi:10.3389/fpls.2016.01077

    Google Scholar 

  • Würschum T (2012) Mapping QTL for agronomic traits in breeding populations. Theor Appl Genet 125:201–210. doi:10.1007/s00122-012-1887-6

    Article  PubMed  Google Scholar 

  • Würschum T, Maurer HP, Kraft T et al (2011) Genome-wide association mapping of agronomic traits in sugar beet. Theor Appl Genet 123:1121–1131. doi:10.1007/s00122-011-1653-1

    Article  PubMed  Google Scholar 

  • Yoshida Y, Matsunaga M, Cheng D et al (2012) Mitochondrial minisatellite polymorphisms in fodder and sugar beets reveal genetic bottlenecks associated with domestication. Biol Plant 56:369–372. doi:10.1007/s10535-012-0101-7

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the French Government, under the management of the Research National Agency (ANR-11-BTBR-0007) through the AKER program (included in the “Investissements d’avenir”).

Author information

Authors and Affiliations

  1. EPHE, PSL Research University, CEFE UMR 5175, CNRS, Université de Montpellier, Université Paul-Valéry Montpellier, Biogéographie et Ecologie des Vertébrés, 1919 route de Mende, 34293, Montpellier Cedex 5, France

    Marco Andrello & Stéphanie Manel

  2. Florimond Desprez, 59242, Cappelle En Pévèle, France

    Karine Henry, Pierre Devaux, Daphné Verdelet & Bruno Desprez

Authors
  1. Marco Andrello
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karine Henry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pierre Devaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daphné Verdelet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bruno Desprez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stéphanie Manel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marco Andrello.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Compliance with ethical standards

Not applicable.

Additional information

Communicated by André J. Bervillé.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 25 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andrello, M., Henry, K., Devaux, P. et al. Insights into the genetic relationships among plants of Beta section Beta using SNP markers. Theor Appl Genet 130, 1857–1866 (2017). https://doi.org/10.1007/s00122-017-2929-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-017-2929-x

Search

Navigation