Skip to main content
Log in

Genetic diversity analysis of Tibetan turnip(Brassica rapa L. ssp. rapifera Matzg) revealed by morphological, physiological, and molecular marker

  • Research Article
  • Published:
Genetic Resources and Crop Evolution Aims and scope Submit manuscript

Abstract

Turnip of the Brassica genus is a traditional crop that is widely cultivated in farming and farming-pastoral regions in Tibet. It is mostly utilized as animal fodder and vegetable around the Tibetan plateau. Given their high altitudes and variable climate types, different regions of Tibet plateau are home to a rich diversity of turnip. A mass of studies related to genetic diversity of highland crops have been carried out in recent years. However, the genetic diversity of Tibetan turnip remains to be elucidated to date. In this study, we performed morphological investigation and simple sequence repeat analysis, to characterize the genetic diversity and population structure of Tibetan turnips. Then, we explored the physiological response of seedlings under low-temperature stress. We also performed a field experiment, to identify clubroot-resistant cultivars. Results showed significant differences in phenotypic traits among different sources of 25 Tibetan turnip accessions. The genetic similarity dendrogram showed that the genetic distance in the 25 accessions was between 0.61 and 0.77. When the similarity coefficient is between 0.644 and 0.646, they can be divided into three subgroups, and they presented a certain relationship between geographical origin and its genetic distance. The central diffusion location suggests that the genetic diversity and population structure of these Tibetan turnip accessions are consistent with their geographical origin. In addition, the potential clubroot resistance accession is 156-13, and the chilling resistance accessions are 156-8 and 156-10. These results suggest the Tibetan turnip is a valuable resource for the genetic analysis and breeding of new clubroot-resistant cultivars.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Agarwal M, Shrivastava N, Padh H (2008) Advances in molecular marker techniques and their applications in plant sciences. Plant Cell Rep 27:617–631

    PubMed  CAS  Google Scholar 

  • Aissiou F, Laperche A, Falentin C, Lodé M, Deniot G, Boutet G, Régnier F, Trotoux G, Huteau V, Coriton O, Rousseau-Guentin M, Abrous O, Chèvre AM, Hadj-Arab H (2018) A novel Brassica rapa L. genetic diversity found in Algeria. Euphytica 214:241

    Google Scholar 

  • Andersen NS, Poulsen G, Andersen BA, Kiær LP, D’Hertefeldt T, Wilkinson MJ, Jørgensen RB (2009) Processes affecting genetic structure and conservation: a case study of wild and cultivated Brassica rapa. Genet Resour Crop Evol 56:189–200

    Google Scholar 

  • Ashworth EN (1992) Formation and spread of ice in plant tissues. Hortic Rev 13:215–255

    Google Scholar 

  • Bjørnstad Å, Aastveit K (1990) Pleiotropic effects on the ml-o mildew resistance gene in barley in different genetical backgrounds. Euphytica 46:217–226

    Google Scholar 

  • Bradshaw JE, Gemmell DJ, Wilson RN (2010) Transfer of resistance to clubroot (Plasmodiophora brassicae) to swedes (Brassica napus L. var. napobrassica Peterm) from B. rapa. Ann Appl Biol 130:337–348

    Google Scholar 

  • Cao JS, Cao SC, Miao Y, Lu G (1997) Cldistic operational analysis and study on the evolution of Chinese cabbage groups (Brassica campestris L.). Acta Hortic Sin 24(1):35–42

    Google Scholar 

  • Chen J, Jing J, Zhan Z, Zhang T, Zhang C, Piao Z (2013) Identification of novel QTLs for isolate-specific partial resistance to Plasmodiophora brassicae in Brassica rapa. PLoS ONE 8:e85307

    PubMed  PubMed Central  Google Scholar 

  • Committee of Chinese herbal medicine (2002) Chinese herbal medicine—Tibetan medicine. Science & Technology Press of Shanghai, Shanghai, pp 349–350

    Google Scholar 

  • De Barba M, Miquel C, Lobreaux S, Quenette PY, Swenson JE, Taberlet P (2017) High-throughput microsatellite genotyping in ecology: improved accuracy, efficiency, standardization and success with low-quantity and degraded DNA. Mol Ecol Resour 17:492–507

    PubMed  Google Scholar 

  • Delfina B, Alessandro T, Francesca D, Andrea V, Patrizia V, Giampiero V, Luigi C (2016) Next generation breeding. Plant Sci 242:3–13

    Google Scholar 

  • Diederichsen E, Frauen M, Linders EGA, Hatakeyama K, Hirai M (2009) Status and perspectives of clubroot resistance breeding in crucifer crops. J Plant Growth Regul 28:265–281

    CAS  Google Scholar 

  • Dixon GR, Dixon GR (2009) Plasmodiophora brassicae in its environment. J Plant Growth Regul 28:212–228

    CAS  Google Scholar 

  • Donald C, Porter I (2009) Integrated control of clubroot. J Plant Growth Regul 28:289–303

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gao JT, Li N, Xuan ZY, Yang WC (2017) Genetic diversity among “Qamgur” varieties in China revealed by SSR markers. Euphytica 213:204

    Google Scholar 

  • Goodwin S, McPherson JD, McCombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 17:333–351

    PubMed  CAS  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Hasan MJ, Strelkov SE, Howard RJ, Rahman H (2012) Screening of Brassica germplasm for resistance to Plasmodiophora brassicae pathotypes prevalent in Canada for broadening diversity in clubroot resistance. Can J Plant Sci 92:501–515

    Google Scholar 

  • Hatakeyama K, Niwa T, Kato T, Ohara T, Kakizaki T, Matsumoto S (2017) The tandem repeated organization of NB-LRR genes in the clubroot-resistant CRb locus in Brassica rapa L. Mol Genet Genom 292:397–405

    CAS  Google Scholar 

  • Heber U (1958) Ursachen der frostresistenz bei winterweizen. Planta 52:431–446

    CAS  Google Scholar 

  • Howard R, Strelkov S, Harding M (2010) Clubroot of cruciferous crops: new perspectives on an old disease. Can J Plant Pathol 32:43–57

    Google Scholar 

  • Hughes MA, Dunn MA (1996) The molecular biology of plant acclimation to low temperature. J Exp Bot 47:291–305

    CAS  Google Scholar 

  • Kalia RK, Rai MK, Kalia S, Singh R, Dhawan AK (2011) Microsatellite markers: an overview of the recent progress in plants. Euphytica 177:309–334

    CAS  Google Scholar 

  • Kaur S, Panesar PS, Bera MB, Kaur V (2015) Simple sequence repeat markers in genetic divergence and marker-assisted selection of rice cultivars: a review. Crit Rev Food Sci Nutr 55:41–49

    PubMed  CAS  Google Scholar 

  • Kuan KC (1985) Cruciferae. In: Wu CY (ed) Flora Xizangica, vol 2. Science Press of China, Beijing, pp 323–412

    Google Scholar 

  • Kuroda H, Sagisaka S (2008) Participation of hydrogen peroxide in the dysfunction of peroxide-scavenging systems in apple flower buds associated with freezing injury. Engei Gakkai Zasshi 67:161–165

    Google Scholar 

  • Li JW (1981) The origins and evolution of vegetable crops in China. Sci Agric Sin 14:90–95

    Google Scholar 

  • Li XX, Shen D (2008) Descriptors and data standard for root and stem mustard (Brassica juncea Coss.). Chinese Agricultural Press, Beijing, pp 1–82

    Google Scholar 

  • Liu J, Cui H (1995) Electrical conductivity method for chilling-resistance evaluation in cucumber. J Northwest Sci-Tech Univ Agric For 23(4):74–77

    Google Scholar 

  • Liu H, Jiang SP, Yang LL, Chen ZJ, Bao SF, Xu AG, Bu HT, Gao P (2012) Hypoglycemic effect of crude saponins of turnip (Brassica rapa L.) on diabetic mice. J Northwest A F Univ 40(6):23–27

    Google Scholar 

  • Liu SR, Li WY, Dang L, Hu CG, Zhang JZ (2013) Development and characterization of genomic and expressed SSRs in citrus by genome-wide analysis. PLoS ONE 8:e75149

    PubMed  PubMed Central  CAS  Google Scholar 

  • Manzanares-Dauleux MJ, Delourme R, Baron F, Thomas G (2000) Mapping of one major gene and of QTLs involved in resistance to clubroot in Brassica napus. Theor Appl Genet 101:885–891

    CAS  Google Scholar 

  • Meng FJ, Liu L, Peng M, Wang ZK, Wang C, Zhao YY (2015) Genetic diversity and population structure analysis in wild strawberry (Fragaria nubicola L.) from Motuo in Tibet Plateau based on simple sequence repeats (SSRs). Biochem Syst Ecol 63:113–118

    CAS  Google Scholar 

  • Meng Z, Song F, Liu T (2018) Genetic diversity and genetic structure analysis of maize (Zea mays) landraces in Tibet. Int J Agric Biol 20:791–798

    CAS  Google Scholar 

  • Neik TX, Barbetti MJ, Batley J (2017) Current status and challenges in identifying disease resistance genes in Brassica napus. Front Plant Sci 8:1788

    PubMed  PubMed Central  Google Scholar 

  • Padilla G, Cartea ME, Rodriguez VM, Ordas A (2005) Genetic diversity in a germplasm collection of Brassica rapa subsp. rapa L. from northwestern Spain. Euphytica 145:171–180

    Google Scholar 

  • Pan X, Cao Q, Wang G (2002) Evaluation of lipid peroxidation for use in selection of cold hardiness cultivars of Almond. Acta Ecol Sin 22:1902–1911

    Google Scholar 

  • Pang W, Shan L, Li X, Li P, Sha Y, Yong PL, Piao Z (2014) Genetic detection of clubroot resistance loci in a new population of Brassica rapa. Hortic Environ Biotechnol 55:540–547

    CAS  Google Scholar 

  • Peng G, Lahlali R, Hwang SF, Pageau D, Hynes RK, Mcdonald MR, Gossen BD, Strelkov SE (2014) Crop rotation, cultivar resistance, and fungicides/biofungicides for managing clubroot (Plasmodiophora brassicae) on canola. Can J Plant Pathol 36:99–112

    CAS  Google Scholar 

  • Porrashurtado L, Ruiz Y, Santos C, Phillips C, Carracedo A, Lareu MV (2013) An overview of STRUCTURE: applications, parameter settings, and supporting software. Front Genet 4:98

    Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74

    PubMed  PubMed Central  CAS  Google Scholar 

  • Rieger M (1989) Freeze protection for horticultural crops. Hortic Rev 11:45–109

    CAS  Google Scholar 

  • Soengas P, Cartea ME, Francisco M, Lema M, Velasco P (2011) Genetic structure and diversity of a collection of Brassica rapa subsp. rapa L. revealed by simple sequence repeat markers. J Agric Sci 149:617–624

    CAS  Google Scholar 

  • Strelkov SE, Hwang SF, Manolii VP, Cao T, Feindel D (2016) Emergence of new virulence phenotypes of Plasmodiophora brassicae on canola (Brassica napus) in Alberta, Canada. Eur J Plant Pathol 145:1–13

    Google Scholar 

  • Takahashi Y, Yokoi S, Takahata Y (2016) Genetic divergence of turnip (Brassica rapa L. em. Metzg. subsp. rapa) inferred from simple sequence repeats in chloroplast and nuclear genomes and morphology. Genet Resour Crop Evol 63:869–879

    CAS  Google Scholar 

  • Tang WM, Chu BQ, Gao WL, Wu CJ, Gong LX, Dai XL, Zhang Y (2015) Comparative studies of chemical compositions and antioxidant capacity of low-polarity components from Tibetan turnip (Brassica rapa L.) and Maca (Lepidium meyenii Walp). Nat Prod Res Dev 27:674–680

    CAS  Google Scholar 

  • Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23:48–55

    PubMed  CAS  Google Scholar 

  • Wang JL, Dan B, Hu SY, Tu JX, Luan YF, Meng X, Zhuo G, Nima ZM, Tang L (2002) RAPD analysis for the genetic diversity of Brassica rapa in Tibet. Acta Genet Sin 29:1021–1027

    PubMed  Google Scholar 

  • Wang JL, Luan YF, Daci ZG, Chang TJ (2006) Geographical distribution and biological characters of wild rapeseed in Tibet. Chin J Oil Crop Sci 28(2):134–137

    Google Scholar 

  • Wang JL, Dan B, Cheng HH, Fang HL, Chang TJ, Li P, Luan YF (2008) AFLP analysis on genetic diversity of wild and cultivated rapeseed (B. campestris and B. juncea) in Tibet. Chin J Oil Crop Sci 30:10–16

    CAS  Google Scholar 

  • Williams PH (1996) A system for the determination of races of Plasmodiophora brassicae that infect cabbage and rutabaga. Phytopathology 56:624–626

    Google Scholar 

  • Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation: evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol 83:278–282

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wit F, Weg MVD (1964) Clubroot-resistance in turnips (Brassica campestris L.). Euphytica 13:9–18

    Google Scholar 

  • Wu CY, Lu AM, Tang YC (2003) The families and genera of angiosperms in China. Science Press of China, Beijing, pp 504–521

    Google Scholar 

  • Xu ZX, Gong TL, Zhao FF (2006) Analysis of climate change in Tibetan Plateau over the past 40 years. J Subtrop Resour Environ 1(1):24–32

    Google Scholar 

  • Yada B, Alajo A, Ssemakula GN, Brown-Guedira G, Otema MA, Stevenson PC, Mwanga ROM, Yencho GC (2017) Identification of simple sequence repeat markers for sweetpotato weevil resistance. Euphytica 213:129

    Google Scholar 

  • Yildirim E, Yildirim N, Ercisli S, Agar G, Karlidag H (2010) Genetic relationships among turnip (Brassica rapa var. rapa) genotypes. Genet Mol Res 9:987

    PubMed  CAS  Google Scholar 

  • Yu FQ, Zhang XG, Huang Z, Chu MG, Song T, Falk KC, Deora A, Chen QL, Zhang Y, McGregor L, Gossen BD, McDonald MR, Peng G (2016) Identification of genome-wide variants and discovery of variants associated with Brassica rapa clubroot resistance gene Rcr1 through bulked segregant RNA sequencing. PLoS ONE 11(4):e0153218

    PubMed  PubMed Central  Google Scholar 

  • Yuan H, Zeng X, Xu Q, Wang Y, Zha S, Nyima T (2018) Genetic diversity of germplasm resource and core collection development in hulless barley. J Triticeae Crops 38:922–928

    Google Scholar 

  • Zhan L, Paterson IG, Fraser BA, Watson B, Bradbury IR, Ravindran PN, Reznick D, Beiko RG, Bentzen P (2017) MEGASAT: automated inference of microsatellite genotypes from sequence data. Mol Ecol Resour 17:247–256

    PubMed  CAS  Google Scholar 

  • Zhang Y, Tang WM, Ma NI, Li JJ, Zhu MD, Gong LX, Chen XJ, Liu YF, Bian B, Wu XQ (2014) Effects of Tibetan turnip and its processed products on human tolerance to hypoxia. Food Sci 35:178–182

    CAS  Google Scholar 

  • Zhu H, Song P, Koo DH, Guo L, Li Y, Sun S, Weng Y, Yang L (2016) Genome wide characterization of simple sequence repeats in watermelon genome and their application in comparative mapping and genetic diversity analysis. BMC Genom 17:557

    Google Scholar 

Download references

Acknowledgements

The authors gratefully thank those students in College of Plant Science, Tibet Agricultural and Animal Husbandry University for collecting the seeds of turnips from the different counties in Tibet. This work was partially supported by National Natural Science Foundation of China (31460521), the Breeding Project of the Sci-tech Foundation of Zhejiang Province (2016C02051-6-1), the Project of SRTP in Zhejiang University (2018R401080), the Project of Sci-tech Foundation of Jiangsu Province (BE2018310), and the Project of Application on Public Welfare Technology in Zhejiang Province (LGN18C150003). The authors thank Dr. Zhenning Liu for his critical reading the manuscript, also thank the anonymous reviewers for their critical comments and suggestions on manuscript revision.

Author information

Authors and Affiliations

Authors

Contributions

XY and WG proposed and designed the research. YG, LZ, YZ and YG performed the experiments. YG, RL, JL, KL and KZ performed the statistical analyses, interpretation of experimental results. YG and XY wrote the manuscript.

Corresponding author

Correspondence to Xiaolin Yu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10722_2019_824_MOESM1_ESM.jpg

Figure S1. Results of malondialdehyde content under the different low-temperatures stresses (5 °C, 15 °C, and 25 °C). Bands in blue, orange, and green present 5 °C, 15 °C, and 25 °C respectively. Error bar represent standard error (three repetitions) (JPEG 894 kb)

10722_2019_824_MOESM2_ESM.jpg

Figure S2. Results of soluble sugar content under different low-temperatures stress (5 °C, 15 °C and 25 °C). Bands in blue, orange, and green present 5 °C, 15 °C, and 25 °C respectively. Error bar represent standard error (three repetitions). (JPEG 905 kb)

Supplementary material 3 (XLSX 18 kb)

Supplementary material 4 (XLSX 10 kb)

Supplementary material 5 (XLSX 11 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, Y., Gong, W., Li, R. et al. Genetic diversity analysis of Tibetan turnip(Brassica rapa L. ssp. rapifera Matzg) revealed by morphological, physiological, and molecular marker. Genet Resour Crop Evol 67, 209–223 (2020). https://doi.org/10.1007/s10722-019-00824-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10722-019-00824-3

Keywords

Navigation