Skip to main content

Development and use of microsatellite markers for genetic diversity analysis of cañahua (Chenopodium pallidicaule Aellen)

Abstract

Cañahua (Chenopodium pallidicaule Aellen) is a poorly studied, annual subsistence crop of the high Andes of South America. Its nutritional value (high in protein and mineral content) and ability to thrive in harsh climates make it an important regional food crop throughout the Andean region. The objectives of this study were to develop genetic markers and to quantify genetic diversity within cañahua. A set of 43 wild and cultivated cañahua genotypes and two related species (Chenopodium quinoa Willd. and Chenopodium petiolare Kunth) were evaluated for polymorphism using 192 microsatellite markers derived from random genomic cañahua sequences produced by 454 pyrosequencing of cañahua genomic DNA. Another 424 microsatellite markers from C. quinoa were also evaluated for cross-species amplification and polymorphism in cañahua. A total of 34 polymorphic microsatellite marker loci were identified which detected a total of 154 alleles with an average of 4.5 alleles per marker locus and an average heterozygosity value of 0.49. A cluster analysis, based on Nei genetic distance, clearly separated from wild cañahua genotypes from the cultivated genotypes. Within the cultivated genotypes, subclades were partitioned by AMOVA analysis into six model-based clusters, including a subclade consisting sole of erect morphotypes. The isolation by distance test displayed no significant correlation between geographic collection origin and genotypic data, suggesting that cañahua populations have moved extensively, presumably via ancient food exchange strategies among native peoples of the Andean region. The molecular markers reported here are a significant resource for ongoing efforts to characterize the extensive Bolivian and Peruvian cañahua germplasm banks, including the development of core germplasm collections needed to support emerging breeding programs.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Achigan-Dako EG (2008) Phylogenetic and genetic variation analyses in cucurbit species (Cucurbitaceae) from West Africa: definition of conservation strategies. Cuvillier Verlag, Göttingen

    Google Scholar 

  2. Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154

    PubMed  Article  CAS  Google Scholar 

  3. Bonifacio A (2003) Chenopodium sp.: genetic resources, ethnobotany, and geographic distribution. Food Rev Int 19:1–7

    Article  Google Scholar 

  4. Di Gaspero G, Peterlunger E, Testolin R, Edwards KJ, Cipriani G (2000) Conservation of microsatellite loci within the genus Vitis. Theor Appl Genet 101:301–308

    Article  CAS  Google Scholar 

  5. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Google Scholar 

  6. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    PubMed  Article  CAS  Google Scholar 

  7. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  PubMed Central  Google Scholar 

  8. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    CAS  Google Scholar 

  9. Flores R (2006) Evaluación preliminar agronómica y morfológica del germoplasma de cañahua (Chenopodium pallidicaule Aellen) en la estación experimental Belen. Universidad Mayor de San Andrés, La Paz

    Google Scholar 

  10. Friedt W, Snowdon RJ, Ordon F, Ahlemeyer J (2007) Plant breeding: assessment of genetic diversity in crop plants and its exploitation in breeding. In: K. Esser UL, W. Beyschlag, J. Murata (eds). Springer, Berlin, pp 151–178

  11. Gade D (1970) Ethnobotany of cañahua (Chenopodium pallidicaule), rustic seed crop of the altiplano. Econ Bot 24:55–61

    Article  Google Scholar 

  12. Gaitan-Solis E, Duque MC, Edwards KJ, Tohme J (2002) Microsatellite repeats in common bean (Phaseolus vulgaris): isolation, characterization, and cross-species amplification in Phaseolus ssp. Crop Sci 42:2128–2136

    Article  CAS  Google Scholar 

  13. Galwey NW (1989) Exploited plants—Quinoa. Biologist 36:267–274

    Google Scholar 

  14. Groben R, Wricke G (1998) Occurrence of microsatellites in spinach sequences from computer databases and development of polymorphic SSR markers. Plant Breed 117:271–274

    Article  CAS  Google Scholar 

  15. Gumerman G (1997) Food and complex societies. J Archaeol Meth Theor 12:105–139

    Article  Google Scholar 

  16. Höglund J (2009) Evolutionary conservation genetics, 1st edn. Oxford University Press, New York

    Book  Google Scholar 

  17. Huelsenbeck JP, Andolfatto P (2007) Inference of population structure under a Dirichlet process model. Genetics 175:1787–1802

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  18. IPGRI, PROINPA, IFAD (2005) Descriptores para cañahua (Chenopodium pallidicaule Aellen). Instituto Internacional de Recursos Fitogenéticos, Roma, Italia; Fundación PROINPA, La Paz, Bolivia; International Fund for Agricultural Development, Roma, Italia

  19. Jarvis DE, Kopp OR, Jellen EN, Mallory MA, Pattee J, Bonifacio A, Coleman CE, Stevens MR, Fairbanks DJ, Maughan PJ (2008) Simple sequence repeat marker development and genetic mapping in quinoa (Chenopodium quinoa Willd.). J Genet 87:39–51

    PubMed  Article  CAS  Google Scholar 

  20. Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129

    PubMed  Article  CAS  Google Scholar 

  21. Mallory MA, Hall RV, McNabb AR, Pratt DB, Jellen EN, Maughan PJ (2008) Development and characterization of microsatellite markers for the grain Amaranths. Crop Sci 48:1098–1106

    Article  CAS  Google Scholar 

  22. Marin W (2002) Distanciamiento entre surcos y plantas en dos ecotipos de kañawa (Chenopodium pallidicaule Aellen) en el Altiplano Norte. Universidad Mayor de San Andrés, La Paz

    Google Scholar 

  23. Marti N, Pimbert M (2007) Barter markets for the conservation of agro-ecosystem multi-functionality: the case of the chalayplasa in the Peruvian Andes. Int J Agr Sustain 5:51–69

    Google Scholar 

  24. Mason SL, Stevens MR, Jellen EN, Bonifacio A, Fairbanks DJ, Coleman CE, McCarty RR, Rasmussen AG, Maughan PJ (2005) Development and use of microsatellite markers for germplasm characterization in quinoa (Chenopodium quinoa Willd.). Crop Sci 45:1618–1630

    Article  CAS  Google Scholar 

  25. Morchen M, Cuguen J, Michaelis G, Hanni C, SaumitouLaprade P (1996) Abundance and length polymorphism of microsatellite repeats in Beta vulgaris L. Theor Appl Genet 92:326–333

    PubMed  Article  CAS  Google Scholar 

  26. Muller K, Borsch T (2005) Phylogenetics of Amaranthaceae based on matK/trnK sequences data: evidence from parsimony, likelihood, and bayesian analysis. Ann Missouri Bot Gard 92:66–102

    Google Scholar 

  27. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  CAS  PubMed Central  Google Scholar 

  28. Nei M, Li WH (1979) Mathematical-model for studying genetic-variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A 76:5269–5273

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  29. Nei M, Tajima F (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105:207–217

    PubMed  CAS  PubMed Central  Google Scholar 

  30. Ott J (1992) Strategies for characterizing highly polymorphic markers in human gene-mapping. Am J Hum Genet 51:283–290

    PubMed  CAS  PubMed Central  Google Scholar 

  31. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  PubMed Central  Google Scholar 

  32. Repo-Carrasco R, Espinoza C, Jacobsen SE (2003) Nutritional value and use of the Andean crops quinoa (Chenopodium quinoa) and kañiwa (Chenopodium pallidicaule). Food Rev Int 19:179–189

    Article  Google Scholar 

  33. Repo-Carrasco-Valencia R, de La Cruz AA, Alvarez JCI, Kallio H (2009) Chemical and functional characterization of kañiwa (Chenopodium pallidicaule) grain, extrudate and bran. Plant Foods Hum Nutr 64:94–101

    PubMed  Article  CAS  Google Scholar 

  34. Risi CJ, Galwey NW (1984) The Chenopodium grains of the Andes: Inca crops for modern agriculture. Adv Appl Biol 10:145–216

    Google Scholar 

  35. Rist S (2000) Linking ethics and the market—Campesino economic strategies in the Bolivian Andes. Mt Res Dev 20:310–315

    Article  Google Scholar 

  36. Rodríguez M (2007) Evaluación de las pérdidas de grano y grado de impurezas en cuatro métodos de cosecha de cañahua (Chenopodium pallidicaule Aellen) en la comunidad de Quipaquipani, Viacha. Universidad Mayor de San Andrés, La Paz

    Google Scholar 

  37. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  38. Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422

    PubMed  CAS  Google Scholar 

  39. Todd JJ, Vodkin LO (1996) Duplications that suppress and deletions that restore expression from a chalcone synthase multigene family. Plant Cell 8:687–699

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  40. Vaz ARD, Borba TCD, Brondani C, Rangel PHN, Camargo GSD, Telles MPD, Filho JAF, Brondani RPV (2009) Genetic analysis of a local population of Oryza glumaepatula using SSR markers: implications for management and conservation programs. Genetica 137:221–231

    Article  Google Scholar 

  41. Weir B (1996) Genetic Data Analysis II: Methods for discrete population genetic data. Sinauer Assoc., Inc, Sunderland

    Google Scholar 

  42. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370

    Article  Google Scholar 

  43. Woods Páez A, Eyzaguirre P (2004) Cañahua deserves to come back. Leisa 20:11–13

    Google Scholar 

  44. Wright S (1946) Isolation by distance under diverse systems of mating. Genetics 31:39–59

    PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by grants from the McKnight Foundation, as well as the Ezra Taft Benson Agriculture and Food institute and Holmes Family Foundation. We gratefully acknowledge the advice and support provided by Dr. Alejandro Bonifacio, PROINPA Foundation, Bolivia and are grateful to Dinesh Adhikary, Nathan Mahler, Joshua Raney, and Shawna and James Daley for technical support in developing the microsatellite protocols. We are also grateful to David Brenner of the USDA NC-7 (Ames, IA) and Dr. Angel Mujica of the National University of the Altiplano (Puno, Peru) for providing seed for this study.

Author information

Affiliations

Authors

Corresponding author

Correspondence to P. J. Maughan.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Vargas, A., Elzinga, D.B., Rojas-Beltran, J.A. et al. Development and use of microsatellite markers for genetic diversity analysis of cañahua (Chenopodium pallidicaule Aellen). Genet Resour Crop Evol 58, 727–739 (2011). https://doi.org/10.1007/s10722-010-9615-z

Download citation

Keywords

  • Cañahuaf
  • Genetic diversity
  • Microsatellite markers
  • Population structure