Genetic diversity and population structure show different patterns of diffusion for bitter and sweet manioc in Brazil

Abstract

Although many important crops originated in Amazonia, the general patterns of their evolutionary histories are still obscure. Currently a major global food crop, manioc originated in southwestern Amazonia and was dispersed throughout the lowland Neotropics before the European conquest. However, little is known about the origin of the bitter and sweet landraces, nor the routes by which these were dispersed in Brazil and beyond. We used a non-systematic Brazil-wide sample of 494 manioc landraces from 11 geographic regions, and ten nuclear microsatellite markers to analyze the genetic diversity of sweet and bitter manioc. Bayesian simulations highlighted the bitter–sweet divergence and also suggested the existence of two groups of sweet manioc (circum-Cerrado and general Brazil) and two groups of bitter manioc (upper Negro River and general Brazil), while the relationships among geographic regions were depicted with clustering analysis. Overall we suggest that: (1) manioc was initially domesticated to be sweet, was then dispersed from southwestern Amazonia into both the Amazon basin and the Cerrado; (2) that bitter manioc arose from the general Brazilian sweet manioc landraces, almost certainly in Amazonia, where bitter manioc became most important and was dispersed both throughout Amazonia and along the Brazilian coast, but especially to the upper Negro River, where it became most diverse. Our study adds insights to the knowledge about how native Amazonian crops have been managed across their history of domestication.

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

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

Data availability statement

The majority of the data set, with passport information and full microsatellite allele data has been uploaded in Online Resource 1 Supplementary Table S1. The indigenous manioc landraces collected by the Bilateral Project CNPq/Instituto Socioambiental—ISA/Institut de Recherche pour le Développement—IRD, proc. No. 91.0211/97-3, are not included, since these require separate authorization from the Federação das Organizações Indígenas do Rio Negro—FOIRN. Please contact GSM for guidance to obtain this new authorization.

References

  1. Albrecht E, Zhang D, Saftner RA, Stommel JR (2012) Genetic diversity and population structure of Capsicum baccatum genetic resources. Genet Resour Crop Evol 59:517–538

    Google Scholar 

  2. Allaby RG, Fuller DQ, Brown TA (2008) The genetic expectations of a protracted model for the origins of domesticated crops. Proc Natl Acad Sci USA 105:13982–13986

    CAS  PubMed  Google Scholar 

  3. Allem AC (1994) The origin of Manihot esculenta Crantz (Euphorbiaceae). Genet Resour Crop Evol 41:133–150

    Google Scholar 

  4. Alves-Pereira A, Peroni N, Abreu AG, Gribel R, Clement CR (2011) Genetic structure of traditional varieties of bitter manioc in three soils in Central Amazonia. Genetica 139:1259–1271

    PubMed  Google Scholar 

  5. Alves-Pereira A, Peroni N, Cavallari MM, Lemes MR, Zucchi MI, Clement CR (2017) High genetic diversity among and within bitter manioc varieties cultivated in different soil types in Central Amazonia. Genet Mol Biol 40:468–479

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Alves-Pereira A, Clement CR, Picanço-Rodrigues D, Veasey EA, Dequigiovanni G, Ramos SLF, Pinheiro JB, Zucchi MI (2018) Patterns of nuclear and chloroplast genetic diversity and structure of manioc along major Brazilian Amazonian rivers. Ann Bot 121:625–639

    PubMed  PubMed Central  Google Scholar 

  7. Andersen MD, Busk PK, Svendsen I, Møller BL (2000) Cytochromes P-450 from cassava (Manihot esculenta Crantz) catalyzing the first steps in the biosynthesis of the cyanogenic glucosides linamarin and lotaustralin—cloning, functional expression in Pichia pastoris, and substrate specificity of the isolated recombinant enzymes. J Biol Chem 275:1966–1975

    CAS  PubMed  Google Scholar 

  8. Arroyo-Kalin M (2010) The Amazonian formative: crop domestication and anthropogenic soils. Diversity 2:473–504

    Google Scholar 

  9. Belkhir K, Goudet J, Chikhi L, Bonhomme F (2004) Genetix, logiciel sous WindowsTM pour la génétique des populations, ver. 4.05. http://www.genetix.univ-montp2.fr/genetix/genetix.htm. Accessed 15 Jan 2011

  10. Bradbury EJ, Duputié A, Delêtre M, Roullier C, Narváez-Trujillo A, Manu-Aduening JA, Emshwiller E, McKey D (2013) Geographic differences in patterns of genetic differentiation among bitter and sweet manioc (Manihot esculenta subsp. esculenta; Euphorbiaceae). Am J Bot 100:857–866

    PubMed  Google Scholar 

  11. Brown CH, Clement CR, Epps P, Luedeling E, Wichmann S (2013) The paleobiolinguistics of domesticated manioc (Manihot esculenta). Ethnobiol Lett 4:61–70

    Google Scholar 

  12. Burns A, Gleadow R, Cliff J, Zacarias A, Cavagnaro T (2010) Cassava: the drought, war and famine crop in a changing world. Sustainability 2:3572–3607

    Google Scholar 

  13. Chavarriaga-Aguirre PP, Maya MM, Bonierbale MW, Kresovich S, Fregene MA, Tohme J, Kochert G (1998) Microsatellites in cassava (Manihot esculenta Crantz): discovery, inheritance and variability. Theor Appl Genet 97:493–501

    CAS  Google Scholar 

  14. Chevenet F, Brun C, Bañuls AL, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinform 7:439

    Google Scholar 

  15. Chiwona-Karltun L, Brimer L, Saka JDK, Mhone AR, Mkumbira J, Johansson L et al (2004) Bitter taste in cassava roots correlates with cyanogenic glucoside level. J Sci Food Agric 84:581–590

    CAS  Google Scholar 

  16. Clement CR, Cristo-Araújo M, d’Eeckenbrugge GC, Alves-Pereira A, Picanço-Rodrigues D (2010) Origin and domestication of native Amazonian crops. Diversity 2:72–106

    Google Scholar 

  17. Clement CR, Cristo-Araújo M, Coppens D’Eeckenbrugge G, Reis VM, Lehnebach R, Picanço-Rodrigues D (2017) Origin and dispersal of domesticated peach palm. Front Ecol Evol 5:148. https://doi.org/10.3389/fevo.2017.00148

    Article  Google Scholar 

  18. Cordeiro CMT, Abadie T (2007) Coleções nucleares. In: Nass LL (ed) Recursos Genéticos Vegetais. Embrapa Recursos Genéticos e Biotecnologia, Brasília, pp 575–604

    Google Scholar 

  19. Dieringer D, Schlötterer C (2003) Microsatellite analyzer (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    CAS  Google Scholar 

  20. Doyle JJ, Doyle JL (1987) Isolation of plant DNA from fresh tissue. Focus 1:13–15

    Google Scholar 

  21. Duputié A, David P, Debain C, McKey D (2007) Natural hybridization between a clonally propagated crop, cassava (Manihot esculenta Crantz) and a wild relative in French Guiana. Mol Ecol 16:3025–3038

    PubMed  Google Scholar 

  22. Duputié A, Massol F, David P, Haxaire C, McKey D (2009) Traditional Amerindian cultivators combine directional and ideotypic selection for sustainable management of cassava genetic diversity. J Evol Biol 22:1317–1325

    PubMed  Google Scholar 

  23. Elias M, Mühlen GS, McKey D, Roa AC, Tohme J (2004) Genetic diversity of traditional South American landraces of cassava (Manihot esculenta Crantz): an analysis using microsatellites. Econ Bot 58:242–256

    Google Scholar 

  24. Emperaire L, Cabral de Oliveira R (2010) Redes sociales y diversidad agrícola en la Amazonía brasileña: un sistema multicéntrico. In: Pochettino ML, Ladio AH, Arenas PM (eds) Tradiciones y Transformaciones en Etnobotánica. Cyted, San Salvador de Jujuy, pp 184–189

    Google Scholar 

  25. Emperaire L, Peroni N (2007) Traditional management of agrobiodiversity in Brazil: a case study of manioc. Hum Ecol 35:761–768

    Google Scholar 

  26. Emperaire L, Mühlen GS, Fleury M et al (2003) Approche comparative de la diversité génétique et de la diversité morphologique des maniocs en Amazonie (Brésil et Guyanes). Les Actes du Bureau des Ressources Génétiques 4:247–267

    Google Scholar 

  27. 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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  29. FAOStat (2018) Food and Agriculture Organization of the United Nations, Statistics Division. http://www.fao.org/faostat/en/#data/QC. Accessed 08 July 2018

  30. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package), version 3.6. Computer program distributed by the author, Department of Genome Sciences, University of Washington, Seattle

  31. Fraser JA (2010) The diversity of bitter manioc (Manihot esculenta Crantz) cultivation in a whitewater Amazonian landscape. Diversity 2:586–609

    Google Scholar 

  32. Fraser JA, Alves-Pereira A, Junqueira AB, Peroni N, Clement CR (2012) Convergent adaptations: bitter manioc cultivation systems in fertile anthropogenic dark earths and floodplain soils in Central Amazonia. PLoS ONE 7:e43636

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Fregene MA, Suarez M, Mkumbira J, Kulembeka H, Ndedya E, Kulaya A et al (2003) Simple sequence repeat marker diversity in cassava landraces: genetic diversity and differentiation in an asexually propagated crop. Theor Appl Genet 107:1083–1093

    CAS  PubMed  Google Scholar 

  34. Gepts P (2004) Crop domestication as a long-term selection experiment. Plant Breed Rev 24:1–44

    Google Scholar 

  35. Gleadow RM, Møller BL (2014) Cyanogenic glycosides: synthesis, physiology, and phenotypic plasticity. Annu Rev Plant Biol 65:155–185

    CAS  PubMed  Google Scholar 

  36. Gribel R, Lemes MR, Bernardes LG, Pinto AE, Shepard GH Jr (2007) Phylogeography of Brazil-nut tree (Bertholletia excelsa, Lecythidaceae): evidence of human influence on the species distribution. Association for Tropical Biology and Conservation, Morelia, p 281

    Google Scholar 

  37. Hernández-Ugalde JA, Mora-Urpí J, Rocha OJ (2011) Genetic relationships among wild and cultivated populations of peach palm (Bactris gasipaes Kunth, Palmae): evidence for multiple independent domestication events. Genet Resour Crop Evol 58:571–583

    Google Scholar 

  38. Isendahl C (2011) The domestication and early spread of manioc (Manihot esculenta Crantz): a brief synthesis. Lat Am Antiq 22:452–468

    Google Scholar 

  39. Johns T (1990) With bitter herbs they shall eat it. Chemical ecology and the origins of human diet and medicine. University of Arizona Press, Tucson

    Google Scholar 

  40. Johns T (2016) A chemical-ecological model of root and tuber domestication in the Andes. In: Harris DR, Hillman GC (eds) Foraging and farming: the evolution of plant exploitation. Routledge, London, pp 504–522

    Google Scholar 

  41. Johns T, Alonso JG (1990) Glycoalkaloid change during the domestication of the potato, Solanum Section Petota. Euphytica 50:203–210

    CAS  Google Scholar 

  42. Jørgensen K, Morant AV, Morant M, Jensen NB, Olsen CE, Kannangara R, Motawia MS, Møller BL, Bak S (2011) Biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in cassava: isolation, biochemical characterization, and expression pattern of CYP71E7, the oxime-metabolizing cytochrome P450 enzyme. Plant Physiol 155:282–292

    PubMed  Google Scholar 

  43. Kannangara R, Motawia MS, Hansen NK, Paquette SM, Olsen CE, Møller BL, Jørgensen K (2011) Characterization and expression profile of two UDP-glucosyltransferases, UGT85K4 and UGT85K5, catalyzing the last step in cyanogenic glucoside biosynthesis in cassava. Plant J 68:287–301. https://doi.org/10.1111/j.1365-313X.2011.04695.x

    CAS  Article  PubMed  Google Scholar 

  44. Lathrap DW (1970) The upper Amazon. Praeger, New York

    Google Scholar 

  45. Lebot V (2009) Tropical root and tuber crops: cassava, sweet potato, yams and aroids. CAB International, Oxford

    Google Scholar 

  46. Léotard G, Duputié A, Kjellberg F, Douzery EJP, Debain C, de Granville J-J, McKey D (2009) Phylogeography and the origin of cassava: new insights from the northern rim of the Amazonian basin. Mol Phylogenet Evol 53:329–334

    PubMed  Google Scholar 

  47. Lin Z, Li X, Shannon LM, Yeh CT, Wang ML, Bai G, Peng Z et al (2012) Parallel domestication of the Shattering1 genes in cereals. Nat Genet 44:720–724

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Martins PS (2001) Dinâmica evolutiva em roças de caboclos amazônicos. In: Vieira ICG, Silva JMC, Oren DC, D’Incao MA (eds) Diversidade biológica e cultural da Amazônia. Museu Paraense Emílio Goeldi, Belém, pp 369–384

    Google Scholar 

  49. Mason AS (2015) SSR genotyping. In: Batley J (ed) Plant genotyping. Springer, New York, pp 77–89

    Google Scholar 

  50. Mba REC, Stephenson P, Edwards K, Melzer S, Nkumbira J, Gullberg U et al (2001) Simple sequence repeat (SSR) markers survey of the cassava (Manihot esculenta Crantz) genome: towards an SSR-based molecular genetic map of cassava. Theor Appl Genet 102:21–31

    CAS  Google Scholar 

  51. McKey D, Beckerman S (1993) Chemical ecology, plant evolution and traditional manioc cultivation systems. In: Hladik CM, Hladick A, Linares OF, Pagezy H, Semple A, Hadley M (eds) Tropical forests, people and food: biocultural interactions and applications to development. Parthenon Carnforth and UNESCO, Paris, pp 83–112

    Google Scholar 

  52. McKey D, Delêtre M (2017) The emergence of cassava as a global crop. In: Hershey CH (ed) Achieving sustainable cultivation of cassava, vol 1. Burleigh Dodds Science Publishing, London, pp 3–32

    Google Scholar 

  53. McKey D, Cavagnaro TR, Cliff J, Gleadow R (2010) Chemical ecology in coupled human and natural systems: people, manioc, multitrophic interactions and global change. Chemoecology 20:109–133

    CAS  Google Scholar 

  54. Moses M, Umaharam P, Dayanandan S (2014) Microsatellite based analysis of the genetic structure and diversity of Capsicum chinense in the Neotropics. Genet Resour Crop Evol 61:741–755

    CAS  Google Scholar 

  55. Mühlen GS, Martins PS, Ando A (2000) Variabilidade genética de etnovariedades de mandioca, avaliada por marcadores de DNA. Sci Agr 57:319–328

    Google Scholar 

  56. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170

    CAS  PubMed  Google Scholar 

  57. Oliveira EJ, Ferreira CF, Santos VS, Jesus ON, Oliveira GAF, Silva MS (2014) Potential of SNP markers for the characterization of Brazilian cassava germplasm. Theor Appl Genet 127:1423–1440

    PubMed  Google Scholar 

  58. Olsen KM (2004) SNPs, SSRs and inferences on cassava’s origin. Plant Mol Biol 56:517–526

    CAS  PubMed  Google Scholar 

  59. Olsen KM, Schaal BA (1999) Evidence on the origin of cassava: phylogeography of Manihot esculenta. Proc Natl Acad Sci USA 96:5586–5591

    CAS  PubMed  Google Scholar 

  60. Olsen KM, Schaal BA (2001) Microsatellite variation in cassava (Manihot esculenta, Euphorbiaceae) and its wild relatives: further evidence for a southern Amazonian origin of domestication. Am J Bot 88:131–142

    CAS  PubMed  Google Scholar 

  61. Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Google Scholar 

  62. Peroni N, Kageyama PY, Begossi A (2007) Molecular differentiation, diversity, and folk classification of “sweet” and “bitter” cassava (Manihot esculenta) in Caiçara and Caboclo management systems (Brazil). Genet Resour Crop Evol 54:1333–1349

    Google Scholar 

  63. Perrut-Lima P, Mühlen GS, Carvalho CRL (2014) Cyanogenic glycoside content in Manihot esculenta subsp. flabellifolia in south-central Rondônia, Brazil, in the center of domestication of M. esculenta subsp. esculenta. Genet Resour Crop Evol 61:1035–1038

    CAS  Google Scholar 

  64. Piperno DR, Pearsall DM (1998) The origins of agriculture in the lowland Neotropics. Academic Press, San Diego

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Pujol B, David P, McKey D (2005) Microevolution in agricultural environments: how a traditional Amerindian farming practice favours heterozygosity in cassava (Manihot esculenta Crantz, Euphorbiaceae). Ecol Lett 8:138–147

    Google Scholar 

  67. Purugganan MD, Fuller DQ (2009) The nature of selection during plant domestication. Nature 457:843–848

    CAS  PubMed  Google Scholar 

  68. Rabbi IY, Kulembeka HP, Masumba E, Marri PR, Ferguson M (2012) An EST-derived SNP and SSR genetic linkage map of cassava (Manihot esculenta Crantz). Theor Appl Genet 125:329–342

    CAS  PubMed  Google Scholar 

  69. Reeves PA, Richards CM (2007) Distinguishing terminal monophyletic groups from reticulate taxa: performance of phenetic, tree-based, and network procedures. Syst Biol 56:302–320

    PubMed  Google Scholar 

  70. Renvoize BS (1972) The area of origin of Manihot esculenta as a crop plant—a review of the evidence. Econ Bot 26:352–360

    Google Scholar 

  71. Rodrigues DP, Astolfi Filho S, Clement CR (2004) Molecular marker-mediated validation of morphologically defined landraces of pejibaye (Bactris gasipaes) and their phylogenetic relationships. Genet Resour Crop Evol 51:871–882

    CAS  Google Scholar 

  72. Rozenthal JP, Dirzo R (1997) Effects of life history, domestication and agronomic selection on plant defense against insects: evidence from maizes and wild relatives. Evol Ecol 11:337–355

    Google Scholar 

  73. Seeb JE, Carvalho G, Hauser L, Naish K, Roberts S, Seeb LW (2011) Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in non-model organisms. Mol Ecol Resour 11(Suppl 1):1–8

    PubMed  Google Scholar 

  74. Siqueira MVBM, Queiroz-Silva JR, Bressan EA, Borges A, Pereira KJC, Pinto JG, Veasey EA (2009) Genetic characterization of cassava (Manihot esculenta) landraces in Brazil assessed with simple sequence repeats. Genet Mol Biol 32:104–110

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Siqueira MVBM, Pinheiro TT, Borges A, Valle TL, Zatarim M, Veasey EA (2010) Microsatellite polymorphisms in cassava landraces from the Cerrado biome, Mato Grosso do Sul, Brazil. Biochem Genet 48:879–895

    CAS  PubMed  Google Scholar 

  76. Sousa SB, Silva GF, Dias MC, Clement CR, Sousa NR (2017) Farmer variety exchange along Amazonian rivers influence the genetic structure of manioc maintained in a regional Brazilian GeneBank. Genet Mol Res 16:gmr16039690

    Google Scholar 

  77. Studer A, Zhao Q, Ross-Ibarra J, Doebley J (2011) Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43:1160–1163

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Sujii PS, Martins K, de Oliveira Wadt LH, Azevedo VCR, Solferini VN (2015) Genetic structure of Bertholletia excelsa. Conserv Genet 16:955–964

    Google Scholar 

  79. Thomas E, van Zonneveld M, Loo J, Hodgkin T, Galluzzi G, Etten J (2012) Present spatial diversity patterns of Theobroma cacao L. in the Neotropics reflect genetic differentiation in Pleistocene refugia followed by human-influenced dispersal. PLoS ONE 7:e47676. https://doi.org/10.1371/journal.pone.0047676

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  80. Valle TL, Mühlen GS (2003) Agrupamento de variedades de mandioca mansas e bravas através de marcadores moleculares. Project Report to FAPESP, São Paulo

  81. Valle TL, Carvalho CRL, Ramos MTB, Mühlen GS, Vilela OV (2004) Conteúdo cianogênico em progênies de mandioca originadas do cruzamento de variedades mansas e bravas. Bragantia 63:221–226

    CAS  Google Scholar 

  82. Vigouroux Y, Glaubitz JC, Matsuoka Y, Goodman MM, Sánchez GJ, Doebley J (2008) Population structure and genetic diversity of New World maize races assessed by DNA microsatellites. Am J Bot 95:1240–1253

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, 00/00239-3 and 00/00240-1), for primary funding, the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, CT-Amazônia-575588/08-0) for logistic and analytical support, the numerous traditional and indigenous farmers who agreed to our collections, the Bilateral Project CNPq/Instituto Socioambiental (ISA)/Institut de Recherche pour le Développement (IRD), (CNPq, 91.0211/97-3). We thank the French Bureau des Ressources Génétiques, for use of manioc landraces from the upper Negro River, ISA and the Federação das Organizações Indígenas do Rio Negro (FOIRN) for authorizing reuse of the genetic information from the manioc landraces of the upper Negro River. We thank Laure Emperaire (IRD), Doyle McKey (Université de Montpellier), Manuel Arroyo-Kalin (University College London), for comments on the manuscript, and Josefino Fialho (Embrapa Cerrados), for several manioc samples. AA-P thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, 51/2013) and FAPESP (2018/00036-9) for post-doctoral scholarships. CRC thanks CNPq (303851/2015-5) for a research fellowship.

Author information

Affiliations

Authors

Contributions

GSM and TLV designed research, GSM, TLV and CRLC performed research, GSM, TLV and CRLC contributed reagents, GSM, AA-P and CRC analyzed data, ABJ contributed GIS support and map design, GSM, AA-P, CRC, TLV, and ABJ wrote the paper.

Corresponding author

Correspondence to Alessandro Alves-Pereira.

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.

Supplementary Table S1

Passport data, SSR genotypes and ancestry coefficients of Structure analysis for 494 Brazilian manioc landraces. Supplementary Table S2 Microsatellite identification, size range in base pairs (bp), number of alleles (A), observed heterozygosity (HO), expected heterozygosity (HE), and inbreeding coefficient (f) estimated from 494 Brazilian manioc landraces. Loci were developed by aChavarriaga-Aguirre et al. (1998) and bMba et al. (2001). *significant at p < 0.05 (XLSX 119 kb)

Supplementary Fig. S1

Plot of ΔK of possible groups of 494 Brazilian manioc landraces obtained from ten Structure analysis simulations. The Structure analysis was extended to K = 20 because of the 11 geographical groupings of the manioc landraces, nine of which had both bitter and sweet manioc. Supplementary Fig. S2 Comparison of principal coordinate analyses according to different groupings of the 494 Brazilian manioc landraces screened with ten SSR loci. Groups according to A) bitter and sweet identification by passport data, and according to results of Structure analysis for B) K = 2, C) K = 3 and D) K = 4. Supplementary Fig. S3 Proportional representation of the four major groups of Brazilian manioc landraces identified by the Structure analysis within the 11 geographically-defined groupings (DOC 1967 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mühlen, G.S., Alves-Pereira, A., Carvalho, C.R.L. et al. Genetic diversity and population structure show different patterns of diffusion for bitter and sweet manioc in Brazil. Genet Resour Crop Evol 66, 1773–1790 (2019). https://doi.org/10.1007/s10722-019-00842-1

Download citation

Keywords

  • Bayesian clustering
  • Cassava
  • Domestication
  • Genetic relationships
  • Geographic distribution
  • Manihot esculenta