Skip to main content

Advertisement

Log in

Genomic Diversity of Three Brazilian Native Food Crops Based on Double-Digest Restriction Site-Associated DNA Sequencing

  • Published:
Tropical Plant Biology Aims and scope Submit manuscript

Abstract

The megabiodiversity of Brazil created opportunities for the domestication of a number of crop species, including some of major global importance. Considering the economic value of many Brazilian native crops, the genetic characterization of their populations is fundamental to support the utilization and conservation of their genetic resources, currently threatened by deforestation and the intensification of monuculture of exotic crops. Recent advances in DNA sequencing technologies have promoted the rapid genomic evaluation of non-model species, including those of only local importance. In this context, we evaluated the genomic diversity of three native Brazilian crops: manioc (Manihot esculenta), annatto (Bixa orellana) and the juçara palm (Euterpe edulis). Double-digest restriction site-associated DNA sequencing (ddRAD) was employed to identify thousands of SNP markers in each crop species (1952 in manioc, 3362 in annatto and 1040 in juçara). Population genomic analyses identified many loci putatively under selection, but the unavailability of genome sequences for annatto and juçara hampers further characterization for these crops. Nonetheless, the SNP markers identified were effective in the characterization of the genomic diversity and population structure. The levels of genomic diversity and inbreeding were compatible with the biology of each species. While wild and cultivated manioc were remarkably genetically divergent, the same was not observed between accessions of wild and cultivated annatto, and genetic differentiation was observed among juçara samples from different environments. The application of population genomic approaches may be valuable for the establishment of better practices of management of these crops, promoting the conservation and valorization of Brazilian native genetic resources.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /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.

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

The ddRAD sequences generated and analyzed during the current study will be available after publication as FASTQ files (.fq.gz) in the Sequence Read Archive (SRA) repository of the National Center for Biotechnology Information (NCBI), accession PRJNA493823 (https://www.ncbi.nlm.nih.gov/sra/PRJNA493823).

References

  • Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1(1):95–111

    PubMed  PubMed Central  Google Scholar 

  • Allem AC (2002) The origins and taxonomy of cassava. In: Hillocks RJ, Thresh JM, Bellotti AC (eds) Cassava: biology, production and utilization. CAB International, Oxford

    Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart GH (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    CAS  PubMed  Google Scholar 

  • Allendorf FW, Luikart GH, Aitken SN (2013) Conservation and the genetics of populations. Oxford Wiley-Blackwell, Oxford

    Google Scholar 

  • Almeida E, Pinheiro A (1992) Biologia floral e mecanismo de reprodução em urucuzeiro (Bixa orellana L.) I. tipo “fruto verde piloso”. In: Reunião técnico científica sobre melhoramento genético do urucuzeiro. Embrapa – CEPATU, Belém

    Google Scholar 

  • 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 

  • 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(4):625–639. https://doi.org/10.1093/aob/mcx190

    Article  PubMed  PubMed Central  Google Scholar 

  • Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA (2016) Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet 17:81–92

    CAS  PubMed  PubMed Central  Google Scholar 

  • Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) Lositan: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9:323

    PubMed  PubMed Central  Google Scholar 

  • Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3(10):e3376

    PubMed  PubMed Central  Google Scholar 

  • Barrett RDH, Hoekstra HE (2011) Molecular spandrels: tests of adaptation at the genetic level. Nat Rev Genet 12(11):767–780

    CAS  PubMed  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. P Roy Soc Lond 263:1619–1626

    Google Scholar 

  • Bevan MW, Uauy C (2013) Genomics reveals new landscapes for crop improvement. Genome Biol 14(6):206

    PubMed  PubMed Central  Google Scholar 

  • Bonierbale M, Roa AC, Maya MM, Duque MC, Thome J (1997) Assessment of genetic diversity in Manihot species with AFLPs. African J Root Tuber Crops 2:139

    Google Scholar 

  • Bragg JG, Megan AS, Andrew RL, Borevitz JO (2015) Genomic variation across landscapes: insights and applications. New Phytol 207(4):953–967

    PubMed  Google Scholar 

  • Brancalion PHS, Vidal E, Lavorenti NA, Batista JLF, Rodrigues RR (2012) Soil-mediated effects on potential Euterpe edulis (Arecaceae) fruit and palm heart sustainable management in the Brazilian Atlantic Forest. Forest Ecol Manag 284:78–85

    Google Scholar 

  • Bredeson JV et al (2016) Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat Biotechnol 34(5):562–570

    CAS  PubMed  Google Scholar 

  • Brozynska M, Omar ES, Furtado A, Crayn D, Simon B, Ishikawa R, Henry RJ (2014) Chloroplast genome of novel rice germoplasm identified in northern Australia. Trop Plant Biol 7(3–4):111–120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brozynska M, Furtado A, Henry RJ (2016) Genomics of crop wild relatives: expanding the gene pool for crop improvement. Plant Biotechnol J 14(4):1070–1085

    CAS  PubMed  Google Scholar 

  • Carvalho JFRP, Robinson IP, Alfenas AC (2005) Isozymic variability in a Brazilian collection of annatto (Bixa orellana L.). Pesqui Agropecu Bras 40(7):653–660

    Google Scholar 

  • Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3 (Bethesda) 1(3):171–182

    CAS  Google Scholar 

  • Catchen JM, Hohenlohe P, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22(11):3124–3140

    PubMed  PubMed Central  Google Scholar 

  • Clement CR (1999) 1492 and the loss of Amazonian crop genetic resources. I. The relation between domestication and human population decline. Econ Bot 53(2):188–202

    Google Scholar 

  • 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 

  • Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dequigiovanni G, Ramos SLF, Zucchi MI, Bajay MM, Pinheiro JB, Fabri EG, Bressan EA, Veasey EA (2014) Isolation and characterization of microsatellite loci for Bixa orellana, an important source of natural dyes. Genet Mol Res 13(4):9097–1002

    CAS  PubMed  Google Scholar 

  • Dequigiovanni G, Ramos SLF, Alves-Pereira A, Fabri EG, Carvalho PRN, Silva MG, Abdo MTVN, Martins ALM, Clement CR, Veasey EA (2017) Genetic diversity and structure in a major Brazilian annatto (Bixa orellana) germplasm bank revealed by microsatellites and biochemical traits. Genet Resour Crop Evol 64:1775–1788

    Google Scholar 

  • Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321

    CAS  PubMed  Google Scholar 

  • Donkin RA (1974) Bixa orellana: the eternal shrub. Anthropos 69:33–56

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bull 12:11–15

    Google Scholar 

  • 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(2):242–256

    Google Scholar 

  • Emerson KJ, Merz CR, Catchen JM, Hohenlohe PA, Cresko WA, Bradshaw WE, Holzapfel CM (2010) Resolving postglacial phylogeography using high-throughput sequencing. Proc Natl Acad Sci U S A 107(37):16196–16200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fraser JA, Clement CR (2008) Dark earths and manioc cultivation in Central Amazonia: a window on pre-Columbian agricultural systems? Bol Mus Par Emilio Goeldi 3(2):175–194

    Google Scholar 

  • Freeland JR, Kirk H, Petersen S (2011) Molecular ecology. Wiley-Blackwell, West Sussex

    Google Scholar 

  • Fuller DQ (2007) Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World. Ann Bot 100:903–924

    PubMed  PubMed Central  Google Scholar 

  • Gaiotto FA, Grattapaglia D, Vencovsky R (2003) Genetic structure, mating system, and long-distance gene flow in heart of palm (Euterpe edulis Mart.). J Heredity 94(5):399–406

    CAS  Google Scholar 

  • Galetti M, Guevara R, Côrtes MC, Fadini R, Matter SV et al (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340(6136):1086–1090

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High- throughput functional annotation and data mining with the Blsat2Go suite. Nucleic Acids Res 36(10):3420–3435

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goudet J (2004) Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186

    Google Scholar 

  • Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS One 7(9):e45170

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hamblin MT, Warburton ML, Buckler ES (2007) Empirical comparison of simple sequence repeats and single nucleotide polymorphisms in assessment of maize diversity and relatedness. PLoS One 2(12):e1367

    PubMed  PubMed Central  Google Scholar 

  • Henderson A, Galeano G, Bernal R (1995) Field guide to the palms of the Americas. Princeton University, Princeton

    Google Scholar 

  • Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental change. Nat Rev Genet 9(6):421–432

    CAS  PubMed  Google Scholar 

  • Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6(2):e1000862

    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 27:3070–3071

    CAS  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

    PubMed  PubMed Central  Google Scholar 

  • Kamvar ZN, Tabima JF, Grunwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281

    PubMed  PubMed Central  Google Scholar 

  • Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation of population genetics parameters and their associated errors. Methods Ecol Evol 4(8):782–788

    Google Scholar 

  • Kess T, Gross J, Harper F, Boulding EG (2015) Low-cost ddRAD method of SNP discovery and genotyping applied to the periwinkle Littorina saxatilis. J Molluscan Stud 82(1):104–109

    Google Scholar 

  • Kohn MH, Murphy WJ, Ostrander EA, Wayne RK (2006) Genomics and conservation genetics. Trends Ecol Evol 21(11):629–637

    PubMed  Google Scholar 

  • Ladizinsky G (1998) Plant evolution under domestication. Kluwer Academic, London

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lebot V (2009) Tropical root and tuber crops: cassava, sweet potato, yams and aroids. Crop production science in horticulture (17). CAB books, CABI, Wallingford

    Google Scholar 

  • Li H (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27(21):2987–2993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25(16):2078–2079

    PubMed  PubMed Central  Google Scholar 

  • Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4(12):981–994

    CAS  PubMed  Google Scholar 

  • Macher J-N, Rozenberg A, Pauls SU, Tollrian R, Wagner R, Leese F (2015) Assessing the phylogeographic history of the montane caddisfly Thremma gallicum using mitochondrial and restriction-site-associated DNA (RAD) markers. Ecol Evol 5(3):648–662

    PubMed  PubMed Central  Google Scholar 

  • Mantovani A, Morellato LP (2000) Fenologia da floração, frutificação, mudança foliar e aspectos da biologia floral do palmiteiro. Sellowia 49:23–38

    Google Scholar 

  • McKey D, Beckerman S (1993) Chemical ecology, plant evolution and traditional Manioc cultivation systems. In: Hladik CM, 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

    Google Scholar 

  • McKey D, Elias M, Pujol B, Duputié A (2010) The evolutionary ecology of clonally propagated domesticated plants. New Phytol 186(2):318–332

    PubMed  Google Scholar 

  • McKey D, Elias M, Pujol B, Duputié A (2012) Ecological approaches to crop domestication. In: Gepts P, Famula TR, Bettinger R, Brush SB, Damania AB, McGuire PE, Qualset CO (eds) Biodiversity in agriculture: domestication, evolution and sustainability. Cambridge University Press, Cambridge

    Google Scholar 

  • Mirante AS, Sampaio MJA, Inglis MCV (2009) The state of Brazil’s plant genetic resources: second national report: conservation and sustainable utilization for food and agriculture. Embrapa Genetic Resources and Biotechnology, Brasília

    Google Scholar 

  • MMA - Ministério do Meio Ambiente (2002) Secretaria de Biodiversidade e Florestas. Biodiversidade Brasileira. Avaliação e identificação de áreas e ações prioritárias para conservação, utilização sustentável e repartição dos benefícios da biodiversidade nos biomas brasileiros. MMA/SBF, Brasília

  • MMA - Ministério do Meio Ambiente (2008) Instrução Normativa n°6, de 23 de setembro de 2008. Espécies da flora brasileira ameaçadas de extinção. Diário oficial da união de 23 de Setembro de 2008. (Seção 1) http://www.ibama.gov.br/phocadownload/category/47-_?download=999%3A_06-2008.p. Cited 21 Mar 2015

  • Monzote L, Montalvo AM, Almanonni S, Scull R, Miranda M, Abreu J (2006) Activity of the essential oil from Chenopodium ambrosioides grown in Cuba against Leishmania amazonensis. Chemotherapy 52:130–136

    CAS  PubMed  Google Scholar 

  • Moreira PA, Lins J, Dequigiovanni G, Veasey EA, Clement CR (2015) The domestication of annatto (Bixa orellana) from Bixa urucurana in Amazonia. Econ Bot 69:127–135

    Google Scholar 

  • Morin PA, Martien KK, Taylor BL (2009) Assessing statistical power of SNPs for population structure and conservation studies. Mol Ecol Resour 9:66–73

    CAS  PubMed  Google Scholar 

  • Nass LL, Sigrist MS, Ribeiro CSC, Reifschneider JB (2012) Genetic resources: the basis for sustainable and competitive plant breeding. Crop Breed Appl Biotechnol 2:75–86

    Google Scholar 

  • Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8(1):68–82

    CAS  PubMed  Google Scholar 

  • Novello M, Viana JPG, Alves-Pereira A, Silvestre EA, Nunes HF, Pinheiro JB, Brancalion PHS, Zucchi MI (2018) Genetic conservation of a threatened Neotropical palm through community-management of fruits in agroforest and second-growth forests. Forest Ecol Manag 407:200–209

    Google Scholar 

  • 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 

  • Olsen KM, Schaal BA (1999) Evidence on the origin of cassava: Phylogeography of Manihot esculenta. Proc Natl Acad Sci U S A 96(10):5586–5591

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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(1):131–142

    CAS  PubMed  Google Scholar 

  • Olsen KM, Wendel JF (2013) Crop plants as models for understanding plant adaptation and diversification. Front Plant Sci 4:290. https://doi.org/10.3389/fpls.2013.00290

    Article  PubMed  PubMed Central  Google Scholar 

  • Orlande T, Laarman J, Mortimer J (1996) Palmito sustainability and economics in Brazil’s Atlantic coastal forest. Forest Ecol Manag 80:257–265

    Google Scholar 

  • Peroni N, Kageyama P, 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 

  • Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7:e37135

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prochnik S, Marri P, Desany B, Rabinowicz P, Kodira C, Mohiuddin M, Rodriguez F, Fauquet C, Tohme J, Harkins T, Rokhsar D, Rounsley S (2012) The cassava genome: current progress, future directions. Trop Plant Biol 5(1):88–94

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reis MS, Fantini AC, Nodari RO, Reis A, Guerra MP, Mantovani A (2000) Management and conservation of natural populations in Atlantic rain forest: the case study of palm heart (Euterpe edulis Martius). Biotropica 32:894–902

    Google Scholar 

  • Rival L, McKey D (2008) Domestication and diversity in manioc (Manihot esculenta Crantz ssp. esculenta, Euphorbiaceae). Curr Anthropol 49(6):1119–1128

    Google Scholar 

  • Sandy-Cuen PM, Becerra R (2003) Manejo campesino de recursos naturales. El achiote. BioDiversitas 7:7–11

    Google Scholar 

  • Seeb JE, Carvalho G, Hauser L, Naish K, Roberts S, Seeb LW (2011) Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in nonmodel organisms. Mol Ecol Resour 11(s1):1–8

    PubMed  Google Scholar 

  • Souza SEXF, Vidal E, Chagas GF, Elgar AT, Brancalion PHS (2016) Ecological outcomes and livelihood benefits of community-managed agroforests and second growth forests in Southeast Brazil. Biotropica 48:868–881

    Google Scholar 

  • Stölting KN, Nipper R, Lindtke D, Caseys C, Waeber S, Castiglione S, Lexer C (2013) Genomic scan for single nucleotide polymorphisms reveals patterns of divergence and gene flow between ecologically divergent species. Mol Ecol 22(3):842–855

    PubMed  Google Scholar 

  • Valdez-Ojeda R, Quiros CF, de Lourdes Aguilar-Espinosa M et al (2010) Outcrossing rates in annatto determined by sequence-related amplified polymorphism. Agron J 102(5):1340–1345

    CAS  Google Scholar 

  • Varshney RK, Nayak SN, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27(9):522–530

    CAS  PubMed  Google Scholar 

  • Vilares AS, São José AR, Rebouças TNH, Souza IVB (1992) Estudo da biologia floral de urucuzeiro (Bixa orellana L.). Rev Bras Corantes Naturais 1:101–105

    Google Scholar 

  • Willing E-M, Dreyer C, van Oosterhout C (2012) Estimates of genetic differentiation measured by FST do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7(8):e42649

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H, Tao Y, Zheng Z, Li C, Sweetingham MW, Howieson JG (2012) Application of next-generation sequencing for rapid marker development in molecular plant breeding: a case study on anthracnose disease resistance in Lupinus angustifolius L. BMC Genomics 13(318):1–11

    Google Scholar 

Download references

Acknowledgments

This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES – BioComputacional 051/2013), and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP – 2012/08307-5, 2013/00003-0). AA-P thanks CAPES and FAPESP (2018/00036-9) for post-doctoral scholarships. MN (2013/17354-0) and GD (2013/08884-5) thank FAPESP for doctoral scholarships. MIZ, JBP, CRC, PHSB and APS thank the National Council for Scientific and Technological Development (CNPq) for research fellowships and a post-doctoral scholarship (grant # 150297/2018-1) of GD. The authors thank Danilo Augusto Sforça and Aline C.L. Moraes for laboratory assistance.

Author information

Authors and Affiliations

Authors

Contributions

AA-P, MN, GD, APS and MIZ designed the research. AA-P, MN, GD, PHSB, EAV, and CRC performed sample collections. AA-P, MN and GD prepared the ddRAD genomic libraries. AA-P, MN, GD, JBP, EAV, PHSB, CRC and MIZ performed analyses and discussed results. All coauthors prepared the manuscript.

Corresponding author

Correspondence to Maria Imaculada Zucchi.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by: Alan Carvalho Andrade

Publisher’s Note

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

Electronic Supplementary Material

ESM 1

(DOCX 461 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alves-Pereira, A., Novello, M., Dequigiovanni, G. et al. Genomic Diversity of Three Brazilian Native Food Crops Based on Double-Digest Restriction Site-Associated DNA Sequencing. Tropical Plant Biol. 12, 268–281 (2019). https://doi.org/10.1007/s12042-019-09229-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12042-019-09229-z

Keywords

Navigation