Genomic Diversity of Three Brazilian Native Food Crops Based on Double-Digest Restriction Site-Associated DNA Sequencing
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.
KeywordsBixa orellana Euterpe edulis Manihot esculenta Population genomics SNP
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.
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.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
- Allem AC (2002) The origins and taxonomy of cassava. In: Hillocks RJ, Thresh JM, Bellotti AC (eds) Cassava: biology, production and utilization. CAB International, OxfordGoogle Scholar
- Allendorf FW, Luikart GH, Aitken SN (2013) Conservation and the genetics of populations. Oxford Wiley-Blackwell, OxfordGoogle 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, BelémGoogle 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 CrossRefPubMedPubMedCentralGoogle 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 2:139Google 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 64:1775–1788CrossRefGoogle Scholar
- Donkin RA (1974) Bixa orellana: the eternal shrub. Anthropos 69:33–56Google Scholar
- Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bull 12:11–15Google Scholar
- Gepts P (2004) Crop domestication as a long-term selection experiment. Plant Breed Rev 24:1–44Google Scholar
- Henderson A, Galeano G, Bernal R (1995) Field guide to the palms of the Americas. Princeton University, PrincetonGoogle 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):104–109Google Scholar
- Lebot V (2009) Tropical root and tuber crops: cassava, sweet potato, yams and aroids. Crop production science in horticulture (17). CAB books, CABI, WallingfordGoogle Scholar
- Mantovani A, Morellato LP (2000) Fenologia da floração, frutificação, mudança foliar e aspectos da biologia floral do palmiteiro. Sellowia 49:23–38Google 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, ParisGoogle 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, CambridgeGoogle 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, BrasíliaGoogle 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, BrasíliaGoogle Scholar
- 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
- R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Sandy-Cuen PM, Becerra R (2003) Manejo campesino de recursos naturales. El achiote. BioDiversitas 7:7–11Google Scholar
- Vilares AS, São José AR, Rebouças TNH, Souza IVB (1992) Estudo da biologia floral de urucuzeiro (Bixa orellana L.). Rev Bras Corantes Naturais 1:101–105Google 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):1–11Google Scholar