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Genome survey and development of 18 microsatellite markers to assess genetic diversity in Spondias tuberosa Arruda Câmara (Anacardiaceae) and cross-amplification in congeneric species

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Abstract

Spondias tuberosa Arr. Cam belongs to the Anacardiaceae family, an economically important family of plants whose fruits are consumed by humans and animals. The aim of this study was to develop microsatellite markers using sequences from high-throughput sequencing and a magnetic bead enrichment method. The sequences were used to obtain contigs with a minimum of 500 nucleotides using Ray software and the mining of the simple sequence repeats (SSR) was performed with Phobos software, while the primers were designed by Primer3. We developed 18 polymorphic nuclear microsatellite markers and successfully cross-amplified them to three Spondias species. In S. tuberosa, the alleles ranged from 2 to 5 for each locus and Hardy–Weinberg equilibrium was found for 16 loci, with an expected and observed heterozygosity at 0.095–0.755 and 0.1–0.75, respectively. Cross-transferability was obtained for all loci in S. bahiensis, S. dulcis and S. purpurea. We concluded that the microsatellite markers developed in this study are useful in genetic population and conservation studies, as well as for investigating the hybrid origins of Spondias species.

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References

  1. Ambreen H, Kumar S, Variath MT et al (2015) Development of genomic microsatellite markers in Carthamus tinctorius L. (safflower) using next generation sequencing and assessment of their cross-species transferability and utility for diversity analysis. PLoS ONE 10:1–22. https://doi.org/10.1371/journal.pone.0135443

    Article  CAS  Google Scholar 

  2. An J, Yin M, Zhang Q et al (2017) Genome survey sequencing of Luffa cylindrica L. and microsatellite high resolution melting (SSR-HRM) analysis for genetic relationship of luffa genotypes. Int J Mol Sci 8(9):1942. https://doi.org/10.3390/ijms18091942

    Article  CAS  Google Scholar 

  3. Balbino E, Caetano B, Almeida C (2018) Phylogeographic structure of Spondias tuberosa Arruda Câmara (Anacardiaceae): seasonally dry tropical forest as a large and continuous refuge. Tree Genet Genomes 14(5):67. https://doi.org/10.1007/s11295-018-1279-4

    Article  Google Scholar 

  4. Billotte N, Lagoda PJR, Risterucci AM, Baurens FC (1999) Microsatelliteenriched libraries: applied methodology for the development of SSR markers in tropical crops. Fruits 54:277–288

    CAS  Google Scholar 

  5. Boisvert S, Raymond F, Godzaridis E et al (2012) Ray meta: scalable de novo metagenome assembly and profiling. Genome Biol 13:R122. https://doi.org/10.1186/gb-2012-13-12-r122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Espíndola ACM, Almeida CCS, Carvalho NSG, Roza MLA (2004) Diâmetro do caule e método de enxertia na formação de mudas de umbuzeiro (Spondias tuberosa Arr. Cam.). Rev Bras Agrociência 10:371–372

    Google Scholar 

  7. Ferreira ME, Grattapaglia D (1998) Introdução ao uso de marcadores moleculares em análise genética. Embrapa, Brasília

    Google Scholar 

  8. Gruber B, Adamack A (2017) PopGenReport v3.0.0. https://github.com/green-striped-gecko/PopGenReport. A simple framework to analyse population and landscape genetic data

  9. Hodel RGJ, Segovia-Salcedo MC, Landis JB et al (2016) The report of my death was an exaggeration: a review for researchers using microsatellites in the 21st century. Appl Plant Sci 4:1600025. https://doi.org/10.3732/apps.1600025

    Article  Google Scholar 

  10. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129

    Article  CAS  Google Scholar 

  11. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291. https://doi.org/10.1093/bioinformatics/btm091

    Article  CAS  PubMed  Google Scholar 

  12. Kumar M, Choi J-Y, Kumari N et al (2015) Molecular breeding in brassica for salt tolerance: importance of microsatellite (SSR) markers for molecular breeding in brassica. Front Plant Sci 6:1–13. https://doi.org/10.3389/fpls.2015.00688

    Article  Google Scholar 

  13. Lira Júnior JS, Musser RS, Melo EA, Maciel MIS, Lederman IE, Santos VP (2005) Caracterização física e físico-química de frutos de cajá-umbu (Spondias spp.). Ciências Tecnol Aliment 25:757–761. https://doi.org/10.1590/S0101-2061200500040002

    Article  Google Scholar 

  14. Lorenzi H (2008) Árvores Brasileiras: manual de identificação e cultivo de plantas arbóreas do Brasil. Nova Odessa, São Paulo

    Google Scholar 

  15. Machado MC, Carvalho PCL, Berg CVD (2015) Domestication, hybridization, speciation, and the origins of an economically import ant tree crop of Spondias (anacardiaceae) from the Brazilian caatinga dry forest. Neodiversity 8:8–49

    Article  Google Scholar 

  16. Mayer C (2008) Phobos, a tandem repeat search tool for complete genomes, version 3.3.12. Available from: http://www.ruhr-uni-bochum.de/ecoevo/cm/cm_phobos.htm

  17. Mitchell JD, Daly DC (2015) A revision of Spondias L. (Anacardiaceae) in the nzeotropics. PhytoKeys 55:1–92

    Article  Google Scholar 

  18. Motalebipour EZ, Kafkas S, Khodaeiaminjan M et al (2016) Genome survey of pistachio (Pistacia vera L.) by next generation sequencing: development of novel SSR markers and genetic diversity in Pistacia species. BMC Genomics 17:1–14. https://doi.org/10.1186/s12864-016-3359-x

    Article  Google Scholar 

  19. Moura RF, Dawson DA, Nogueira DM (2017) The use of microsatellite markers in neotropical studies of wild birds: a literature review. Ann Acad Bras Cienc 89:145–154. https://doi.org/10.1590/0001-3765201620160378

    Article  Google Scholar 

  20. Nobre LLM, Santos JDO, Leite R, Almeida C (2018) Phylogenomic and single nucleotide polymorphism analyses revealed the hybrid origin of Spondias bahiensis (family Anacardiaceae): de novo genome sequencing and comparative genomics. Genet Mol Biol 41(4):878–883. https://doi.org/10.1590/1678-4685-gmb-2017-0256

    Article  PubMed  PubMed Central  Google Scholar 

  21. Paradis E (2010) Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420

    Article  CAS  PubMed  Google Scholar 

  22. Portis E, Portis F, Valente L et al (2016) A genome-wide survey of the microsatellite content of the globe artichoke genome and the development of a web-based database. PLoS ONE 11:1–20. https://doi.org/10.1371/journal.pone.0162841

    Article  CAS  Google Scholar 

  23. Satya P, Paswan PK, Ghosh S et al (2016) Confamiliar transferability of simple sequence repeat (SSR) markers from cotton (Gossypium hirsutum L.) and jute (Corchorus olitorius L.) to twenty two malvaceous species. 3 Biotech 6:1–7. https://doi.org/10.1007/s13205-016-0392-z

    Article  Google Scholar 

  24. Silva JN, Bezerra da Costa A, Silva JV, Almeida C (2015) DNA barcoding and phylogeny in neotropical species of the genus Spondias. Biochem Syst Ecol 61:240–243. https://doi.org/10.1016/j.bse.2015.06.005

    Article  CAS  Google Scholar 

  25. Silva RA, Souza G, Lemos LSL et al (2017) Genome size, cytogenetic data and transferability of EST-SSRs markers in wild and cultivated species of the genus Theobroma L. (Byttnerioideae, Malvaceae). PLoS ONE 12:1–15. https://doi.org/10.1371/journal.pone.0170799

    Article  CAS  Google Scholar 

  26. Souza VC, Lorenzi H (2005) Botânica Sistemática: guia ilustrado para identificação das famílias de Angiospermas da flora brasileira, baseado em APG II. Instituto Plantarum, São Paulo

    Google Scholar 

  27. Sumathi M, Yasodha R (2014) Microsatellite resources of eucalyptus: current status and future perspectives. Bot Stud 55:1–16. https://doi.org/10.1186/s40529-014-0073-3

    Article  CAS  Google Scholar 

  28. Taheri S, Lee Abdullah T, Yusop M et al (2018) Mining and development of novel SSR markers using next generation sequencing (NGS) data in plants. Molecules 23:399. https://doi.org/10.3390/molecules23020399

    Article  CAS  PubMed Central  Google Scholar 

  29. Vale AA, Lau BL, Leal BSS et al (2016) Development and transferability of microsatellite markers in Habenaria nuda and H. repens (Orchidaceae). Rev Braz Bot 39:387–392. https://doi.org/10.1007/s40415-015-0214-2

    Article  Google Scholar 

  30. Vieira MLC, Santini L, Diniz AL, de Munhoz CF (2016) Microsatellite markers: what they mean and why they are so useful. Genet Mol Biol 39:312–328. https://doi.org/10.1590/1678-4685-GMB-2016-0027

    Article  PubMed  PubMed Central  Google Scholar 

  31. Wanderley AM, Vasconcelos S, Huettel B et al (2017) Development of 15 SSR polymorphic markers for the endangered Ameroglossum pernambucense Eb. Fischer, S. Vogel & A. V. Lopes (Scrophulariaceae), and cross-transferability in congeneric taxa. Rev Braz Bot 40:1007–1011. https://doi.org/10.1007/s40415-017-0410-3

    Article  Google Scholar 

  32. Wei X, Wang L, Zhang Y et al (2014) Development of simple sequence repeat (SSR) markers of sesame (Sesamum indicum) from a genome survey. Molecules 19:5150–5162. https://doi.org/10.3390/molecules19045150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The Federal University of Alagoas provided laboratories and scientific support and the Fundação de Apoio à Pesquisa de Alagoas (FAPEAL) provided funding for this project.

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  1. Laboratório de Recursos Genéticos, Campus de Arapiraca, Universidade Federal de Alagoas, Avenida Manoel Severino Barbosa s/n, Rodovia AL 115, km 6,5. Bairro Bom Sucesso, Arapiraca, AL, Brazil

    Eliane Balbino, Gleica Martins, Suzyanne Morais & Cicero Almeida

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  1. Eliane Balbino
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Correspondence to Cicero Almeida.

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Balbino, E., Martins, G., Morais, S. et al. Genome survey and development of 18 microsatellite markers to assess genetic diversity in Spondias tuberosa Arruda Câmara (Anacardiaceae) and cross-amplification in congeneric species. Mol Biol Rep 46, 3511–3517 (2019). https://doi.org/10.1007/s11033-019-04768-w

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  • DOI: https://doi.org/10.1007/s11033-019-04768-w

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