Abstract
Cassava (Manihot esculenta Crantz) is one of the most important food security crops in the tropics and increasingly being adopted for agro-industrial processing. Genetic improvement of cassava can be enhanced through marker-assisted breeding. For this, appropriate genomic tools are required to dissect the genetic architecture of economically important traits. Here, a genome-wide SNP-based genetic map of cassava anchored in SSRs is presented. An outbreeder full-sib (F1) family was genotyped on two independent SNP assay platforms: an array of 1,536 SNPs on Illumina’s GoldenGate platform was used to genotype a first batch of 60 F1. Of the 1,358 successfully converted SNPs, 600 which were polymorphic in at least one of the parents and was subsequently converted to KBiosciences’ KASPar assay platform for genotyping 70 additional F1. High-precision genotyping of 163 informative SSRs using capillary electrophoresis was also carried out. Linkage analysis resulted in a final linkage map of 1,837 centi-Morgans (cM) containing 568 markers (434 SNPs and 134 SSRs) distributed across 19 linkage groups. The average distance between adjacent markers was 3.4 cM. About 94.2% of the mapped SNPs and SSRs have also been localized on scaffolds of version 4.1 assembly of the cassava draft genome sequence. This more saturated genetic linkage map of cassava that combines SSR and SNP markers should find several applications in the improvement of cassava including aligning scaffolds of the cassava genome sequence, genetic analyses of important agro-morphological traits, studying the linkage disequilibrium landscape and comparative genomics.
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References
Ahn S, Tanksley SD (1993) Comparative linkage maps of the rice and maize genomes. Proc Natl Acad Sci USA 90:7980–7984
Akano AO, Dixon AGO, Mba C, Barrera E, Fregene M (2002) Genetic mapping of a dominant gene conferring resistance to cassava mosaic disease. Theor Appl Genet 105:521–525
Akhunov E, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor Appl Genet 119:507–517
Alves AAA (2002) Cassava botany and physiology. In: Hillocks RJ, Thresh MJ, Bellotti AC (eds) Cassava: biology, production and utilisation. CABI International, Oxford, pp 67–89
Anithakumari AM, Tang J, van Eck HJ, Visser RGF, Leunissen JAM, Vosman B, van der Linden CG (2010) A pipeline for high throughput detection and mapping of SNPs from EST databases. Mol Breed 26:65–75
Appleby N, Edwards D, Batley J (2009) New technologies for ultra-high throughput genotyping in plants. Methods Mol Biol 513:19–39
Bechsgaard J, Bataillon T, Schierup Mh (2004) Uneven segregation of sporophytic self-incompatibility alleles in Arabidopsis lyrata. J Evol Biol 17:554–561
Boonchanawiwat A, Sraphet S, Boonseng O, Lightfoot DA, Triwitayakorn K (2011) QTL underlying plant and first branch height in cassava (Manihot esculenta Crantz). Field Crops Res 121:343–349
Buckler ES, Thornsberry JM (2002) Plant molecular diversity and application to genomics. Curr Opin Plant Biol 5:107–111
Chen X, Xia Z, Fu Y, Lu C, Wang W (2010) Constructing a genetic linkage map using an F1 population of non-inbred parents in cassava (Manihot esculenta Crantz). Plant Mol Biol Report 28:676–683
CIAT (2003) Annual Report IP3. Improved cassava for the developing world. International Centre for Tropical Agriculture (CIAT), pp 8–90, Cali
Dellaporta SL, Wood J, Hicks JR (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21
Edwards D, Forster JW, Cogan NOI, Batley J, Chagne’ D (2010) Single nucleotide polymorphism discovery. In: Oraguzie NC, Rikkerink EHA, Gardiner SE, De Silva HN (eds) Association mapping in plants. Springer, New York, pp 53–76
Elshire R, Glaubitz J, Sun Q, Poland J, Kawamoto K et al (2011) A robust simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. doi:10.1371/journal.pone.0019379
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
Fan JB, Oliphant A, Shen R et al (2003) Highly parallel SNP genotyping. Cold Spring Harb Symp Quant Biol 68:69–78
FAOSTAT (2010) Food and agriculture organizations statistics database. FAO, Rome. http://faostat.fao.org/. Accessed Oct 2010
Ferguson ME, Hearne SJ, Close TJ, Wanamaker S, Moskal WA, Town CD, de Young J, Marri PR, Rabbi IY, de Villiers EP (2011) Identification, validation and high-throughput genotyping of transcribed gene SNPs in cassava. Theor Appl Genetics. doi:10.1007/s00122-011-1739-9
Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374
Fregene M, Angel F, Gomez R, Rodriguez F, Chavarriaga P, Roca W, Tohme J, Bonierbale M (1997) A molecular genetic map of cassava (Manihot esculenta Crantz). Theor Appl Genet 95:431–441
Gunderson KL, Steemers FJ, Lee G, Mendoza LG, Chee MS (2005) A genome-wide scalable SNP genotyping assay using microarray technology. Nat Genet 37:549–554
Hackett CA, Wachira FN, Paul S, Powell W, Waugh R (2000) Construction of a genetic linkage map for Camellia sinensis (tea). Heredity 85:346–355
Hippolyte I, Bakry F, Seguin M, Gardes L, Rivallan R, Risterucci AM et al (2010) A saturated SSR/DArT linkage map of Musa acuminata addressing genome rearrangements among bananas. BMC Plant Biol 10:65
Hwang TY, Sayama T, Takahashi M et al (2009) High-density integrated linkage map based on SSR markers in soybean. DNA Res 16:213–225
Jansson C, Westerbergh A, Zhang J, Hud X, Sun C (2009) Cassava, a potential biofuel crop in (the) People’s Republic of China. Appl Energy 86:95–99
Jorge V, Fregene MA, Duque MC, Bonierbale MW, Tohme J, Verdier V (2000) Genetic mapping of resistance to bacterial blight disease in cassava (Manihot esculenta Crantz). Theor Appl Genet 101:865–872
Kanju E, Mkamilo G, Mgoo V, Ferguson M (2010) Statistical evidence linking the zigzag stem habit with tolerance to cassava brown streak disease. ROOTS 12:4–6
Kizito BE, Ronnberg-Wastljung AC, Egwang T, Gullberg U, Fregene M, Westerbergh A (2007) Quantitative trait loci controlling cyanogenic glucoside and dry matter content in cassava (Manihot esculenta Crantz) roots. Hereditas 144:129–136
Kunkeaw S, Tangphatsornruang S, Smith DR, Triwitayakorn K (2010) Genetic linkage map of cassava (Manihot esculenta Crantz) based on AFLP and SSR markers. Plant Breed. doi:10.1111/j.1439-0523.2009.01623.x
Kunkeaw S, Yoocha T, Sraphet S, Boonchanawiwat A, Boonseng O, Lightfoot DA, Triwitayakorn K, Tangphatsornruang S (2011) Construction of a genetic linkage map using simple sequence repeat markers from expressed sequence tags for cassava (Manihot esculenta Crantz). Mol Breed 27:67–75
Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199
Leppälä J, Bechsgaard JS, Schierup MH, Savolainen O (2008) Transmission ratio distortion in Arabidopsis lyrata: effects of population divergence and the S-locus. Heredity 100:71–78
Lopez CE, Quesada-Ocampo LM, Bohorquez A, Duque MC, Vargas J, Tohme J, Verdier V (2007) Mapping EST-derived SSRs and ESTs involved in resistance to bacterial blight in Manihot esculenta. Genome 50:1078–1088
Lu H, Romero-Severson J, Bernardo R (2002) Chromosomal regions associated with segregation distortion in maize. Theor Appl Genet 105:622–628
Meuwissen TH, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829
Okogbenin E, Fregene M (2003) Genetic mapping of QTLs affecting productivity and plant architecture in a full-sib cross from non-inbred parents in cassava (Manihot esculenta Crantz). Theor Appl Genet 107:1452–1462
Okogbenin E, Marin J, Fregene M (2006) An SSR-based molecular genetic map of cassava. Euphytica 147:433–440
Okogbenin E, Marin J, Fregene M (2008) QTL analysis for early yield in a pseudo F2 population of cassava. Afr J Biotechnol 7:131–138
Pasquet RS, Peltier A, Hufford MB, Oudin E, Saulnier J, Paul L, Knudsen JT, Herren HR, Gepts P (2008) Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. PNAS 105:13456–13461
Pereira MG, Lee M, Bramel-Cox P, Woodman W, Doebley J, Whitkus R (1994) Construction of an RFLP map in sorghum and comparative mapping in maize. Genome 37:236–243
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Prochnik S, Marri PR, Desany B, Rabinowicz PD, Kodira C, Mohiuddin M, Rodriguez F, Fauquet C, Tohme J, Harkins T, Rokhsar DS, Rounsley S (2011) The cassava genome: current progress, future directions. Tropical Plant Biol. doi:10.1007/s12042-011-9088-z
Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100
Rojas MC, Pérez JC, Ceballos H, Baena D, Morante N, Calle F (2009) Analysis of inbreeding depression in eight S1 cassava families. Crop Sci 49:543–548
Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:234
Shen R, Fan J-B, Campbell D, Chang W, Chen J, Doucet D, Yeakley J, Bibikova M, Wickham Garcia E, McBride C, Steemers F, Garcia F, Kermani BG, Gunderson K, Oliphant A (2005) High-throughput SNP genotyping on universal bead arrays. Mutat Res 573:70–82
Sraphet S, Boonchanawiwat A, Thanyasiriwat T, Boonseng O, Tabata S, Sasamoto S, Shirasawa K, Isobe S, Lightfoot DA, Tangphatsornruang S, Triwitayakorn K (2011) SSR and EST-SSR-based genetic linkage map of cassava (Manihot esculenta Crantz). Theor Appl Genet 122:1161–1170
Swanson-Wagner RA, Eichtenn SR, Kumari S, Tiffin P, Stein JC, Ware D, Springer NM (2010) Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res. doi:10.1101/gr.109165.110
Syvänen AC (2001) Accessing genetic variation: genotyping single nucleotide polymorphisms. Nat Rev Genet 2:930–942
Syvänen AC (2005) Toward genome-wide SNP genotyping. Nat Genet 37:5–10
Tavassolian I, Rabie G, Gregory D, Mnejja M, Wirthensohn MG, Hunt PW, Gibson JB, Ford CM, Sedgley M, Wu S (2010) Construction of an almond linkage map in an Australian population Nonpareil × Lauranne. BMC Genomics 11:551
Thresh JM (2006) Control of tropical plant virus diseases. Adv Virus Res 67:245–295
Ubi BE, Fujimori M, Mano Y, Komatsu T (2004) A genetic linkage map of rhodesgrass based on an F1 pseudo-testcross population. Plant Breed 123:247–253
Van Ooijen JW (2006) JoinMap4. Software for the calculation of genetic linkage maps in experimental populations Kyazma BV, Wageningen
Van Ooijen JW, Voorrips RE (2001) JoinMap® version 3.0: software for the calculation of genetic linkage maps. Plant Research International, Wageningen
Whankaew S, Poopear S, Kanjanawattanawong S, Tangphatsornruang S, Boonseng O, Lightfoot DA, Triwitayakorn K (2011) A genome scan for quantitative trait loci affecting cyanogenic potential of cassava root in an outbred population. BMC Genomics 12:266
Wydra K, Zinsou V, Jorge V, Verdier V (2004) Identification of pathotypes of Xanthomonas axonopodis pv. manihotis in Africa and detection of quantitative trait loci and markers for resistance to bacterial blight of cassava. Phytopathology 94:1084–1093
Xian-Liang S, Xue-Zhen S, Tian-Zhen S (2006) Segregation distortion and its effect on genetic mapping in plants. Chin J Agric Biotechnol 3:163–169
Xu Y, Zhu L, Xiao J, Huang N, McCouch SR (1997) Chromosomal regions associated with segregation distortion of molecular markers in F2, backcross, double haploid, and recombinant inbred populations in rice (Oryza sativa L.). Mol Gen Genet 253:535–545
Acknowledgments
The authors appreciate the financial support from the BioSciences eastern and central Africa Network (BecANet), the Generation Challenge Program (GCP) and the International Institute of Tropical Agriculture (IITA). We would like to thank Jim Lorenzen of IITA and Steve Rounsley (University of Arizona and Dow AgroSciences) for the fruitful discussions that led to the improvement of the manuscript. We sincerely thank the two anonymous reviewers and the associated editor for their useful comments that has also led to further improvement of this paper.
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Communicated by A. Bervillé.
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Online Resource 1 Comparison of order of markers of the present one-step map and the SSR-based map of Whankaew et al. (2011) shows clear co-linearity in the two linkage maps (PDF 106 kb)
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Rabbi, I.Y., Kulembeka, H.P., Masumba, E. et al. An EST-derived SNP and SSR genetic linkage map of cassava (Manihot esculenta Crantz). Theor Appl Genet 125, 329–342 (2012). https://doi.org/10.1007/s00122-012-1836-4
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DOI: https://doi.org/10.1007/s00122-012-1836-4