Abstract
The increasing volume of genomic data on the Phaseolus vulgaris species have contributed to its importance as a model genetic species and positively affected the investigation of other legumes of scientific and economic value. To expand and gain a more in-depth knowledge of the common bean genome, the ends of a number of bacterial artificial chromosome (BAC) were sequenced, annotated and the presence of repetitive sequences was determined. In total, 52,270 BESs (BAC-end sequences), equivalent to 32 Mbp (~6 %) of the genome, were processed. In total, 3,789 BES-SSRs were identified, with a distribution of one SSR (simple sequence repeat) per 8.36 kbp and 2,000 were suitable for the development of SSRs, of which 194 were evaluated in low-resolution screening. From 40 BES-SSRs based on long motifs SSRs (≥trinucleotides) analyzed in high-resolution genotyping, 34 showed an equally good amplification for the Andean and for the Mesoamerican genepools, exhibiting an average gene diversity (H E) of 0.490 and 5.59 alleles/locus, of which six classified as Class I showed a H E ≥ 0.7. The PCoA and structure analysis allowed to discriminate the gene pools (K = 2, FST = 0.733). From the 52,270 BESs, 2 % corresponded to transcription factors and 3 % to transposable elements. Putative functions for 24,321 BESs were identified and for 19,363 were assigned functional categories (gene ontology). This study identified highly polymorphic BES-SSRs containing tri- to hexanucleotides motifs and bringing together relevant genetic characteristics useful for breeding programs. Additionally, the BESs were incorporated into the international genome-sequencing project for the common bean.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402
Asfaw A, Blair MW, Struik PC (2012) Multienvironment quantitative trait loci analysis for photosynthate acquisition, accumulation, and remobilization traits in common bean under drought stress. G3 (Bethesda) 2(5):579–595. doi:10.1534/g3.112.002303
Biswas MK, Chai L, Mayer C, Xu Q, Guo W, Deng X (2012) Exploiting BAC-end sequences for the mining, characterization and utility of new short sequences repeat (SSR) markers in Citrus. Mol Biol Rep 39(5):5373–5386. doi:10.1007/s11033-011-1338-5
Blair MW, Hurtado N (2013) EST-SSR markers from five sequenced cDNA libraries of common bean (Phaseolus vulgaris L.) comparing three bioinformatic algorithms. Mol Ecol Resour 13(4):688–695. doi:10.1111/1755-0998.12099
Blair MW, Pedraza F, Buendia HF, Gaitán-Solís E, Beebe SE, Gepts P, Tohme J (2003) Development of a genome-wide anchored microsatellite map for common bean (Phaseolus vulgaris L.). Theor Appl Genet 107:1362–1374. doi:10.1007/s00122-003-1398-6
Blair MW, Astudillo C, Rengifo J, Beebe SE, Graham R (2011a) QTL analyses for seed iron and zinc concentrations in an intra-genepool population of Andean common beans (Phaseolus vulgaris L.). Theor Appl Genet 122(3):511–521. doi:10.1007/s00122-010-1465-8
Blair MW, Hurtado N, Chavarro CM, Muñoz-Torres MC, Giraldo MC, Pedraza F, Tomkins J, Wing R (2011b) Gene-based SSR markers for common bean (Phaseolus vulgaris L.) derived from root and leaf tissue ESTs: an integration of the BMc series. BMC Plant Biol 11:50. doi:10.1186/1471-2229-11-50
Blair MW, Hurtado N, Sharma P (2012a) New gene-derived simple sequence repeat markers for common bean (Phaseolus vulgaris L.). Mol Ecol Resour 12:661–668. doi:10.1111/j.1755-0998.2012.03136.x
Blair MW, Soler A, Cortés AJ (2012b) Diversification and population structure in common beans (Phaseolus vulgaris L.). PLoS ONE 7(11):e49488. doi:10.1371/journal.pone.0049488
Blair MW, Cortés AJ, Penmetsa RV, Farmer A, Carrasquilla-Garcia N, Cook DR (2013) A high-throughput SNP marker system for parental polymorphism screening, and diversity analysis in common bean (Phaseolus vulgaris L.). Theor Appl Genet 126:535–548. doi:10.1007/s00122-012-1999-z
Bohra A, Dubey A, Saxena RK et al (2011) Analysis of BAC-end sequences (BESs) and development of BES-SSR markers for genetic mapping and hybrid purity assessment in pigeonpea (Cajanus spp.). BMC Plant Biol 11:56. doi:10.1186/1471-2229-11-56
Broughton WJ, Hernández G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128. doi:10.1023/A:1024146710611
Burle ML, Fonseca JR, Kami JA, Gepts P (2010) Microsatellite diversity and genetic structure among common bean (Phaseolus vulgaris L.) landraces in Brazil, a secondary center of diversity. Theor Appl Genet 121:801–813. doi:10.1007/s00122-010-1350-5
Byrne N, Marquez-Garcia MI, Smith DS, Moran GF (1996) Conservation and genetic diversity of microsatellite loci in the genus Eucalyptus. Aust J Bot 44(3):331–341. doi:10.1071/BT9960331
Cannon SB, May GD, Jackson SA (2009) Three sequenced legume genomes and many crop species: rich opportunities for translational genomics. Plant Physiol 151(3):970–977
Cardoso PCB, Veiga MM, Menezes IPP, Valdisser PAMR, Borba TCO, Melo LC, Del Peloso MJ, Brondani C, Vianello RP (2013) Molecular characterization of high performance inbred lines of Brazilian common beans. Genet Mol Res 12(4):5467–5484. doi:10.4238/2013
Cardoso PCB, Brondani C, Menezes IPP, Valdisser PAMR, Borba TCO, Del Peloso MJ, Vianello RP (2014) Discrimination of common bean cultivars using multiplexed microsatellite markers. Genet Mol Res 13(1):1964–1978. doi:10.4238/2014.March.24.1
Castelo AT, Martins W, Gao GR (2002) TROLL—tandem repeat occurrence locator. Bioinformatics 18(4):634–636
Chen M, Wu J, Wang L, Zhang X, Blair MW, Jia J, Wang S (2014) Development of mapped simple sequence repeat markers from common bean (Phaseolus vulgaris L.) based on genome sequences of a Chinese landrace and diversity evaluation. Mol Breeding 33(2):489–496. doi:10.1007/s11032-013-9949-2
Cho YG, Ishii T, Temnykh S, Chen X, Lipovich L, McCouch SR, Park WD, Ayres N, Cartinhour S (2000) Diversity of microsatellites derived from genomic libraries and GenBank sequences in rice (Oryza sativa L.). Theor Appl Genet 100(5):713–722
Choi H, Kim D, Uhm T, Limpens E, Lim H, Mun JH, Kalo P, Penmetsa RV, Seres A, Kulikova O, Roe BA, Bisseling T, Kiss GB, Cook DR (2004) A sequence-based genetic map of Medicago truncatula and comparison of marker colinearity with M. sativa. Genetics 166(3):1463–1502
Chou H, Holmes MH (2001) DNA sequence quality trimming and vector removal. Bioinformatics 17(12):1093–1104
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676. doi:10.1093/bioinformatics/bti610
Córdoba JM, Chavarro C, Schlueter JA, Jackson SA, Blair MW (2010) Integration of physical and genetic maps of common bean through BAC-derived microsatellite markers. BMC Genom 11:436. doi:10.1186/1471-2164-11-436
Cortés AJ, Chavarro MC, Blair MW (2011) SNP marker diversity in common bean (Phaseolus vulgaris L.). Theor Appl Genet 123(5):827–845. doi:10.1007/s00122-011-1630-8
de la Chaux N, Tsuchimatsu T, Shimizu KK, Wagner A (2012) The predominantly selfing plant Arabidopsis thaliana experienced a recent reduction in transposable element abundance compared to its outcrossing relative Arabidopsis lyrata. Mob DNA 3(1):2. doi:10.1186/1759-8753-3-2
Dereeper A, Guyot R, Tranchant-Dubreuil C et al (2013) BAC-end sequences analysis provides first insights into coffee (Coffea canephora P.) genome composition and evolution. Plant Mol Biol 83(3):177–189. doi:10.1007/s11103-013-0077-5
Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 131(13):900–910. doi:10.1104/pp.102.018150.groups
Du J, Grant D, Tian Z, Nelson RT, Zhu L, Shoemaker RC, Ma J (2010) SoyTEdb: a comprehensive database of transposable elements in the soybean genome. BMC Genom 11:113. doi:10.1186/1471-2164-11-113
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conser Genet Resour 4(2):359–361. doi:10.1007/s12686-011-9548-7
Eustice M, Yu Q, Lai CW, Hou S, Thimmapuram J, Liu L, Alam M, Moore PH, Presting GG, Ming R (2008) Development and application of microsatellite markers for genomic analysis of papaya. Tree Genet Genomes 4(2):333–341. doi:10.1007/s11295-007-0112-2
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. doi:10.1111/j.1365-294X.2005.02553.x
Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8(3):175–185. doi:10.1101/gr.8.3.175
FAOSTAT (2009) Food and Agriculture Organization of the United Nations—Statistical Database. http://faostat.fao.org/. Accessed 10 Oct 2013
Frei dit Frey N, Mbengue M, Kwaaitaal M et al (2012) Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. Plant Physiol 159(2):798–809. doi:10.1104/pp.111.192575
Galeano CH, Fernandez AC, Franco-Herrera N, Cichy KA, McClean PE, Vanderleyden J, Blair MW (2011) Saturation of an intra-gene pool linkage map: towards a unified consensus linkage map for fine mapping and synteny analysis in common bean. PLoS ONE 6(12):e28135. doi:10.1371/journal.pone.0028135
Galeano CH, Cortés AJ, Fernández AC, Soler Á, Franco-Herrera N, Makunde G, Vanderleyden J, Blair MW (2012) Gene-based single nucleotide polymorphism markers for genetic and association mapping in common bean. BMC Genet 13:48. doi:10.1186/1471-2156-13-48
Garcia RAV, Rangel PN, Brondani C, Martins WS, Melo LC, Carneiro MS, Borba TC, Brondani RP (2011) The characterization of a new set of EST-derived simple sequence repeat (SSR) markers as a resource for the genetic analysis of Phaseolus vulgaris. BMC Genet 12:41. doi:10.1186/1471-2156-12-41
Gepts P, Beavis WD, Brummer EC, Shoemaker RC, Stalker HT, Weeden NF, Young ND (2005) Legumes as a model plant family genomics for food and feed report of the cross-legume advances through genomics conference. Plant Physiol 137(4):1228–1235. doi:10.1104/pp.105.060871
Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and E. urophylla using a pseudo-testcross strategy and RAPD markers. Genetics 137(4):1121–1137
Hanai LR, de Campos T, Camargo LE et al (2007) Development, characterization, and comparative analysis of polymorphism at common bean SSR loci isolated from genic and genomic sources. Genome 50(3):266–277. doi:10.1139/G07-007
Hanai LR, Santini L, Camargo LE, Fungaro MH, Gepts P, Tsai SM, Vieira ML (2010) Extension of the core map of common bean with EST-SSR, RGA, AFLP, and putative functional markers. Mol Breed 25(1):25–45. doi:10.1007/s11032-009-9306-7
Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9(9):868–877. doi:10.1101/gr.9.9.868
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(14):1801–1806. doi:10.1093/bioinformatics/btm233
Kalavacharla V, Liu Z, Meyers BC, Thimmapuram J, Melmaiee K (2011) Identification and analysis of common bean (Phaseolus vulgaris L.) transcriptomes by massively parallel pyrosequencing. BMC Plant Biol 11:135. doi:10.1186/1471-2229-11-135
Kami J, Poncet V, Geffroy V, Gepts P (2006) Development of four phylogenetically-arrayed BAC libraries and sequence of the APA locus in Phaseolus vulgaris. Theor Appl Genet 112(6):987–998. doi:10.1007/s00122-005-0201-2
Kang W, Hérbert JM (2012) A Sox2 BAC transgenic approach for targeting adult neural stem cells. PLoS ONE 7(11):e49038. doi:10.1371/journal.pone.0049038
Katti MV, Ranjekar PK, Gupta VS (2001) Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 18(7):1161–1167
Kim H, San Miguel P, Nelson W, Collura K, Wissotski M, Walling JG, Kim JP, Jackson SA, Soderlund C, Wing RA (2007) Comparative physical mapping between Oryza sativa (AA genome type) and O. punctata (BB genome type). Genetics 176(1):379–390. doi:10.1534/genetics.106.068783
Kim C, Lee TH, Compton RO, Robertson JS, Pierce GJ, Paterson AH (2013) A genome-wide BAC end-sequence survey of sugarcane elucidates genome composition, and identifies BACs covering much of the euchromatin. Plant Mol Biol 81(1–2):139–147. doi:10.1007/s11103-012-9987-x
Kleine T (2012) Arabidopsis thaliana mTERF proteins: evolution and functional classification. Front Plant Sci 3:233. doi:10.3389/fpls.2012.00233
Kriedt RA, Cruz GMQ, Bonatto SL, Freitas LB (2014) Novel transposable elements in solanaceae: evolutionary relationships among Tnt1-related sequences in wild petunia species. Plant Mol Biol Rep 32(1):142–152. doi:10.1007/s11105-013-0626-8
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645. doi:10.1101/gr.092759.109
Kwak M, Gepts P (2009) Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae). Theor Appl Genet 118(5):979–992. doi:10.1007/s00122-008-0955-4
Lawson MJ, Zhang L (2006) Distinct patterns of SSR distribution in the Arabidopsis thaliana and rice genomes. Genome Biol 7(2):R14. doi:10.1186/gb-2006-7-2-r14
Leclercq S, Rivals E, Jarne P (2007) Detecting microsatellites within genomes: significant variation among algorithms. BMC Bioinformatics 8:125. doi:10.1186/1471-2105-8-125
Li YC, Fahima T, Röder MS, Kirzhner VM, Beiles A, Korol AB, Nevo E (2003) Genetic effects on microsatellite diversity in wild emmer wheat (Triticum dicoccoides) at the Yehudiyya microsite, Israel. Heredity 90(2):150–156. doi:10.1038/sj.hdy.6800190
Martin-Cabrejas MA, Esteban RM, Perez P, Maina G, Waldron KW (1997) Changes in psyscochimical properties of dry beans (Phaseolus vulgaris L.) during long term storage. J Agric Food Chem 47:3223–3227
Martins W, de Sousa D, Proite K, Guimarães P, Moretzsohn M, Bertioli D (2006) New softwares for automated microsatellite marker development. Nucleic Acids Res 34(4):e31. doi:10.1093/nar/gnj030
McClean PE, Mamidi S, McConnell M, Chikara S, Lee R (2010) Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genom 11:184. doi:10.1186/1471-2164-11-184
Mitchell DC, Lawrence FR, Hartman TJ, Curran JM (2009) Consumption of dry beans, peas, and lentils could improve diet quality in the US population. J Am Diet Assoc 109(5):909–913
Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30(2):194–200. doi:10.1038/ng822
Mun JH, Kim DJ, Choi HK, Gish J, Debellé F, Mudge J, Denny R, Endré G, Saurat O, Dudez AM, Kiss GB, Roe B, Young ND, Cook DR (2006) Distribution of microsatellites in the genome of Medicago truncatula: a resource of genetic markers that integrate genetic and physical maps. Genetics 172(4):2541–2555. doi:10.1534/genetics.105.054791
Noguero M, Atif RM, Ochatt S, Thompson RD (2013) The role of the DNA-binding One Zinc Finger (DOF) transcription factor family in plants. Plant Sci 209:32–45. doi:10.1016/j.plantsci.2013.03.016
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28(19):2537–2539. doi:10.1093/bioinformatics/bts460
Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38(1):D822–D827. doi:10.1093/nar/gkp805
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Ragupathy R, Rathinavelu R, Cloutier S (2011) Physical mapping and BAC-end sequence analysis provide initial insights into the flax (Linum usitatissimum L.) genome. BMC Genom 12:217. doi:10.1186/1471-2164-12-217
Ramírez M, Graham MA, Blanco-Lopez L, Silvente S, Medrano-Soto A, Blair MW, Hernandez G, Vance CP, Lara M (2005) Sequencing and analysis of common bean ESTs. Building a foundation for functional genomics. Plant Physiol 137(4):1211–1227
Renwick A, Davison L, Spratt H, King JP, Kimmel M (2001) DNA dinucleotide evolution in humans : fitting theory to facts. Genetics 159(2):737–747
Roberti M, Polosa PL, Bruni F, Manzari C, Deceglie S, Gadaleta MN, Cantatore P (2009) The MTERF family proteins: mitochondrial transcription regulators and beyond. Biochim Biophys Acta 1787(5):303–311. doi:10.1016/j.bbabio.2009.01.013
Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x
Rozen S, Skaletsky H (2000) Primer3 for general users and for biologist programmers. In: Misener S, Krawetz SA (eds) Bioinformatics methods and protocols. Methods molecular biology, vol 132. The Humana Press Inc., Totowa, New Jersey, pp 365–386
Saini N, Shultz J, Lightfoot DA (2008) Re-annotation of the physical map of Glycine max for polyploid-like regions by BAC end sequence driven whole genome shotgun read assembly. BMC Genom 9:323. doi:10.1186/1471-2164-9-323
Schlueter JA, Goicoechea JL, Collura K et al (2008) BAC-end sequence analysis and a draft physical map of the common bean (Phaseolus vulgaris L.) genome. Trop Plant Biol 1(1):40–48. doi:10.1007/s12042-007-9003-9
Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183. doi:10.1038/nature08670
Schmutz J, McClean PE, Mamidi S et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46(7):707–713. doi:10.1038/ng.3008
Shoemaker RC, Grant D, Olson T et al (2008) Microsatellite discovery from BAC end sequences and genetic mapping to anchor the soybean physical and genetic maps. Genome 51(4):294–302. doi:10.1139/G08-010
Shultz JL, Kazi S, Bashir R, Afzal JA, Lightfoot DA (2007) The development of BAC-end sequence-based microsatellite markers and placement in the physical and genetic maps of soybean. Theor Appl Genet 114(6):1081–1090. doi:10.1007/s00122-007-0501-9
Sonah H, Deshmukh RK, Sharma A, Singh VP, Gupta DK, Gacche RN, Rana JC, Singh NK, Sharma TR (2011) Genome-wide distribution and organization of microsatellites in plants: an insight into marker development in Brachypodium. PLoS ONE 6(6):e21298. doi:10.1371/journal.pone.0021298
Staden R, Beal KF, Bonfield JK (1999) The staden package, 1998. In: Misener S, Krawetz SA (ed) Bioinformatics methods and protocols. Methods molecular biology, vol 132. The Humana Press Inc., Totowa, New Jersey, pp 115–130
Tautz D (1989) Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res 17(16):6463–6471. doi:10.1093/nar/17.16.6463
Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11(8):1441–1452. doi:10.1101/gr.184001
Thudi M, Bohra A, Nayak SN et al (2011) Novel SSR markers from BAC-end sequences, DArT arrays and a comprehensive genetic map with 1,291 marker loci for chickpea (Cicer arietinum L.). PLoS ONE 6(11):e27275. doi:10.1371/journal.pone.0027275
Tóth G, Gáspári Z, Jurka J (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res 10(7):967–981. doi:10.1101/gr.10.7.967
Vallone PM, Butler JM (2004) AutoDimer: a screening tool for primer-dimer and hairpin structures. Biotechniques 37(2):226–231
Varshney RK, Song C, Saxena RK et al (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31(3):240–246. doi:10.1038/nbt.2491
Victoria FC, Maia LC, de Oliveira AC (2011) In silico comparative analysis of SSR markers in plants. BMC Plant Biol 11:15. doi:10.1186/1471-2229-11-15
Wang H, Penmetsa RV, Yuan M et al (2012) Development and characterization of BAC-end sequence derived SSRs, and their incorporation into a new higher density genetic map for cultivated peanut (Arachis hypogaea L.). BMC Plant Biol 12:10. doi:10.1186/1471-2229-12-10
Wang Z, Yan H, Fu X, Li X, Gao H (2013) Development of simple sequence repeat markers and diversity analysis in alfalfa (Medicago sativa L.). Mol Biol Rep 40(4):3291–3298. doi:10.1007/s11033-012-2404-3
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982. doi:10.1038/nrg2165
Wu J, Gu YQ, Hu Y, You FM, Dandekar AM, Leslie CA, Aradhya M, Dvorak J, Luo MC (2012) Characterizing the walnut genome through analyses of BAC end sequences. Plant Mol Biol 78(1–2):95–107. doi:10.1007/s11103-011-9849-y
Young ND, Debellé F, Oldroyd GED et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480(7378):520–524. doi:10.1038/nature10625
Yu K (2012) Bacterial artificial chromosome libraries of pulse crops: characteristics and applications. J Biomed Biotechnol 2012:493186. doi:10.1155/2012/493186
Yu K, Park SJ, Poysa V, Gepts P (2000) Integration of simple sequence repeat (SSR) markers into a molecular linkage map of common bean (Phaseolus vulgaris L.). J Hered 91(6):429–434. doi:10.1093/jhered/91.6.429
Zaiontz C (2013) Real statistical analysis using Excel. http://www.real-statistics.com. Accessed 20 May 2014
Zhu Z, Jiang W, Thompson HJ (2012) Edible dry bean consumption (Phaseolus vulgaris L.) modulates cardiovascular risk factors and diet-induced obesity in rats and mice. Br J Nutr 108(Suppl 1):66–73. doi:10.1017/S0007114512000839
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We thank the National Council for Scientific and Technological Development (CNPq) for the grants to GSP, CB, EGB and RPV; the Coordination for the Improvement of Higher Education Personnel/Ministry of Education (CAPES/MEC) for the grants to BSFM, the Minas Gerais State Research Foundation (FAPEMIG) for the grant to TS; and the Brazilian Agricultural Research Corporation (EMBRAPA) for financial support for this research. We also thank the anonymous referees for providing important comments that improved the first version of this manuscript.
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Müller, B.S.F., Sakamoto, T., Menezes, I.P.P. et al. Analysis of BAC-end sequences in common bean (Phaseolus vulgaris L.) towards the development and characterization of long motifs SSRs. Plant Mol Biol 86, 455–470 (2014). https://doi.org/10.1007/s11103-014-0240-7
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DOI: https://doi.org/10.1007/s11103-014-0240-7