Abstract
Genomic resources are sparse in most ecologically and economically important North American hardwood species. As part of the Hardwood Genomics project (http://www.hardwoodgenomics.org/), we evaluated the utility of restriction site associated DNA sequencing (RAD-Seq) for framework genetic linkage map construction in honeylocust (Gleditsia triacanthos L.), a leguminous tree common in eastern North America. Starting with a large open-pollinated family of progeny from a single tree, a mapping pedigree of 92 putative full-sibs was identified by kin group assignment and paternity analyses with microsatellite markers. RAD-Seq using Illumina next-generation DNA sequencing (NGS) generated over 117 M reads among the 92 plants. De novo reference genome clustering and alignment of samples to the reference genome revealed 5849 candidate single nucleotide polymorphisms (SNPs), of which 1570 were retained after quality filtering. Of the 1570 SNPs, 236 were in pseudo-testcross mapping configuration in the maternal parent and segregated approximately in the expected 1:1 ratio. The final map generated has a total length of 815.57 cM and consists of 178 markers on 14 linkage groups, corresponding to the haploid chromosome number in honey locust. Synteny and collinearity between honey locust and model legumes Glycine max, Medicago truncatula, and Phaseolus vulgaris were found for six of the honey locust linkage groups. RAD-Seq proved to be useful for framework linkage map construction in honey locust, a species for which no genomic resources had previously been available. However, greater sequence coverage and larger full-sib mapping pedigrees are necessary for the development of high-density linkage maps with future applications in quantitative trait locus (QTL) mapping.
Similar content being viewed by others
References
Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH (2011) Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188:799–808
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
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:e3376
Barchi L, Lanteri S, Portis E, Acquadro A, Vale G, Toppino L, Rotino GL (2011) Identification of SNP and SSR markers in eggplant using RAD tag sequencing. BMC Genomics 12:304
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449
Bus A, Hecht J, Huettel B, Reinhardt R, Stich B (2012) High-throughput polymorphism detection and genotyping in Brassica napus using next-generation RAD sequencing. BMC Genomics 13:281
Campbell FT, Schlarbaum SE (2014) Fading forests III. American forests. What choice will we make? The Nature Conservancy, Arlington, p 167
Claros MG, Bautista R, Guerrero-Fernandez D, Benzerki H, Seoane P, Fernandez-Pozo N (2012) Why assembling plant genome sequences is so challenging. Biology 1:439–459
Cui Y, Zhang F, Xu J, Li Z, Xu S (2015) Mapping quantitative trait loci in selected breeding populations: a segregation distortion approach. Heredity 115:538–546
Edwards D, Batley J, Cogan NOI, Forster JW, Chagne D (2007) Single nucleotide polymorphism discovery. In: Oraguzie NC, Rikkerink EHA, Gardiner SE, DeSilva HN (eds) Association mapping in plants. Springer, New York, pp 53–76
El-Kassaby YA, Cappa EP, Liewlaksaneeyanawin C, Klapste J, Lstiburek M (2011) Breeding without breeding: is a complete pedigree necessary for efficient breeding? PLoS One 6:e25737
Gibbs JN, Wainhouse D (1986) Spread of forest pests and pathogens in the northern hemisphere. Forestry 59:141–153
Gonen S, Lowe N, Cezard T, Gharbi K, Bishop S, Houston R (2014) Linkage maps of the Atlantic salmon (Salmo salar) genome derived from RAD sequencing. BMC Genomics 15:166
Gonen S, Bishop SC, Houston RD (2015) Exploring the utility of cross-laboratory RAD-sequencing datasets for phylogenetic analysis. BMC Res Notes 8:299
Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186
Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross mapping strategy and RAPD markers. Genetics 137:1121–1137
Grattapaglia D, Bertolucci FL, Sederoff RR (1995) Genetic mapping of QTLs controlling vegetative propagation in Eucalyptus grandis and E. urophylla using a pseudo-testcross strategy and RAPD markers. Theor Appl Genet 90:933–947
Hipp AL, Eaton DAR, Cavender-Bares J, Fitzek E, Nipper R, Manos PS (2014) A framework phylogeny of the American oak clade based on sequenced RAD data. PLoS One 9:e93975
Hougaard BK, Madsen LH, Sandal N, Moretzsohn MD, Fredslund J, Schauser L, Nielsen AM, Rohde T, Sato S, Tabata S, Bertioli DJ, Stougaard J (2008) Legume anchor markers link syntenic regions between Phaseolus vulgaris, Lotus japonicus, Medicago truncatula and Arachis. Genetics 179:2299–2312
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106
Keller I, Bensasson D, Nichols RA (2007) Transition-transversion bias is not universal: a counter example from grasshopper pseudogenes. PLoS Genet 3:185–191
Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4:779–782
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 19:1639–1645
Kumar S (1996) Patterns of nucleotide substitution in mitochondrial protein coding genes of vertebrates. Genetics 143:537–548
La Malfa S, Curro S, Douglas AB, Brugaletta M, Caruso M, Gentile A (2014) Genetic diversity revealed by EST-SSR markers in carob tree (Ceratonia siliqua L.). Biochem Syst Ecol 55:205–211
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25
Lewis G, Schrire B, Mackinder B, Lock M (2005) Legumes of the world. The Royal Botanical Gardens, Kew
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data P (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Owusu SA, Staton M, Jennings TN, Schlarbaum S, Coggeshall MV, Romero-Severson J, Carlson JE, Gailing O (2013) Development of genomic microsatellites in Gleditsia triacanthos (Fabaceae) using Illumina sequencing. Appl Plant Sci 1:1300050
Owusu SA, Schlarbaum S, Carlson JE, Gailing O (2016) Gene flow analyses and identification of full-sib families in isolated populations of Gleditsia triacanthos L. Botany-Botanique 94:523–532 doi:10.1139/cjb-2015-0244
Paillet FL (2002) Chestnut: history and ecology of a transformed species. J Biogeogr 29:1517–1530
Pegadaraju V, Nipper R, Hulke B, Qi LL, Schultz Q (2013) De novo sequencing of sunflower genome for SNP discovery using RAD (restriction site associated DNA) approach. BMC Genomics 14:556
Pfender WF, Saha MC, Johnson EA, Slabaugh MB (2011) Mapping with RAD (restriction-site associated DNA) markers to rapidly identify QTL for stem rust resistance in Lolium perenne. Theor Appl Genet 122:1467–1480
Pootakham W, Ruang-Areerate P, Jomchai N, Sonthirod C, Sangsrakru D, Yoocha T, Theerawattanasuk K, Nirapathpongporn K, Romruensukharom P, Tragoonrung S, Tangphatsornruang S (2015) Construction of a high-density integrated genetic linkage map of rubber tree (Hevea brasiliensis) using genotyping-by-sequencing (GBS). Front Plant Sci 6:367
Preston RJ Jr, Braham RR (2002) North American trees. Iowa State Press, Ames
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X-C, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C, Torres-Torres M, Geffroy V, Moghaddam SM, Gao D, Abernathy B, Barry K, Blair M, Brick MA, Chovatia M, Gepts P, Goodstein DM, Gonzales M, Hellsten U, Hyten DL, Jia G, Kelly JD, Kudrna D, Lee R, Richard MMS, Miklas PN, Osorno JM, Rodrigues J, Thareau V, Urrea CA, Wang M, Yu Y, Zhang M, Wing RA, Cregan PB, Rokhsar DS, Jackson SA (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713
Schnabel A, Hamrick JL (1995) Understanding the population genetic structure of Gleditsia triacanthos L.: the scale and pattern of pollen gene flow. Evolution 49:921–931
Schnabel A, Wendel JF (1998) Cladistic biogeography of Gleditsia (Leguminosae) based on ndhF and rpl16 chloroplast gene sequences. Amer J Bot 85:1753–1765
Slavov GT, Nipper R, Robson P, Farrar K, Allison GG, Bosch M, Clifton-Brown JC, Donnison IS, Jensen E (2014) Genome-wide association studies and prediction of 17 traits related to phenology, biomass and cell wall composition in the energy grass Miscanthus sinensis. New Phytol 201:1227–1239
Smith WB, Darr DR (2004) U.S. forest resource facts and historical trends. U.S. Department of Agriculture, Forest Service, Washington, p 37
Staton M, Best T, Khodwekar S, Owusu S, Xu T, Xu Y, Jennings T, Cronn R, Arumuganathan AK, Coggeshall M, Gailing O, Liang H, Romero-Severson J, Schlarbaum S, Carlson JE (2015) Preliminary genomic characterization of ten hardwood tree species from multiplexed low coverage whole genome sequencing. PLoS One 10:e0145031
Stӧlting 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 22:842–855
Sun R, Chang Y, Yang F, Wang Y, Li H, Zhao Y, Chen D, Wu T, Zhang X, Han Z (2015) A dense SNP genetic map constructed using restriction site-associated DNA sequencing enables detection of QTLs controlling apple fruit quality. BMC Genomics 16:747
Tong CF, Li HG, Wang Y, Li XR, Ou JJ, Wang DY, Xu HX, Ma C, Lang XY, Liu GX, Zhang B, Shi JS (2016) Construction of high-density linkage maps of Populus deltoides × P. simonii using restriction-site associated DNA sequencing. PLoS One 11:e0150692
Van Ooijen JW (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma, Wageningen
Varshney RK, Nayak SN, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27:522–530
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Whitham TG, Gehring CA, Lamit LJ, Wojtowicz T, Evans LM, Keith AR, Smith DS (2012) Community specificity: life and afterlife effects of genes. Trends Plant Sci 17:271–281
Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analyses of the plastid matK gene resolves many well-supported subclades within the family. Amer J Bot 91:1846–1862
Wu J, Li L-T, Li M, Khan MA, Li X-G, Chen H, Yin H, Zhang S-L (2014) High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. J Exp Bot 65:5771–5781
Xu SZ (2008) Quantitative trait locus mapping can benefit from segregation distortion. Genetics 180:2201–2208
Xu P, Xu SZ, Wu XH, Tao Y, Wang BG, Wang S, Qin DH, Lu ZF, Li GJ (2014) Population genomic analyses from low-coverage RAD-Seq data: a case study on the non-model cucurbit bottle gourd. Plant J 77:430–442
Yang ZH, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17:32–43
Yang ZH, Yoder AD (1999) Estimation of the transition/transversion rate bias and species sampling. J Mol Evol 48:274–283
Yin TM, DiFazio SP, Gunter LE, Riemenschneider D, Tuskan GA (2004) Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map. Theor Appl Genet 109:451–463
Young ND, Debelle F, Oldroyd GED, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KFX, Gouzy J, Schoof H, Van de Peer Y, Proost S, Cook DR, Meyers BC, Spannagl M, Cheung F, De Mita S, Krishnakumar V, Gundlach H, Zhou S, Mudge J, Bharti AK, Murray JD, Naoumkina MA, Rosen B, Silverstein KAT, Tang H, Rombauts S, Zhao PX, Zhou P, Barbe V, Bardou P, Bechner M, Bellec A, Berger A, Berges H, Bidwell S, Bisseling T, Choisne N, Couloux A, Denny R, Deshpande S, Dai X, Doyle JJ, Dudez A-M, Farmer AD, Fouteau S, Franken C, Gibelin C, Gish J, Goldstein S, Gonzalez AJ, Green PJ, Hallab A, Hartog M, Hua A, Humphray SJ, Jeong D-H, Jing Y, Jocker A, Kenton SM, Kim D-J, Klee K, Lai H, Lang C, Lin S, Macmil SL, Magdelenat G, Matthews L, McCorrison J, Monaghan EL, Mun J-H, Najar FZ, Nicholson C, Noirot C, O’Bleness M, Paule CR, Poulain J, Prion F, Qin B, Qu C, Retzel EF, Riddle C, Sallet E, Samain S, Samson N, Sanders I, Saurat O, Scarpelli C, Schiex T, Segurens B, Severin AJ, Sherrier DJ, Shi R, Sims S, Singer SR, Sinharoy S, Sterck L, Viollet A, Wang B-B, Wang K, Wang M, Wang X, Warfsmann J, Weissenbach J, White DD, White JD, Wiley GB, Wincker P, Xing Y, Yang L, Yao Z, Ying F, Zhai J, Zhou L, Zuber A, Denarie J, Dixon RA, May GD, Schwartz DC, Rogers J, Quetier F, Town CD, Roe BA (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
Acknowledgments
The study was supported by grant # TRPGR IOS-1025974 from the National Science Foundation Plant Genome Research Program. Additional support was provided by the Ecosystem Science Center and the Biotech Research Center at Michigan Technological University.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Materials
Below is the link to the electronic supplementary material.
ESM 1
Supplementary Fig. 1. Alignment of honey locust maps calculated from the marker set that was derived from the stringent (left-hand side) and relaxed (right-hand side) RAD-Seq clustering protocol. (PPTX 82 kb)
ESM 2
Supplementary Fig. 2. Individual sample sequence performance including number of reads and sequence coverage. (DOCX 536 kb)
ESM 3
(XLSX 16 kb)
ESM 4
(XLSX 36 kb)
ESM 5
(XLSX 9 kb)
Rights and permissions
About this article
Cite this article
Gailing, O., Staton, M.E., Lane, T. et al. Construction of a Framework Genetic Linkage Map in Gleditsia triacanthos L.. Plant Mol Biol Rep 35, 177–187 (2017). https://doi.org/10.1007/s11105-016-1012-0
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-016-1012-0