Abstract
Linkage disequilibrium (LD) in crops, established by domestication and early breeding, can be a valuable basis for mapping the genome. We undertook an assessment of LD in sugarcane (Saccharum spp), characterized by one of the most complex crop genomes, with its high ploidy level (≥8) and chromosome number (>100) as well as its interspecific origin. Using AFLP markers, we surveyed 1,537 polymorphisms among 72 modern sugarcane cultivars. We exploited information from available genetic maps to determine a relevant statistical threshold that discriminates marker associations due to linkage from other associations. LD is very common among closely linked markers and steadily decreases within a 0–30 cM window. Many instances of linked markers cannot be recognized due to the confounding effect of polyploidy. However, LD within a sample of cultivars appears as efficient as linkage analysis within a controlled progeny in terms of assigning markers to cosegregation groups. Saturating the genome coverage remains a challenge, but applying LD-based mapping within breeding programs will considerably speed up the localization of genes controlling important traits by making use of phenotypic information produced in the course of selection.
Similar content being viewed by others
References
Aitken KS, Jackson PA, McIntyre CL (2005) A combination of AFLP and SSR markers provides extensive map coverage and identification of homo(eo)logous linkage groups in a sugarcane cultivar. Theor Appl Genet 110:789–801
Arceneaux G (1965) Cultivated sugarcanes of the world and their botanical derivation. Proc Int Soc Sugar Cane Technol 12:844–854
Asnaghi C, Roques D, Ruffel S, Kaye C, Hoarau JY, Télismart H, Girard JC, Raboin LM, Risterucci AM, Grivet L, D’Hont A (2004) Targeted mapping of a sugarcane rust resistance gene (Bru1) using bulked segregant analysis and AFLP markers. Theor Appl Genet 108:759–764
Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177
Cardon LR, Bell JI (2001) Association study designs for complex diseases. Nat Rev Genet 2:91–99
Cuadrado A, Acevedo R, de Moreno Dias la Espina S, Jouve N, de la Torre C (2004) Genome remodelling in three modern S. officinarum × S. spontaneum sugarcane cultivars. J Exp Bot 55:847–854
Daugrois JH, Grivet L, Roques D, Hoarau JY, Lombard H, Glaszmann JC, D’Hont A (1996) A putative major gene for rust resistance linked with an RFLP marker in sugarcane cultivar R570. Theor Appl Genet 92:1059–1064
D’Hont A (2005) Unravelling the genome structure of polyploids using FISH and GISH; examples of sugarcane and banana. Cytogenet Genome Res 109:27–33
D’Hont A, Grivet L, Feldmann P, Rao RS, Berding N, Glaszmann JC (1996) Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics. Mol Gen Genet 250:405–413
Dufour P, Deu M, Grivet L, D’Hont A, Paulet F, Bouet A, Lanaud C, Glaszmann JC, Hamon P (1997) Construction of a composite sorghum genome map and comparison with sugarcane, a related complex polyploid. Theor Appl Genet 94:409–418
Farnir F, Coppieters W, Arranz JJ, Berzi P, Cambisano N, Grisart B, Karim L, Marcq F, Moreau L, Mni M, Nezer C, Simon P, Vanmanshoven P, Wagenaar D, Georges M (2000) Extensive genome-wide linkage disequilibrium in cattle. Genome Res 10:220–227
Flint-Garcia SA, Thornsberry JM, Buckler IV ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374
Gallais A (2003) Quantitative genetics and breeding methods in autopolyploid plants. INRA Editions, Paris, 515 pp
Garcia AAF, Kido EA, Meza AN, Souza HMB, Pinto LR, Pastina MM, Leite CS, da Silva JAG, Ulian EC, Figueira A, Souza AP (2006) Development of an integrated genetic map of a sugarcane (Saccharum spp.) commercial cross, based on a maximum-likelihood approach for estimation of linkage and linkage phases. Theor Appl Genet 112:298–314
Garris AJ, McCouch SR, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165:759–769
Grivet L, Arruda P (2001) Sugarcane genomics: depicting the complex genome of an important tropical crop. Curr Opin Plant Biol 5:122–127
Grivet L, D’Hont A, Roques D, Feldmann P, Lanaud C, Glaszmann JC (1996) RFLP mapping in cultivated sugarcane (Saccharum spp.): genome organization in a highly polyploid and aneuploid interspecific hybrid. Genetics 142:987–1000
Grivet L, Glaszmann JC, Vincentz M, da Silva F, Arruda P (2003) ESTs as a source for sequence polymorphism discovery in sugarcane: example of the Adh genes. Theor Appl Genet 106:190–197
Guimaraes CT, Sills GR, Sobral BWS (1997) Comparative mapping of Andropogoneae: Saccharum L. (sugarcane) and its relation to sorghum and maize. Proc Natl Acad Sci 94:14261–14266
Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485
Hamblin MT, Fernandez MGS, Casa AM, Mitchell SE, Paterson AH, Kresovich S (2005) Equilibrium processes cannot explain high levels of short- and medium-range linkage disequilibrium in the domesticated grass Sorghum bicolor. Genetics 171:12474–1256
Hansen M, Kraft T, Ganestam S, Säll T, Nilsson NO (2001) Linkage disequilibrium mapping of the bolting gene in sea beet using AFLP markers. Genet Res Camb 77:61–66
Hoarau JY, Offmann B, D’Hont A, Risterucci AM, Roques D, Glaszmann JC, Grivet L (2001) Genetic dissection of a modern cultivar (Saccharum spp.) I. genome mapping with AFLP markers. Theor Appl Genet 103:84–97
Jannoo N, Grivet L, Dookun A, D’Hont A, Glaszmann JC (1999) Linkage desequilibrium among modern sugarcane cultivars. Theor Appl Genet 99:1053–1060
Jannoo N, Grivet L, David J, D’Hont A, Glaszmann JC (2004). Differential chromosome pairing affinities at meiosis in polyploid sugarcane revealed by molecular markers. Heredity 93:460–467
Kraakman ATW, Niks RE, van den Berg PMMM, Stam P, van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446
Mehta CR, Patel NR (1983) A network algorithm for performing Fisher’s exact test in r × c contingency tables. J Am Stat Assoc 78:427–434
Ming R, Liu SC, Lin YR, Da Silva J, Wilson W, Braga D, van Deinze A, Wenslaff TF, Wu KK, Moore PH, Burnquist W, Sorrells ME, Irvine JE, Paterson AH (1998) Detailed alignment of Saccharum and Sorghum chromosomes: comparative organization of closely related diploid and polyploid genomes. Genetics 150:1663–1682
Ming R, Liu SC, Moore PH, Irvine JE, Paterson AH (2001) QTL analysis in a complex autopolyploid: genetic control of sugar content in sugarcane cultivars under salinity. Plant Physiol 104:521–526
Ming R, DelMonte T, Moore PH, Irvine JE, Paterson AH (2002a) Comparative analysis of QTLs affecting plant height and flowering time among closely-related diploid and polyploid genomes. Genome 45:794–803
Ming R, Wang YW, Dryer X, Moore PH, Irvine JE, Paterson AH (2002b) Molecular dissection of complex traits in autopolyploid: mapping QTLs influencing sugar yield and related traits in sugarcane. Theor Appl Genet 105:332–345
Morgante M, Salamini F (2003) From plant genomics to breeding practice. Curr Opin Biotech 14:214–219
Nei M, Li W (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:427–434
Nordborg M, Tavaré S (2002) Linkage disequilibrium: what history has to tell us. Trends Genet 18:83–90
Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloof JN, Noyes T, Oefner PJ, Stahl EA, Weigel D (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 30:190–193
Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J. (2005) The Pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3(7): e196. doi:10.1371/journal.pbio.0030196
Perrier X, Flori A, Bonnot F (2003) Methods of data analysis. In: Hamon PS, Seguin M, Perrier X, Glaszmann JC (eds) Genetic diversity of cultivated tropical plants, Cirad, Montpellier, pp 31–63
Pinto LR, Oliveira KM, Ulia EC, Garcia AAF, de Souza AP (2004) Survey in the sugarcane expressed sequence tag database (SUCEST) for simple sequence repeats. Genome 47:795–804
Piperidis G, D’Hont A (2001) Chromosome composition analysis of various Saccharum interspecific hybrids by genomic in situ hybridisation (GISH). Int Soc Sugar Cane Technol Congr 11:565
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959
Pritchard JK, Wen W (2003) Documentation for structure software: Version 2. http://pritch.bsd.uchicago.edu
Raboin LM, Oliveira KM, Lecunff L, Telismart H, Roques D, Butterfield M, Hoarau JY, D’Hont A (2006) Genetic mapping in the high polyploid sugarcane using a bi-parental progeny; identification of a gene controlling stalk colour and a new rust resistance gene. Theor Appl Genet 112:1382–1391
Rahmani M, Hodges AW, Kiker CF, Shiralipour A (2000) Biomass research and development in Florida: results of 20 years experience. Proceedings of the bioenergy. The nineth biennial bioenergy conference, Buffalo, 15–19 October
Rafalski A, Morgante M (2004) Corn and humans: recombination and linkage disequilibrium in two genomes of similar size. Trends Genet 20:103–111
Reffay N, Jackson PA, Aitken KS, Hoarau JY, D’Hont A, Besse P, McIntyre CL (2005) Characterisation of genome regions incorporated from an important wild relative into Australian sugarcane. Mol Breed 15:367–381
Rossi M, Araujo PG, Paulet F, Garsmeur O, Dias VM, Chen H, van Sluys MA, D’Hont A (2003) Genomic distribution and characterization of EST-derived resistance gene analogs (RGAs) in sugarcane. Mol Gen Genet 269:406–419
Ruiz M, Rouard M, Raboin LM, Lartaud M, Lagoda P, Courtois B (2004) Tropgene-DB, a multitropical crop information system. Nucleic Acids Res 32: D364–D367
SAS Institute (1990) SAS procedures guide, version 6. 3rd edn. SAS Institute Inc, Cary
Stich B, Melchinger AE, Frish M, Maurer HP, Heckenberger M, Reif JC (2005) Linkage disequilibrium in European elite maize germplasm investigated with SSRs. Theor Appl Genet 111:723–730
Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci 98:9161–9166
Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414
Wei X, Jackson PA, Mc Intyre CL, Aitken KS, Croft B (2006) Associations between DNA markers and resistance to diseases in sugarcane and effects of population substructure. Theor Appl Genet 114:155–164
Wenzl P, Carling J, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A (2004) Diversity arrays technology (DArT) for whole-genome profiling of barley. Proc Natl Acad Sci 101:9915–9920
Acknowledgments
We gratefully thank J.Y. Hoarau for his helpful revision of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. E. Bradshaw.
Louis-Marie Raboin and Jérôme Pauquet contributed equally to this work.
Rights and permissions
About this article
Cite this article
Raboin, LM., Pauquet, J., Butterfield, M. et al. Analysis of genome-wide linkage disequilibrium in the highly polyploid sugarcane. Theor Appl Genet 116, 701–714 (2008). https://doi.org/10.1007/s00122-007-0703-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-007-0703-1