Abstract
Sugarcane (Saccharum spp. hybrids) is one of the world’s most important economic crops for both the food and biofuel industries. It has one of the most complex genomes of any crop plant, varieties are unbalanced polyploids and derived from interspecific hybridisation between the domesticated Saccharum officinarum and a wild relative S. spontaneum. Here I review sugarcane’s complex genetics and chart the history of DNA marker development in sugarcane over the last 30 years. Despite its complex autopolyploid genome of over 100 chromosomes, marker development has spanned the first hybridisation-based markers, restriction fragment length polymorphism markers (RFLP) to the high-throughput next generation sequence methods currently used to detect single nucleotide polymorphism (SNP). Although there is a long history of research and development in sugarcane, it is only comparatively recently that marker technology has caught up with the need for discovery of large numbers of single-dose SNP markers and methods for genotyping that are fast, efficient and cost-effective that can be used for selection in a breeding program. The choice of genotyping platform depends on the breeding application and both whole genome SNP methods (array-based and genotype-by-sequencing (GBS)) and low density scalable and cost-effective platform technologies have a place in sugarcane breeding.
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Aitken, K.S., P.A. Jackson, and C.L. McIntyre. 2005. A combination of AFLP and SSR markers provides extensive map coverage and identification of homo(eo)logous linkage groups in a sugarcane variety. Theoretical and Applied Genetics 110: 789–801.
Aitken, K.S., J.C. Li, P.A. Jackson, G. Piperidis, and C.L. McIntyre. 2006. AFLP analysis of genetic diversity within Saccharum officinarum and comparison with sugarcane varieties. Australian Journal of Agricultural Research 57: 1167–1184.
Aitken, K.S., P.A. Jackson, and C.L. McIntyre. 2007. Construction of genetic linkage map for Saccharum officinarum incorporating both simplex and duplex markers to increase genome coverage. Genome 50: 742–756.
Aitken, K.S., M.D. McNeil, S. Hermann, P.C. Bundock, A. Kilian, K. Heller-Uszynska, R.J. Henry, and J.C. Li. 2014a. A comprehensive genetic map of sugarcane that provides enhanced map coverage and integrates high-throughput Diversity Array Technology (DArT) markers. BMC Genomics 15: 152.
Aitken, K.S., M.D. McNeil, P.J. Berkman, S. Hermann, A. Kilian, P.C. Bundock, and J.C. Li. 2014b. Comparative mapping in the Poaceae family reveals translocations in the complex polyploid genome of sugarcane. BMC Plant Biology 14: 190.
Aitken, K.S., A. Farmer, P. Berkman, C. Muller, X. Wei, E. Demano, P.A. Jackson, M. Magwire, B. Dietrich, and R. Kota. 2017. Generation of a 234K sugarcane SNP chip. International Sugar Journal 119: 816–820.
Alwala, S., C.A. Kimbeng, J.C. Veremis, and K.A. Gravois. 2008. Linkage mapping and genome analysis in a Saccharum interspecific cross using AFLP, SRAP and TRAP markers. Euphytica 164: 37–51.
Arceneaux, G. 1965. Cultivated sugarcanes of the world and their botanical derivation. Proceedings of the International Society of Sugar Cane Technologists 12: 844–854.
Asnaghi, C., D. Roques, S. Ruffel, C. Kaye, J.Y. Hoarau, H. Télismart, J.C. Girard, L.M. Raboin, A.M. Risterucci, L. Grivet, and A. D’Hont. 2004. Targeted mapping of a sugarcane rust resistance gene (Bru1) using bulked segregant analysis and AFLP markers. Theoretical and Applied Genetics 108: 759–764.
Balsalobre, T.W.A., G.D. Pereira, G.R.A. Margarido, R. Gazaffi, F.Z. Barreto, C.O. Anoni, C.B. Cardoso-Silva, E.A. Costa, M.C. Mancini, H.P. Hoffmann, A.P. de Souza, A.A.F. Garcia, and M.S. Carneiro. 2017. GBS-based single dosage markers for linkage and QTL mapping allow gene mining for yield-related traits in sugarcane. BMC Genomics 18: 72. https://doi.org/10.1186/s12864-016-3383-x.
Bundock, P.C., F.G. Eilott, G. Ablett, A.D. Benson, R.E. Casu, K.S. Aitken, and R.J. Henry. 2009. Targeted single nucleotide polymorphism (SNP) discovery in a highly ployploid plant species using 454 sequencing. Plant Biotechnology Journal. 7: 347–354.
Bundock, P.C., R.E. Casu, and R.J. Henry. 2012. Enrichment of genomic DNA for polymorphism detection in a non-model high polyploid crop plant. Plant Biotechnology Journal 10: 657–667.
Burner, D.M., and B.L. Legendre. 1993. Chromosome transmission and meiotic stability of sugarcane (Saccharum spp.) hybrid derivatives. Crop Science 33: 600–606.
Burnquist, W.L., M.E. Sorrells, and S.D. Tanksley. 1992. Characterisation of genetic variability in Saccharum germplasm by means of Restriction Fragment Length Polymorphism (RFLP) analysis. Proceedings of the International Society of Sugar Cane Technologists 21: 355–365.
Burnquist, W.L. 1991. Development and application of restriction fragment length polymorphism technology in sugarcane (Saccharum spp.) breeding. Ph.D. Dissertation, Cornell University, Ithaca, NY.
Costet, L., L. Le Cunff, S. Royaert, L.M. Raboin, C. Hervouet, L. Toubi, H. Telismart, O. Garsmeur, Y. Rousselle, J. Pauquet, S. Nibouche, J.C. Glaszmann, J.Y. Hoarau, and A. D’Hont. 2012a. Haplotype structure around Bru1 reveals a narrow genetic basis for brown rust resistance in modern sugarcane varieties. Theoretical and Applied Genetics 125: 825–836.
Costet, L., L.M. Raboin, M. Payet, A. D’Hont, and S. Nibouche. 2012b. A major quantitative trait allele for resistance to the Sugarcane yellow leaf virus (Luteoviridae). Plant Breeding 131: 637–640.
Cordeiro, G.M., G.O. Taylor, and R.J. Henry. 2000. Characterisation of microsatellite markers from sugarcane (Saccharum sp.), a highly polyploid species. Plant Science 155: 161–168.
Daniels, J., and B.T. Roach. 1987. Taxonomy and evolution. In Sugarcane improvement through breeding, ed. D.J. Heinz, 7–84. Amsterdam: Elsevier Press.
Daugrois, P., L. Grivet, D. Roques, J.Y. Hoarau, H. Lombard, J.C. Glaszmann, and A. D’Hont. 1996. A putative major gene for rust resistance linked with a RFLP marker in sugarcane varieties R570. Theoretical and Applied Genetics 92: 1059–1064.
Da Silva, J., R.J. Honeycutt, W. Burnquist, S.M. Al-Janabi, M.E. Sorrells, S.D. Tanksley, and B.W.S. Sobral. 1995. Saccharum spontaneum L. ‘SES 208’ genetic linkage map combining RFLP- and PCR-based markers. Molecular Breeding 1: 165–179.
Da Silva, J.A.G., M.E. Sorrells, W.L. Burnquist, and S.D. Tanksley. 1993. RFLP linkage map and genome analysis of Saccharum spontaneum. Genome 36: 782–791.
Deomano, E., P. Jackson, X. Wei, K. Aitken, R. Kota, and P. Perez-Rodriguez. 2020. Genomic prediction of sugar content and cane yield in sugarcane clones in different stages of selection in a breeding program, with and without pedigree information. Molecular Breeding 40: 38.
D’Hont, A., L. Grivet, and P. Feldmann. 1996. Characterisation of the double genome structure of modern sugarcane varietiess (Saccharum spp.) by molecular cytogenetics. Molecular and General. Genetics 250: 405–416.
D’Hont, A., D. Ison, K. Alix, C. Roux, and J.C. Glaszmann. 1998. Determination of basic chromosome numbers in the genus Saccharum by physical mapping of ribosomal RNA genes. Genome 41: 221–225.
Elshire, R.J., J.C. Glaubitz, Q. Sun, J.A. Poland, K. Kawamoto, E.S. Buckler, and S.E. Mitchell. 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6: e19378.
Evans, D.L., and S.V. Joshi. 2016. Complete chloroplast genomes of Saccharum spontaneum, Saccharum officinarum and Miscanthus floridulus (Panicoideae: Andropogoneae) reveal the plastid view on sugarcane origins. Systematics and Biodiversity 14(6): 548–571.
Evans, D.L., T.T. Hlongwane, S.V. Joshi, and D.M.R. Pachón. 2019. The sugarcane mitochondrial genome: Assembly, phylogenetics and transcriptomics. PeerJ 7: e7558. https://doi.org/10.7717/peerj.7558.
Gallacher, D.J., D.J. Lee, and N. Berding. 1995. Use of Isozyme phenotypes for rapid discrimination among sugarcane clones. Australia Journal of Agricultural. Research. 46: 601–609.
Garcia, A.A.F., M. Mollinari, T.G. Marconi, O.R. Serang, R.R. Silva, M.L.C. Vieira, R. Vicentini, E.A. Costa, M.C. Mancini, M.O.S. Garcia, M.M. Pastina, R. Gazaffi, E.R.F. Martins, N. Dahmer, D.A. Sforca, C.B.C. Silva, P. Bundock, R.J. Henry, G.M. Souza, M.A. van Sluys, M.G.A. Landell, M.S. Carneiro, M.A.G. Vincentz, L.R. Pinto, R. Vencovsky, and A.P. Souza. 2013. SNP genotyping allows an in-depth characterisation of the genome of sugarcane and other complex autopolyploids. Scientific Reports 3: 3399. https://doi.org/10.1038/srep03399.
Garsmeur, O., G. Droc, R. Antonise, J. Grimwood, B. Potier, K. Aitken, J. Jenkins, G. Martin, C. Charron, C. Hervouet, L. Costet, N. Yahiaoui, A. Healey, D. Sims, Y. Cherukuri, A. Sreedasyam, A. Kilian, A. Chan, M.A. Van Sluys, K. Swaminathan, C. Town, H. Berges, B. Simmons, J.C. Glaszmann, E. van der Vossen, R. Henry, J. Schmutz, and A. D’Hont. 2018. A mosaic monoploid reference sequence for the highly complex genome of sugarcane. Nature Communications. https://doi.org/10.1038/s41467-018-05051-5.
Glaszmann, J.C., A. Fautret, J.L. Noyer, P. Feldmannn, and C. Lanaud. 1989. Biochemical genetic markers in sugarcane. Theoretical and Applied Genetics 78: 537–543.
Glaszmann, J.C., P. Dufour, L. Grivet, A. D’Hont, M. Deu, F. Paulet, and P. Hamon. 1997. Comparative genome analysis between several tropical grasses. Euphytica 96: 13–21.
Glynn, N.C., C. Laborde, R.W. Davidson, M.S. Irey, B. Glaz, A. D’Hont, and J.C. Comstock. 2013. Utilization of a major brown rust resistance gene in sugarcane breeding. Molecular Breeding 31:323–331.https://doi.org/10.1007/s11032-012-9792-x.
Heller-Uszynska, K., G. Uszynski, E. Huttner, M. Evers, J. Carlig, V. Caig, K. Aitken, P. Jackson, G. Piperidis, M. Cox, R. Gilmour, A. D’Hont, M. Butterfield, J.C. Glaszmann, and A. Kilian. 2011. Diversity Arrays Technology effectively reveals DNA polymorphism in a large and complex genome of sugarcane. Molecular Breeding 28: 37–55.
Hoarau, J.Y., B. Offmann, A. D’Hont, A.M. Risterucci, D. Roques, J.C. Glaszmann, and L. Grivet. 2001. Genetic dissection of a modern sugarcane varieties (Saccharum spp.). 1. Genome mapping with AFLP markers. Theoretical and Applied Genetics 103: 84–97.
Jannoo, N., L. Grivet, J. David, A. D’Hont, and J.C. Glaszmann. 2004. Differential chromosome pairing affinities at meiosis in polyploid sugarcane revealed by molecular markers. Heredity 93: 460–467.
Johnson, M., N. Janakiraman, and V. Irudayaraj. 1997. Isozyme analysis on different varieties of sugarcane. Journal of Stress Physiology and Biochemistry 8: 22–31.
Maccheroni, W., H. Jordão, R. Degaspari, and S. Matsuoka. 2007. Development of a dependable microsatellite-based fingerprinting system for sugarcane. Proceedings of the International Society of Sugar Cane Technologists 26: 889–900.
Manimekalai, R., G. Suresh, H. Govinda Kurup, S. Athiappan, and M. Kandalam. 2020. Role of NGS and SNP genotyping methods in sugarcane improvement programs. Critical Reviews in Biotechnology. 40(6): 865–880. https://doi.org/10.1080/07388551.2020.1765730.
McCouch, S.R., G. Kochert, Z.H. Yu, Z.Y. Wang, G.S. Kush, W.R. Coffman, and S.D. Tanksley. 1988. Molecular mapping of rice chromosomes. Theoretical and Applied Genetics. 76: 815–829.
McIntyre, C.L., and P.A. Jackson. 2001. Low level of selfing found in a sample of crosses in Australian sugarcane breeding programs. Euphytica 117: 245–249.
McNeil, M.D., G. Piperidis, S. Bhuiyan, J. Li, X. Wei, B. Collard, and K. Aitken. 2017. Development of a high-throughput low-cost SNP genotyping panel for sugarcane breeding. Proceedings of the Australian Society of Sugar Cane Technologists. 39: AG49.
Meng, Z., J.L. Han, Y.J. Lin, Y.Y. Zhao, Q.F. Lin, X.K. Ma, J.P. Wang, M.Q. Zhang, L.S. Zhang, Q.H. Yang, and K. Wang. 2019. Characterization of a Saccharum spontaneum with a basic chromosome number of x = 10 provides new insights on genome evolution in genus Saccharum. Theoretical and Applied Genetics. 133: 187–199. https://doi.org/10.1007/s00122019-03450-w.
Miller, J.C., and S.D. Tanksley. 1990. RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theoretical and Applied Genetics. 80: 437–448.
Ming, R., S.C. Liu, Y.R. Lin, J. Da Silva, W. Wilson, D. Braga, A. Van Deynze, T.F. Wenslaff, K.K. Wu, P.H. Moore, W. Burnquist, M.E. Sorrells, J.E. Irvine, and A.H. Paterson. 1998. Detailed alignment of Saccharum and Sorghum chromosomes: Comparative organisation of closely related diploid and polyploid genomes. Genetics 150: 1663–1682.
Ming, R., S.C. Liu, J.E. Bowers, P.H. Moore, J.F. Irvine, and A.H. Paterson. 2002. Construction of a Saccharum consensus genetic map from two interspecific crosses. Crop Science 42: 570–583.
Mudge, J., W.R. Andersen, R.L. Kehrer, and D.J. Fairbanks. 1996. A RAPD genetic map of Saccharum officinarum. Crop Science 36: 1362–1366.
Nair, N.V., S. Nair, T.V. Sreenivasan, and M. Mohan. 1999. Analysis of genetic diversity and phylogeny in Saccharum and related genera using RAPD markers. Genetic Resources and Crop Evolution 46: 73–79.
Nair, N.V., A. Selvi, T.V. Sreenivasan, and K.N. Pushpalatha. 2002. Molecular diversity in Indian sugarcane varieties as revealed by randomly amplified DNA polymorphisms. Euphytica 127: 219–225.
Pan, Y.B. 2010. Databasing molecular identities of sugarcane (Saccharum spp.) clones constructed with microsatellite (SSR) markers. American Journal of Plant Science 1: 87–94.
Piperidis, G., G.O. Taylor, and G.R. Smith. 2001. A microsatellite marker database for fingerprinting sugarcane clones. Proceedings of the International Society of Sugar Cane Technologists. 24: 632–633.
Piperidis, G., A.R. Rattey, G.O. Taylor, and M.C. Cox. 2004. DNA markers: A tool for identifying sugarcane varieties. Proceedings of the Australian Society of Sugar Cane Technologists. 26: 2004.
Piperidis, N., and A. D’Hont. 2020. Sugarcane genome architecture decrypted with chromosome-specific oligo probes. The Plant Journal. 103(6): 2039–2051. https://doi.org/10.1111/tpj.14881.
Raboin, L.-M., J. Pauquet, M. Butterfield, A. D’Hont, and J.C. Glaszmann. 2008. Analysis of genome-wide linkage disequilibrium in the highly polyploid sugarcane. Theoretical and Applied Genetics 116: 701–714. https://doi.org/10.1007/s00122-007-0703-1.
Ripol, M.I., G.A. Churchill, J.A.G. Da Silva, and M. Sorrells. 1999. Statistical aspects of genetic mapping in autopolyploids. Gene 235: 31–41.
Ritter, E., C. Gebhardt, and F. Salamini. 1990. Estimation of recombination frequencies and construction of RFLP linkage maps in plants from between heterozygous parents. Genetics 125: 645–560.
Rossi, M., G.P. Araujo, F. Paulet, O. Garsmeur, V.M. Dias, H. Chen, M. Van Sluys, and A. D’Hont. 2003. Genomic distribution and characteristation of EST-derived resistance gene analogs (RGAs) in sugarcane. Molecular Genetics and Genomics 269: 406–419.
Scheben, A., J. Batley, and D. Edwards. 2017. Genotyping-by-sequencing approaches to characterize crop genomes: Choosing the right tool for the right application. Plant Biotechnology Journal. 15: 149–161.
Song, J., X. Yang, M.F.R. Resende, L.G. Neves, J. Todd, J. Zhang, J.C. Comstock, and J. Wang. 2016. Natural allelic variations in highly polyploidy Saccharum complex. Frontiers in Plant Science 7: 804.
Joshi, S.V., and E.H. Albertse. 2013. Development of a fingerprinting database and varieties identification in sugarcane using a genetic analyser. Proceedings of the South African Sugar Technology Association 86: 200–212.
Sreenivasan, T.V., B. Ahloowalia, and D. Heinz. 1987. Cytogenetics. In Sugarcane improvement through breeding, ed. D.J. Heinz, 211–253. Amsterdam: Elsevier Press.
Tenaillon, M.L., M.C. Sawkins, A.D. Long, R.L. Gaut, J.F. Doebley, and B.S. Gaut. 2001. Patterns of DNA sequence polymorphisms along chromosome 1 of maize (Zea mays ssp. Mays L.). Proceedings of the National Academy of Sciences of the United States of America 98: 9161–9166.
Vieira, M.L.C., C.B. Almeida, C.A. Oliveira, L.O. Tacuatia, C.F. Munhoz, L.A. Cauz-Santos, L.R. Pinto, C.B. Monteiro-Vitorello, M.A. Xavier, and E.R. Forni-Martins. 2018. Revisiting meiosis in sugarcane: Chromosomal irregularities and the prevalence of bivalent configurations. Frontiers in Genetics 9: 1–12.
Wei, X., P.A. Jackson, C.L. McIntyre, K.S. Aitken, and B. Croft. 2006. Associations between DNA markers and resistance to diseases in sugarcane and effects of population substructure. Theoretical and Applied Genetics 114: 155–164.
Wei, X., P.A. Jackson, S. Hermann, A. Kilian, K. Heller-Uszynska, and E. Deomano. 2010. Simultaneously accounting for population structure, genotype by environment interaction, and spatial variation in marker-trait associations in sugarcane. Genome 53: 973–981.
Wood, B. 1987. Restriction fragment length polymorphism distinguishes members of Saccharum sinense and Sbarberi. Plant Physiology 83(Suppl): 15.
Wu, K.K., W. Burnquist, M.E. Sorrells, T.L. Tew, P.H. Moore, and S.D. Tanksley. 1992. The detection and estimation of linkage in polyploids using single-dose restriction fragments. Theoretical and Applied Genetics 83: 294–300.
Yadav, S., P. Jackson, X. Wei, E.M. Ross, K. Aitken, E. Deomano, F. Atkin, B.J. Hayes, and K.P. Voss-Fels. 2020. Accelerating genetic gain in sugarcane breeding using genomic selection. Agronomy 10: 585. https://doi.org/10.3390/agronomy10040585.
Yang, X., J. Song, Q. You, D.R. Paudel, J. Zhang, and J. Wang. 2017a. Mining sequence variations in representative polyploid sugarcane germplasm accessions. BMC Genomics 18: 594.
Yang, X., S. Sood, N. Glynn, M.S. Islam, J. Comstock, and J.P. Wang. 2017b. Constructing high density genetic maps for polyploid sugarcane (Saccharum spp.) and identifying quantitative trait loci controlling brown rust resistance. Molecular Breeding 37: 116.
You, Q., X. Yang, Z. Peng, M.S. Islam, S. Sood, Z.L. Luo, J. Comstock, L.P. Xu, and J.P. Wang. 2019. Development of an Axiom Sugarcane 100K SNP array for genetic map construction and QTL identification. Theoretical and Applied Genetics 132: 2829–2845.
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Aitken, K.S. History and Development of Molecular Markers for Sugarcane Breeding. Sugar Tech 24, 341–353 (2022). https://doi.org/10.1007/s12355-021-01000-7
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DOI: https://doi.org/10.1007/s12355-021-01000-7