A novel tetraploid S. spontaneum with basic chromosome x = 10 was discovered, providing us insights in the origin and evolution in Saccharum species.
Sugarcane (Saccharum spp., Poaceae) is a leading crop for sugar production providing 80% of the world’s sugar. However, the genetic and genomic complexities of this crop such as its high polyploidy level and highly variable chromosome numbers have significantly hindered the studies in deciphering the genomic structure and evolution of sugarcane. Here, we developed the first set of oligonucleotide (oligo)-based probes based on the S. spontaneum genome (x = 8), which can be used to simultaneously distinguish each of the 64 chromosomes of octaploid S. spontaneum SES208 (2n = 8x = 64) through fluorescence in situ hybridization (FISH). By comparative FISH assay, we confirmed the chromosomal rearrangements of S. spontaneum (x = 8) and S. officinarum (2n = 8x = 80), the main contributors of modern sugarcane cultivars. In addition, we examined a S. spontaneum accession, Np-X, with 2n = 40 chromosomes, and we found that it was a tetraploid with the unusual basic chromosome number of x = 10. Assays at the cytological and DNA levels demonstrated its close relationship with S. spontaneum with basic chromosome number x = 8 (the most common accessions in S. spontaneum), confirming its S. spontaneum identity. Population genetic structure and phylogenetic relationship analyses between Np-X and 64 S. spontaneum accessions revealed that Np-X belongs to the ancient Pan-Malaysia group, indicating a close relationship to S. spontaneum with basic chromosome number of x = 8. This finding of a tetraploid S. spontaneum with basic chromosome number of x = 10 suggested a parallel evolution path of genomes and polyploid series in S. spontaneum with different basic chromosome numbers.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Albert PS, Zhang T, Semrau K, Rouillard JM, Kao YH, Wang CR, Danilova TV, Jiang J, Birchler JA (2019) Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. Proc Natl Acad Sci USA 116:1679–1685
Beliveau BJ, Joyce EF, Apostolopoulos N, Yilmaz F, Fonseka CY, McCole RB, Chang Y, Li JB, Senaratne TN, Williams BR, Rouillard JM, Wu CT (2012) Versatile design and synthesis platform for visualizing genomes with oligopaint FISH probes. Proc Natl Acad Sci USA 109:21301–21306
Bellon H, Bůžek C, Gaudant J, Kvaček Z, Walther H (1998) The České Středohoří magmatic complex in Northern Bohemia 40 K-40Ar ages for volcanism and biostratigraphy of the cenozoic freshwater formations. Newsl Stratigr 36:77–103
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Bouckaert R, Heled J, Kühnert D, Vaughan T, Drummond AJ (2014) BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537
Boyle S, Rodesch MJ, Halvensleben HA, Jeddeloh JA, Bickmore WA (2011) Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosome Res 19:901–909
Braz GT, He L, Zhao H, Zhang T, Semrau K, Rouillard JM, Torres GA, Jiang J (2018) Comparative oligo-FISH mapping: an efficient and powerful methodology to reveal karyotypic and chromosomal evolution. Genetics 208:513–523
Bremer G (1961) Problems in breeding and cytology of sugar cane. Euphytica 10:59–78
Cuadrado A, Acevedo R, Díaz M, de 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
Daniels J, Roach BT (1987) Taxonomy and evolution. In: Heinz DJ (ed) Sugarcane improvement through breeding. Elsevier, Amsterdam, pp 7–84
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
D’Hont A, Lu YH, Feldmann P, Glaszmann JC (1993) Cytoplasmic diversity in sugar cane revealed by heterologous probes. Sugar Cane 1:12–25
D’Hont A, Grivet L, Feldmann P, Glaszmann JC, Rao S, Berding N (1996) Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics. Mol Gen Genet MGG 250:405–413
D’Hont A, Ison D, Alix K, Roux C, Glaszmann JC (1998) Determination of basic chromosome numbers in the genus Saccharum by physical mapping of ribosomal RNA genes. Genome 41:221–225
D’Hont A, Paulet F, Glaszmann JC (2002) Oligoclonal interspecific origin of ‘North Indian’ and ‘Chinese’ sugarcanes. Chromosome Res 10:253–262
Ebersberger I, Strauss S, Haeseler AV (2009) HaMStR: profile hidden markov model based search for orthologs in ESTs. BMC Evol Biol 9(1):157
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Garsmeur O, Droc G, Antonise R, Grimwood J, Potier B, Aitken K, Jenkins J, Martin G, Charron C, Hervouet C, Costet L, Yahiaoui N, Healey A, Sims D, Cherukuri Y, Sreedasyam A, Kilian A, Chan A, Van Sluys MA, Swaminathan K, Town C, Berges H, Simmons B, Glaszmann JC, van der Vossen E, Henry R, Schmutz J, D’Hont A (2018) A mosaic monoploid reference sequence for the highly complex genome of sugarcane. Nat Commun 9:2638
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Xian A, Lin F, Raychowdhury R, Zeng Q (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644–652
Ha S, Moore PH, Heinz D, Kato S, Ohmido N, Fukui K (1999) Quantitative chromosome map of the polyploid Saccharum spontaneum by multicolor fluorescence in situ hybridization and imaging methods. Plant Mol Biol 39:1165–1173
Han Y, Zhang T, Thammapichai P, Weng Y, Jiang J (2015) Chromosome-specific painting in cucumis species using bulked oligonucleotides. Genetics 200:771–779
Heinz D (1987) Sugarcane improvement through breeding. Elsevier, Amsterdam
Hou L, Xu M, Zhang T, Xu Z, Wang W, Zhang J, Yu M, Ji W, Zhu C, Gong Z, Gu M, Jiang J, Yu H (2018) Chromosome painting and its applications in cultivated and wild rice. BMC Plant Biol 18:110
Irvine JE (1999) Saccharum species as horticultural classes. Theor Appl Genet 98:186–194
Jannoo N, Grivet L, Seguin M, Paulet F, Domaingue R, Rao PS, Dookun A, D’Hont A, Glaszmann JC (1999) Molecular investigation of the genetic base of sugarcane cultivars. Theor Appl Genet 99:171–184
Jannoo N, Grivet L, Chantret N, Garsmeur O, Glaszmann JC, Arruda P, D’Hont A (2007) Orthologous comparison in a gene-rich region among grasses reveals stability in the sugarcane polyploid genome. Plant J 50:574–585
Jiang J (2019) Fluorescence in situ hybridization in plants: recent developments and future applications. Chromosome Res 27:153–165
Jiang J, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Lennoux CG (1939) Sugarcane collection in New Guinea during1937. Proc Int Soc Sugar Cane Technol 6:171–182
Li W (2006) Fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Lu YH, D’Hont A, Walker DIT, Rao PS, Feldmann P, Glaszmann JC (1994) Relationships among ancestral species of sugarcane revealed with RFLP using single copy maize nuclear probes. Euphytica 78:7–18
Mario DR, Ziheng Y (2011) Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times. Mol Biol Evol 28:2161–2172
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
Meng Z, Zhang Z, Yan T, Lin Q, Wang Y, Huang W, Huang Y, Li Z, Yu Q, Wang J, Wang K (2018) Comprehensively characterizing the cytological features of Saccharum spontaneum by the development of a complete set of chromosome-specific oligo probes. Front Plant Sci 9:1624
Ming R, Moore PH, Wu K-K, D’Hont A, Glaszmann JC, Tew TL, Mirkov TE, da Silva J, Jifon J, Rai M, Schnell RJ, Brumbley SM, Lakshmanan P, Comstock JC, Paterson AH (2010) Sugarcane improvement through breeding and biotechnology. Plant breeding reviews. Wiley, Hoboken, pp 15–118
Panje RR, Babu CN (1960) Studies in Saccharum spontaneum distribution and geographical association of chromosome numbers. Cytologia 25:152–172
Parthasarathy N (1948) Origin of noble sugar-canes (Saccharum officinarum L.). Nature 161(4094):608
Piperidis G, Piperidis N, D’Hont A (2010) Molecular cytogenetic investigation of chromosome composition and transmission in sugarcane. Mol Genet Genomics 284:65–73
Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842
Raghavan TS (1951) The sugarcanes of india: some cyto-genetic considerations. J Hered 42:199–206
Rithidech K, Ramirez DA (1974) Cytological survey of Saccharum spontaneum L. in the Philippines. Philipp Agric 5:205–224
Salvador CG, Silla-Martínez JM, Toni G (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973
Schenck S, Crepeau MW, Wu KK, Moore PH, Yu Q, Ming R (2004) Genetic diversity and relationships in native Hawaiian Saccharum officinarum sugarcane. J Hered 95:327–331
Schubert I (2007) Chromosome evolution. Curr Opin Plant Biol 10:109–115
Stevenson GC (1965) Genetics and breeding of sugar cane. Longmans, Green & Co., Ltd., London
Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA (2010) The age of the grasses and clusters of origins of C4 photosynthesis. Glob Change Biol 14:2963–2977
Wang K, Song X, Han Z, Guo W, Yu JZ, Sun J, Pan J, Kohel RJ, Zhang T (2006) Complete assignment of the chromosomes of Gossypium hirsutum L. by translocation and fluorescence in situ hybridization mapping. Theor Appl Genet 113:73–80
Wang J, Roe B, Macmil S, Yu Q, Murray JE, Tang H, Chen C, Najar F, Wiley G, Bowers J, Van Sluys M-A, Rokhsar DS, Hudson ME, Moose SP, Paterson AH, Ming R (2010) Microcollinearity between autopolyploid sugarcane and diploid sorghum genomes. BMC Genom 11:1–17
Xiang Y, Huang CH, Hu Y, Wen J, Li S, Yi T, Chen H, Xiang J, Ma H (2016) Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Mol Biol Evol 34:262
Xin H, Zhang T, Han Y, Wu Y, Shi J, Xi M, Jiang J (2018) Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma 127:313–321
Yamada NA, Rector LS, Tsang P, Carr E, Scheffer A, Sederberg MC, Aston ME, Ach RA, Tsalenko A, Sampas N, Peter B, Bruhn L, Brothman AR (2011) Visualization of fine-scale genomic structure by oligonucleotide-based high-resolution FISH. Cytogenet Genome Res 132:248–254
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
Yang QH, He SC (1996) Studies on Saccharum spontaneum chromosome numbers and geographical distribution in Yunnan, China. Sugarcane 3:10–13
Yu X-H, Wang X-H, Yang Q-H (2019) Genetic diversity and phylogenetic relationship of Saccharum spontaneum L. with different ploidy levels based on SRAP markers. Sugar Tech 21:802–814
Zeng L, Zhang Q, Sun R, Kong H, Zhang N, Ma H (2014) Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nat Commun 5:4956
Zhang J, Zhang X, Tang H, Zhang Q, Hua X, Ma X, Zhu F, Jones T, Zhu X, Bowers J, Wai CM, Zheng C, Shi Y, Chen S, Xu X, Yue J, Nelson DR, Huang L, Li Z, Xu H, Zhou D, Wang Y, Hu W, Lin J, Deng Y, Pandey N, Mancini M, Zerpa D, Nguyen JK, Wang L, Yu L, Xin Y, Ge L, Arro J, Han JO, Chakrabarty S, Pushko M, Zhang W, Ma Y, Ma P, Lv M, Chen F, Zheng G, Xu J, Yang Z, Deng F, Chen X, Liao Z, Zhang X, Lin Z, Lin H, Yan H, Kuang Z, Zhong W, Liang P, Wang G, Yuan Y, Shi J, Hou J, Lin J, Jin J, Cao P, Shen Q, Jiang Q, Zhou P, Ma Y, Zhang X, Xu R, Liu J, Zhou Y, Jia H, Ma Q, Qi R, Zhang Z, Fang J, Fang H, Song J, Wang M, Dong G, Wang G, Chen Z, Ma T, Liu H, Dhungana SR, Huss SE, Yang X, Sharma A, Trujillo JH, Martinez MC, Hudson M, Riascos JJ, Schuler M, Chen LQ, Braun DM, Li L, Yu Q, Wang J, Wang K, Schatz MC, Heckerman D, Van Sluys MA, Souza GM, Moore PH, Sankoff D, VanBuren R, Paterson AH, Nagai C, Ming R (2018) Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet 50:1565–1573
Zhang J, Zhang Q, Li L, Tang H, Zhang Q, Chen Y, Arrow J, Zhang X, Wang A, Miao C, Ming R (2019) Recent polyploidization events in three Saccharum founding species. Plant Biotechnol J 17:264–274
This work was supported by the National Natural Science Foundation of China (31771862), National Engineering Research Center of Sugarcane Open Fund (2017.1.5, NER2018.1.5) and State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources (SKLCUSA-b201808). We would like to thank National Field Genebank of Sugarcane Germplasm of China and National Infrastructure for Crop Germplasm Resources–Sugarcane platform of China for supplying us the S. spontaneum plants.
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
This article does not contain any studies that were performed with human participants or animals by any of the authors.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by Ian D Godwin.
About this article
Cite this article
Meng, Z., Han, J., Lin, Y. et al. Characterization of a Saccharum spontaneum with a basic chromosome number of x = 10 provides new insights on genome evolution in genus Saccharum. Theor Appl Genet 133, 187–199 (2020). https://doi.org/10.1007/s00122-019-03450-w