Skip to main content
SpringerLink
Log in

Characterization of a Saccharum spontaneum with a basic chromosome number of x = 10 provides new insights on genome evolution in genus Saccharum

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

A novel tetraploid S. spontaneum with basic chromosome x = 10 was discovered, providing us insights in the origin and evolution in Saccharum species.

Abstract

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 via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bremer G (1961) Problems in breeding and cytology of sugar cane. Euphytica 10:59–78

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Daniels J, Roach BT (1987) Taxonomy and evolution. In: Heinz DJ (ed) Sugarcane improvement through breeding. Elsevier, Amsterdam, pp 7–84

    Chapter  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Hont A, Lu YH, Feldmann P, Glaszmann JC (1993) Cytoplasmic diversity in sugar cane revealed by heterologous probes. Sugar Cane 1:12–25

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • D’Hont A, Paulet F, Glaszmann JC (2002) Oligoclonal interspecific origin of ‘North Indian’ and ‘Chinese’ sugarcanes. Chromosome Res 10:253–262

    Article  PubMed  Google Scholar 

  • Ebersberger I, Strauss S, Haeseler AV (2009) HaMStR: profile hidden markov model based search for orthologs in ESTs. BMC Evol Biol 9(1):157

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Zhang T, Thammapichai P, Weng Y, Jiang J (2015) Chromosome-specific painting in cucumis species using bulked oligonucleotides. Genetics 200:771–779

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heinz D (1987) Sugarcane improvement through breeding. Elsevier, Amsterdam

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Irvine JE (1999) Saccharum species as horticultural classes. Theor Appl Genet 98:186–194

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jiang J (2019) Fluorescence in situ hybridization in plants: recent developments and future applications. Chromosome Res 27:153–165

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068

    Article  CAS  PubMed  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lennoux CG (1939) Sugarcane collection in New Guinea during1937. Proc Int Soc Sugar Cane Technol 6:171–182

    Google Scholar 

  • Li W (2006) Fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mario DR, Ziheng Y (2011) Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times. Mol Biol Evol 28:2161–2172

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Panje RR, Babu CN (1960) Studies in Saccharum spontaneum distribution and geographical association of chromosome numbers. Cytologia 25:152–172

    Article  Google Scholar 

  • Parthasarathy N (1948) Origin of noble sugar-canes (Saccharum officinarum L.). Nature 161(4094):608

    Article  CAS  PubMed  Google Scholar 

  • Piperidis G, Piperidis N, D’Hont A (2010) Molecular cytogenetic investigation of chromosome composition and transmission in sugarcane. Mol Genet Genomics 284:65–73

    Article  CAS  PubMed  Google Scholar 

  • Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghavan TS (1951) The sugarcanes of india: some cyto-genetic considerations. J Hered 42:199–206

    Article  Google Scholar 

  • Rithidech K, Ramirez DA (1974) Cytological survey of Saccharum spontaneum L. in the Philippines. Philipp Agric 5:205–224

    Google Scholar 

  • Salvador CG, Silla-Martínez JM, Toni G (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Schubert I (2007) Chromosome evolution. Curr Opin Plant Biol 10:109–115

    Article  CAS  PubMed  Google Scholar 

  • Stevenson GC (1965) Genetics and breeding of sugar cane. Longmans, Green & Co., Ltd., London

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Yang QH, He SC (1996) Studies on Saccharum spontaneum chromosome numbers and geographical distribution in Yunnan, China. Sugarcane 3:10–13

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China

    Zhuang Meng, Jinlei Han, Yujing Lin, Qingfang Lin, Xiaokai Ma, Jianping Wang, Liangsheng Zhang & Kai Wang

  2. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Lab for Sugarcane Biology, Guangxi University, Nanning, Guangxi, China

    Muqing Zhang & Kai Wang

  3. Sugarcane Research Institution, Yunnan Agricultural University, Kunming, Yunnan, China

    Qinghui Yang

  4. State Key Laboratory of Genetic Engineering and Ministry of Education Key Laboratory of Biodiversity Sciences and Ecological Engineering, Institute of Plant Biology, Institute of Biodiversity Sciences, School of Life Sciences, Fudan University, Shanghai, China

    Yiyong Zhao

  5. Department of Agronomy, University of Florida, Gainesville, FL, 32611, USA

    Jianping Wang

Authors
  1. Zhuang Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jinlei Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yujing Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yiyong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qingfang Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaokai Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jianping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Muqing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Liangsheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qinghui Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KW and QY designed the research and drafted manuscript. ZM, YL, YZ, QL, JH, and XM conducted the experiments. ZM, KW and JH designed chromosome-specific oligo probes. KW, QY, YZ, LZ, JW, and MZ participated in the data analysis and manuscript preparation. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Qinghui Yang or Kai Wang.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical approval

This article does not contain any studies that were performed with human participants or animals by any of the authors.

Additional information

Communicated by Ian D Godwin.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-019-03450-w

Search

Navigation