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

  • Zhuang Meng
  • Jinlei Han
  • Yujing Lin
  • Yiyong Zhao
  • Qingfang Lin
  • Xiaokai Ma
  • Jianping Wang
  • Muqing Zhang
  • Liangsheng Zhang
  • Qinghui YangEmail author
  • Kai WangEmail author
Original Article

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.

Notes

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 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.

Compliance with ethical standards

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.

Supplementary material

122_2019_3450_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 15 kb)
122_2019_3450_MOESM2_ESM.docx (14 kb)
Supplementary material 2 (DOCX 13 kb)
122_2019_3450_MOESM3_ESM.pdf (915 kb)
Supplementary material 3 (PDF 914 kb)

References

  1. 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 116:1679–1685CrossRefGoogle Scholar
  2. 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 109:21301–21306CrossRefGoogle Scholar
  3. 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 36:77–103CrossRefGoogle Scholar
  4. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle Scholar
  5. Bouckaert R, Heled J, Kühnert D, Vaughan T, Drummond AJ (2014) BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537CrossRefGoogle Scholar
  6. 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 19:901–909CrossRefGoogle Scholar
  7. 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 208:513–523CrossRefGoogle Scholar
  8. Bremer G (1961) Problems in breeding and cytology of sugar cane. Euphytica 10:59–78CrossRefGoogle Scholar
  9. 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 55:847–854CrossRefGoogle Scholar
  10. Daniels J, Roach BT (1987) Taxonomy and evolution. In: Heinz DJ (ed) Sugarcane improvement through breeding. Elsevier, Amsterdam, pp 7–84CrossRefGoogle Scholar
  11. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefGoogle Scholar
  12. D’Hont A, Lu YH, Feldmann P, Glaszmann JC (1993) Cytoplasmic diversity in sugar cane revealed by heterologous probes. Sugar Cane 1:12–25Google Scholar
  13. 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 250:405–413CrossRefGoogle Scholar
  14. 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 41:221–225CrossRefGoogle Scholar
  15. D’Hont A, Paulet F, Glaszmann JC (2002) Oligoclonal interspecific origin of ‘North Indian’ and ‘Chinese’ sugarcanes. Chromosome Res 10:253–262CrossRefGoogle Scholar
  16. Ebersberger I, Strauss S, Haeseler AV (2009) HaMStR: profile hidden markov model based search for orthologs in ESTs. BMC Evol Biol 9(1):157CrossRefGoogle Scholar
  17. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefGoogle Scholar
  18. 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 9:2638CrossRefGoogle Scholar
  19. 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 29:644–652CrossRefGoogle Scholar
  20. 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 39:1165–1173CrossRefGoogle Scholar
  21. Han Y, Zhang T, Thammapichai P, Weng Y, Jiang J (2015) Chromosome-specific painting in cucumis species using bulked oligonucleotides. Genetics 200:771–779CrossRefGoogle Scholar
  22. Heinz D (1987) Sugarcane improvement through breeding. Elsevier, AmsterdamGoogle Scholar
  23. 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 18:110CrossRefGoogle Scholar
  24. Irvine JE (1999) Saccharum species as horticultural classes. Theor Appl Genet 98:186–194CrossRefGoogle Scholar
  25. 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 99:171–184CrossRefGoogle Scholar
  26. 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 50:574–585CrossRefGoogle Scholar
  27. Jiang J (2019) Fluorescence in situ hybridization in plants: recent developments and future applications. Chromosome Res 27:153–165CrossRefGoogle Scholar
  28. Jiang J, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068CrossRefGoogle Scholar
  29. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359CrossRefGoogle Scholar
  30. Lennoux CG (1939) Sugarcane collection in New Guinea during1937. Proc Int Soc Sugar Cane Technol 6:171–182Google Scholar
  31. Li W (2006) Fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658CrossRefGoogle Scholar
  32. 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 25:2078–2079CrossRefGoogle Scholar
  33. 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 78:7–18CrossRefGoogle Scholar
  34. Mario DR, Ziheng Y (2011) Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times. Mol Biol Evol 28:2161–2172CrossRefGoogle Scholar
  35. 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 20:1297–1303CrossRefGoogle Scholar
  36. 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 9:1624CrossRefGoogle Scholar
  37. 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 15–118Google Scholar
  38. Panje RR, Babu CN (1960) Studies in Saccharum spontaneum distribution and geographical association of chromosome numbers. Cytologia 25:152–172CrossRefGoogle Scholar
  39. Parthasarathy N (1948) Origin of noble sugar-canes (Saccharum officinarum L.). Nature 161(4094):608CrossRefGoogle Scholar
  40. Piperidis G, Piperidis N, D’Hont A (2010) Molecular cytogenetic investigation of chromosome composition and transmission in sugarcane. Mol Genet Genomics 284:65–73CrossRefGoogle Scholar
  41. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842CrossRefGoogle Scholar
  42. Raghavan TS (1951) The sugarcanes of india: some cyto-genetic considerations. J Hered 42:199–206CrossRefGoogle Scholar
  43. Rithidech K, Ramirez DA (1974) Cytological survey of Saccharum spontaneum L. in the Philippines. Philipp Agric 5:205–224Google Scholar
  44. Salvador CG, Silla-Martínez JM, Toni G (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973CrossRefGoogle Scholar
  45. 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 95:327–331CrossRefGoogle Scholar
  46. Schubert I (2007) Chromosome evolution. Curr Opin Plant Biol 10:109–115CrossRefGoogle Scholar
  47. Stevenson GC (1965) Genetics and breeding of sugar cane. Longmans, Green & Co., Ltd., LondonGoogle Scholar
  48. 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 14:2963–2977CrossRefGoogle Scholar
  49. 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 113:73–80CrossRefGoogle Scholar
  50. 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 11:1–17CrossRefGoogle Scholar
  51. 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 34:262PubMedCentralGoogle Scholar
  52. 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 127:313–321CrossRefGoogle Scholar
  53. 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 132:248–254CrossRefGoogle Scholar
  54. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591CrossRefGoogle Scholar
  55. Yang QH, He SC (1996) Studies on Saccharum spontaneum chromosome numbers and geographical distribution in Yunnan, China. Sugarcane 3:10–13Google Scholar
  56. 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 21:802–814CrossRefGoogle Scholar
  57. 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 5:4956CrossRefGoogle Scholar
  58. 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 50:1565–1573CrossRefGoogle Scholar
  59. 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 17:264–274CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems BiologyFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Lab for Sugarcane BiologyGuangxi UniversityNanningChina
  3. 3.Sugarcane Research InstitutionYunnan Agricultural UniversityKunmingChina
  4. 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 SciencesFudan UniversityShanghaiChina
  5. 5.Department of AgronomyUniversity of FloridaGainesvilleUSA

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