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Molecular insights into the origin of the brown rust resistance gene Bru1 among Saccharum species

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Analysis of 387 sugarcane clones using Bru 1 diagnostic markers revealed two possible sources of Bru 1 in Chinese cultivars: one from Saccharum spontaneum and another from Saccharum robustum of New Guinea.

Abstract

Sugarcane brown rust (SBR) is an important fungal disease in many sugarcane production areas around the world, and can cause considerable yield losses in susceptible sugarcane cultivars. One major SBR resistance gene, named Bru1, initially identified from cultivar R570, was shown to be a major SBR resistance source in most of the sugarcane producing areas of the world. In this study, by using the two Bru1-associated markers, R12H16 and 9O20-F4, we surveyed the presence of Bru1 in a Chinese sugarcane germplasm collection of 387 clones, consisting of 228 hybrid cultivars bred by different Chinese sugarcane breeding establishments, 54 exotic hybrid cultivars introduced from other countries and 105 clones of sugarcane ancestral species. The Bru1-bearing haplotype was detected in 43.4% of Chinese sugarcane cultivars, 20.4% of exotic hybrid cultivars, and only 3.8% of ancestral species. Among the 33 Chinese cultivars for which phenotypes of resistance to SBR were available, Bru1 was present in 69.2% (18/26) of the resistant clones. Analyses of the allelic sequence variations of R12H16 and 9O20-F4 suggested two possible sources of Bru1 in Chinese cultivars: one from S. spontaneum and another from S. robustum of New Guinea. In addition, we developed an improved Bru1 diagnostic marker, 9O20-F4-HaeIII, which can eliminate all the false results of 9O20-F4-RsaI observed among S. spontaneum, as well as a new dominant Bru1 diagnostic marker, R12E03-2, from the BAC ShCIR12E03. Our results provide valuable information for further efforts of breeding SBR-resistant varieties, searching new SBR resistance sources and cloning of Bru1 in sugarcane.

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References

  • Amalraj VA, Balasundaram N (2006) On the taxonomy of the members of ‘Saccharum complex’. Genet Resour Crop Evol 53:35–41

    Article  Google Scholar 

  • Asnaghi C, Paulet F, Kaye C, Grivet L, Deu M, Glaszmann JC, D’Hont A (2000) Application of synteny across Poaceae to determine the map location of a sugarcane rust resistance gene. Theor Appl Genet 101:962–969

    Article  CAS  Google Scholar 

  • Asnaghi C, D’hont A, Glaszmann J, Rott P (2001) Resistance of sugarcane cultivar R 570 to Puccinia melanocephala isolates from different geographic locations. Plant Dis 85:282–286

    Article  Google Scholar 

  • Asnaghi C, Roques D, Ruffel S, Kaye C, Hoarau JY, Telismart 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

    Article  CAS  PubMed  Google Scholar 

  • Bhatt SR, Gill SS (1985) The implications of 2n egg gametes in nobilization and breeding of sugarcane. Euphytica 34:377–384

    Article  Google Scholar 

  • Bremer G (1961a) Problems in breeding and cytology of sugarcane. I. A short history of sugarcane breeding—the original forms of Saccharum. Euphytica 10(1):59–78

    Article  Google Scholar 

  • Bremer G (1961b) Problems in breeding and cytology of sugarcane. II. The sugar cane breeding from a cytological view-point. Euphytica 10(2):121–258

    Google Scholar 

  • Canilha L, Chandel AK, Milessi TSS, Antunes FAF, Freitas WLC, Felipe MGA, Silva SS (2012) Bioconversion of sugarcane biomass into ethanol: an overview about composition, pretreatment methods, detoxification of hydrolysates, enzymatic saccharification and ethanol fermentation. J Biomed Biotechnol 8:989572

    Google Scholar 

  • Chandel AK, Silva SS, Carvalho W, Singh OV (2012) Sugarcane bagasse and leaves: foreseeable biomass of biofuel and bio-products. J Chem Technol Biotechnol 87:1–20

    Article  Google Scholar 

  • Comstock JC, Shine J Jr, Raid RN (1992) Effect of rust on sugarcane growth and biomass. Plant Dis 76:175–177

    Article  Google Scholar 

  • Comstock JC, Sood SG, Glynn NC, McKemy Shine JJJ, Castlebury LA (2008) First report of Puccinia kuehnii, causal agent of orange rust of sugarcane, in the United States and Western Hemisphere. Plant Dis 92:175

    Article  Google Scholar 

  • Costet L, Le Cunff L, Royaert S, Raboin LM, Hervouet C, Toubi L, Telismart H, Garsmeur O, Rousselle Y, Pauquet J, Nibouche S, Glaszmann JC, Hoarau JY, D’Hont A (2012) Haplotype structure around Bru1 reveals a narrow genetic basis for brown rust resistance in modern sugarcane cultivars. Theor Appl Genet 125(5):825–836

    Article  CAS  PubMed  Google Scholar 

  • D’Hont A, Grivet L, Feldmann P, Rao PS, Berding N (1996) Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp) by molecular cytogenetics. Mol Gen Genet 250:405–413

    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 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 

  • Daniels J, Daniels CA (1975) Geographical, historical and cultural aspects of the origin of the Indian and Chinese sugarcanes S. barberi and S. sinense. Sugarcane Breed Newslett 36:4–23

    Google Scholar 

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

    Chapter  Google Scholar 

  • Daniels J, Smith P, Paton N, Williams CA (1975) The origin of the genus Saccharum. Sugarcane Breed Newsett 36:24–39

    Google Scholar 

  • 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 a RFLP marker in sugarcane cultivar‘R570’. Theor Appl Genet 92:1059–1064

    Article  CAS  PubMed  Google Scholar 

  • Dean JL, Tai PYP, Todd EH (1979) Sugarcane rust in Florida. Sugar J 42:10

    Google Scholar 

  • D’Hont A, Lu YH, Feldmann P, Glaszmann JC (1993) Cytoplasmic diversity in sugarcane revealed by heterologous probes. Sugar Cane 1993(1):12–15

    Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Garsmeur O, Charron C, Bocs S, Jouffe V, Samain S, Couloux A, Droc G, Zini C, Glaszmann JC, Van Sluys MA, D’Hont A (2011) High homologous gene conservation despite extreme autopolyploid redundancy in sugarcane. New Phytol 189(2):629–642

    Article  CAS  PubMed  Google Scholar 

  • Glaszmann JC, Lu YH, Lanaud C (1990) Variation of nuclear ribosomal DNA in sugarcane. J Genet Breed 44:191–198

    Google Scholar 

  • Glynn NC, Laborde C, Davidson RW, Irey MS, Glaz B, D’Hont A, Comstock JC (2013) Utilization of a major brown rust resistance gene in sugarcane breeding. Mol Breed 31(2):323–331

    Article  CAS  Google Scholar 

  • Grivet L, Glaszmann JC, D’Hont A (2005) Molecular evidence of sugarcane evolution and domestication. In: Motley TJ, Zerega N, Cross H (eds) Darwin’s harvest: new approaches to the origins, evolution, and conservation of crops. Columbia University Press, New York, pp 49–66

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–99

    CAS  Google Scholar 

  • Hoarau JY, Offmann B, D’Hont A, Risterucci AM, Roques D, Glaszmann JC, Grivet L (2001) Genetic dissection of a modern sugarcane cultivar (Saccharum spp.). I. Genome mapping with AFLP markers. Theor Appl Genet 103:84–97

    Article  CAS  Google Scholar 

  • Hoy JW, Hollier CA (2009) Effect of brown rust on yield of sugarcane in Louisiana. Plant Dis 93:1171–1174

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, Mc Gettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947

    Article  CAS  PubMed  Google Scholar 

  • Le Cunff L, Garsmeur O, Raboin LM, Pauquet J, Telismart H, Selvi A, Grivet L, Philippe R, Begum D, Deu M, Costet L, Wing R, Glaszmann JC, D’Hont A (2008) Diploid/polyploid syntenic shuttle mapping and haplotype-specific chromosome walking toward a rust resistance gene (Bru1) in highly polyploid sugarcane (2n ~ 12x ~ 115). Genetics 180(1):649–660

    Article  PubMed  PubMed Central  Google Scholar 

  • Li WF, Wang XY, Huang YK, Zhang RY, Shan HL, Yin J, Luo ZM (2017) Molecular detection of Bru1 gene and identification of brown rust resistance in chinese sugarcane germplasm. Sugar Technol 19(2):183–190

    Article  CAS  Google Scholar 

  • Liu YQ, Li YP, Liang WH, Song QD, Qin XL, Ye L (2015) Current situation of sugar cane industry in the world. World Agriculture 2015(8):147–152

    Google Scholar 

  • Lu YH, D’Hont A, Walker DIT, Rao PS, Feldmann P, Glaszmann JC (1994a) Relationships among ancestral species of sugarcane revealed with RFLP using single copy maize nuclear probes. Euphytica 78:7–18

    Article  Google Scholar 

  • Lu YH, D’Hont A, Paulet F, Grivet L, Arnaud M, Glaszmann JC (1994b) Molecular diversity and genome structure in modern sugarcane varieties. Euphytica 78:216–226

    Article  Google Scholar 

  • Luo J, Pan YB, Xu L, Zhang H, Yuan Z, Deng Z, Chen R, Que Y (2014) Cultivar evaluation and essential test locations identification for sugarcane breeding in China. Sci World J 2014:302753

    Google Scholar 

  • Mukherjee SK (1957) Origin and distribution of Saccharum. Bot Gaz 119:55–61

    Article  Google Scholar 

  • Panje RR (1972) The role of Saccharum spontaneum in sugarcane breeding. Proc Int Soc Sugar Cane Technol 14:217–223

    Google Scholar 

  • Panje RR, Babu CN (1960) Studies in Saccharum spontaneum: distribution and geographic association of chromo-some numbers. Cytologia (Tokyo) 25:152–172

    Article  Google Scholar 

  • Parco AS, Avellaneda MC, Hale AH, Hoy JW, Kimbeng CA, Pontif MJ, Gravois KA, Baisakh N (2014) Frequency and distribution of the brown rust resistance gene Bru1 and implications for the Louisiana sugarcane breeding programme. Plant Breed 133(5):654–659

    Article  CAS  Google Scholar 

  • Peixoto-Junior RF, Creste S, Landell MGA, Nunes DS, Sanguino A, Campos MF, Vencovsky R, Tambarussi EV, Figueira A (2014) Genetic diversity among Puccinia melanocephala isolates from Brazil assessed using simple sequence repeat markers. Genet Mol Res 13(3):7852–7863

    Article  CAS  PubMed  Google Scholar 

  • Peng SG (1980) The general situation of evolution of sugarcane varieties at home and abroad. J South Agric 10:12–15

    Google Scholar 

  • Peng SG (1996) Varietal evolution of sugarcane in Taiwan. Southwest China J Agric Sci 9(1):117–124

    Google Scholar 

  • Piperidis G, Piperidis N, D’Hont A (2010) Molecular cytogenetic investigation of chromosome composition and transmission in sugarcane. Mol Genet Genom 284(1):65–73

    Article  CAS  Google Scholar 

  • Pocovi MII, Rech GE, Collavino NG, Caruso GB, Rios R, Mariotti JA (2010) Molecular diversity of Puccinia melanocephala populations. J Phytopathol 158:769–775

    Article  Google Scholar 

  • Price S (1968) Cytology of Chinese and North Indian sugarcanes. Econ Bot 22:155–164

    Article  Google Scholar 

  • Purdy LH, Liu JL, Dean JL (1983) Sugarcane rust, a newly important disease. Plant Dis 67:1292–1295

    Article  Google Scholar 

  • Que Y, Xu L, Wu Q, Liu Y, Ling H, Liu Y, Zhang Y, Guo J, Su Y, Chen J, Wang S, Zhang C (2014) Genome sequencing of Sporisorium scitamineum provides insights into the pathogenic mechanisms of sugarcane smut. BMC Genom 15:996

    Article  Google Scholar 

  • Raboin LM, Oliveira KM, Lecunff L, Telismart H, Roques D, Butterfield M, Hoarau JY, D’Hont A (2006) Genetic mapping in sugarcane, a high polyploid, using bi-parental progeny: identification of a gene controlling stalk colour and a new rust resistance gene. Theor Appl Genet 112:1382–1391

    Article  CAS  PubMed  Google Scholar 

  • Racedo J, Perera MF, Bertani R, Funes C, González V, Cuenya MI, D’Hont A, Welin B, Castagnaro AP (2013) Bru1 gene and potential alternative sources of resistance to sugarcane brown rust disease. Euphytica 191:429–436

    Article  CAS  Google Scholar 

  • Roach BT (1972) Nobilization of sugarcane. Proc Int Soc Sugar Cane Technol 14:206–216

    Google Scholar 

  • Roach BT (1977) Utilization of Saccharum spontaneum in sugarcane breeding. Proc Int Soc Sugar Cane Technol 16:43–57

    Google Scholar 

  • Ruan XY, Yan F, Sun CJ (1983) Occurrence of Puccinia erianthi on sugarcane in Yunnan province. Acta Mycologica Sinia 2:260–261

    Google Scholar 

  • Sreenivasan TV, Ahloowalia BS, Heinz DJ (1987) Cytogenetics. In: Heinz DJ (ed) Sugarcane improvement through breeding. Elsevier, Amsterdam, pp 143–210

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todd J, Glaz B, Burner D, Kimbeng C (2015) Historical use of cultivars as parents in Florida and Louisiana sugarcane breeding programs. Int Sch Res Not 2015:257417

    PubMed  PubMed Central  Google Scholar 

  • Wang XY, Li WF, Huang YK, Lu X, Luo ZH, Yin J, Shan HL, Zhang RY (2013) Evaluation of sugarcane introgression lines for resistance to brown rust disease caused by Puccinia melanocephala. Trop Plant Pathol 38(2):097–101

    Article  Google Scholar 

  • Wei Q, Yang BL, Gao ZJ (2015) Analysis of current situation of sugar cane industry. J Agric Mech Res 4:247–254

    Google Scholar 

  • Zhang XY (1996) Utilization of S. robustum descendants in sugarcane breeding. Sugarcane 3(1):14–18

    Google Scholar 

  • Zhang YX (2003) Sugarcane breeding strategies in Taiwan. Sugarcane Canesugar 2003(1):22–25

    Google Scholar 

  • Zhang Q, Qi YW, Zhang CM, Chen YS, Deng HH (2009) Pedigree analysis of genetic relationship among core parents of sugarcane in Mainland China. Guangdong Agric Sci 2009(10):44–48

    Google Scholar 

  • Zhang J, Sharma A, Yu Q, Wang J, Li L, Zhu L, Zhang X, Chen Y, Ming R (2016) Comparative structural analysis of Bru1 region homeologs in Saccharum spontaneum and S. officinarum. BMC Genom 17:446

    Article  CAS  Google Scholar 

  • Zhou M (2013) Conventional sugarcane breeding in South Africa: progress and future prospects. Am J Plant Sci 4:189–196

    Article  Google Scholar 

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Acknowledgements

This work was supported by a startup fund for distinguished scholars of Fujian Agriculture and Forestry University, and the Project of Education and Scientific Research of Young Teacher of Fujian (JA13102). The authors would like to thank Xin Lu for providing facilities and help in obtaining the leaf tissues from NNSGR.

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Authors and Affiliations

  1. Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Key Laboratory of Ministry of Agriculture for Sugarcane Biology and Genetic Breeding, College of Crop Science, Fujian Agriculture and Forestry University, Jinshan, Fuzhou, 350002, People’s Republic of China

    Heng-Bo Wang, Ping-Hua Chen, Yan-Qing Yang & Yun-Hai Lu

  2. CIRAD, UMR AGAP, 34398, Montpellier, France

    Angelique D’Hont

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  1. Heng-Bo Wang
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  2. Ping-Hua Chen
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  3. Yan-Qing Yang
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  4. Angelique D’Hont
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  5. Yun-Hai Lu
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Contributions

YL conceived and designed the experiments; HW, PC and YY conducted the experiments; HW and YL processed the data; YL wrote the manuscript; AD reviewed the manuscript; all authors read and approved the manuscript.

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Correspondence to Yun-Hai Lu.

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The authors declare that the experiments presented in this publication comply with the current laws of China and France.

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Informed consent was obtained from all individual participants included in the study.

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Communicated by Dr. Antonio Augusto Franco Garcia.

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Wang, HB., Chen, PH., Yang, YQ. et al. Molecular insights into the origin of the brown rust resistance gene Bru1 among Saccharum species. Theor Appl Genet 130, 2431–2443 (2017). https://doi.org/10.1007/s00122-017-2968-3

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