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Euphytica

, 215:150 | Cite as

Identifying markers for resistance to sugarcane orange rust (Puccinia kuehnii) via selective genotyping and capture sequencing

  • Per McCordEmail author
  • Neil Glynn
  • Jack Comstock
Article
  • 35 Downloads

Abstract

Sugarcane orange rust, caused by the fungus Puccinia kuehnii, is a serious disease of sugarcane. The most effective strategy to combat the disease is to develop resistant cultivars. Phenotypic screening for resistance is laborious, and breeders would benefit from molecular markers linked to the trait. The objective of this research was to identify, via association mapping, markers linked to resistance to orange rust. From the germplasm collection at Canal Point, Florida, 724 genotypes were screened for orange rust resistance via artificial inoculation of field-grown plants. A total of 38 susceptible and 37 resistant genotypes that were at or near the extremes of the population distribution were chosen for genotyping. Genotyping was accomplished via capture sequencing using 32,555 sugarcane probes anchored to the sorghum genome. Several methods were used to account for population structure and/or kinship. The most appropriate methods (determined by the genomic inflation factor) were mixed models and EIGENSTRAT. A total of 38 unique SNPs identified by these methods were then validated on 560 members of the population, using high resolution melting of PCR amplicons. Ten of these markers were statistically significant for the quantitative measure of rust severity, of which nine were also significant for the qualitative measure of ‘status’ (resistant/susceptible). The maximum amount of variation explained by any single marker was approximately 11%. This research has provided markers which can be deployed to help select superior parents for orange rust resistance, and also provided valuable insight for future research towards genetic control of orange rust in sugarcane.

Keywords

Association mapping Capture sequencing Sugarcane orange rust Selective genotyping 

Notes

Supplementary material

10681_2019_2340_MOESM1_ESM.tiff (249 kb)
Rating system utilized to evaluate sugarcane genotypes after artificial inoculation with orange rust urediniospores (TIFF 248 kb)
10681_2019_2340_MOESM2_ESM.tiff (23 kb)
A scree plot of within cluster sum of squares (WSS) vs. cluster (index) derived from k-means clustering of the plot of the first two principal components that were themselves derived from multidimensional scaling of the genomic kinship matrix (TIFF 23 kb)

References

  1. Albert JA, Molla MN, Muzny DM, Nazareth L, Wheeler D, Song X, Richmond TA, Middle CM, Rodesch MJ, Packard CJ, Weinstock GM, Gibbs RA (2007) Direct selection of human genomic loci by microarray hybridization. Nat Methods 4:903–907CrossRefGoogle Scholar
  2. Asnaghi C, Roques D, Ruffel S, Kaye C, Horau J-Y, Telismart H, Girard J, Raboin L, Risterucci A, Grivet L (2004) Targeted mapping of a sugarcane rust resistance gene (Bru1) using bulked segregant analysis and AFLP markers. Theor Appl Genet 108:759–764CrossRefGoogle Scholar
  3. Aulchenko YS (2015) GenABEL tutorial.  https://doi.org/10.5821/zenodo.19738
  4. Aulchenko YS, Ripke S, Isaacs A, Van Duijn CM (2007a) GenABEL: an R library for genome-wide association analysis. Bioinformatics 23:1294–1296CrossRefGoogle Scholar
  5. Aulchenko YS, De Koning DJ, Haley C (2007b) Genomewide rapid association using mixed model and regression: a fast and simple method for genomewide pedigree-based quantitative trait loci association analysis. Genetics 177:577–585CrossRefGoogle Scholar
  6. Bainbridge MN, Wang M, Burgess DL, Kovar C, Rodesch MJ, D’Ascenzo M, Kitzman J, Wu YQ, Newsham I, Richmond TA, Jeddeloh JA, Muzny D, Albert TJ, Gibbs RA (2010) Whole exome capture in solution with 3Gbp of data. Genome Biol 11:R62CrossRefGoogle Scholar
  7. Banerjee N, Siraree A, Yadav S, Kumar S, Singh J, Kumar S, Pandey DK, Singh RK (2015) Marker-trait association study for sucrose and yield in contributing traits in sugarcane (Saccharum spp. hybrid). Euphytica 205:185–201CrossRefGoogle Scholar
  8. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 89:10–19.  https://doi.org/10.1002/047114727.mb1910s89 CrossRefGoogle Scholar
  9. Bradbury PJ, Zhang Z, Droon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635CrossRefGoogle Scholar
  10. Burton PR, Clayton DG, Cardon LR, Craddock N et al (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3000 shared controls. Nature 447:661–678CrossRefGoogle Scholar
  11. Clayton DG et al (2005) Population structure, differential bias and genomic control in a large-scale, case–control association study. Nat Genet 37:1243–1246CrossRefGoogle Scholar
  12. Costet L, Le Cunff L, Royaert S, Raboin L-M, Hervouet C, Toubi L, Telismart H, Garsmeur O, Rousselle Y, Pauquet J, Nibouche S, Glaszmann J-C, Hoarau J-Y, D’Hont A (2012) Haplotype structure around Bru1 reveals a narrow genetic basis for brown rust resistance in modern sugarcane cultivars. Theor Appl Genet 125:825–836CrossRefGoogle Scholar
  13. Daugrois J, Grivet L, Roques D, Hoarau J-Y, Lombard H, Glaszmann J-C, D’Hont A (1996) A putative major gene for rust resistance linked with a RFLP marker in sugarcane cultivar ‘R570’. Theor Appl Genet 92:1059–1064CrossRefGoogle Scholar
  14. De Bakker PIW, Ferreira MAR, Jia X, Neale BM, Raychaudhuri S, Voight BF (2008) Practical aspects of imputation-driven meta-analysis of genome-wide association studies. Hum Mol Genet 17:R122–R128.  https://doi.org/10.1093/hmg/ddn288 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Debibakas S, Rocher S, Garsmeur O, Toubi L, Roques D, D’Hont A, Hoarau J-Y, Daugrois JH (2014) Prospecting sugarcane resistance to sugarcane yellow leaf virus by genome-wide association. Theor Appl Genet 127:1719–1732CrossRefGoogle Scholar
  16. Dufour P, Deu M, Grivet L, D’Hont A, Paulet F, Bouet A, Lanaud C, Glaszmann J-C, Hamon P (1997) Construction of a composite sorghum genome map and comparison with sugarcane, a related complex polyploid. Theor Appl Genet 94:409–418CrossRefGoogle Scholar
  17. FAOSTAT, Food and Agriculture Organization of the United Nations, Statistics Division. http://faostat3.fao.org/compare/E. Accessed 21 Sept 2017
  18. Fontanesi L, Buttazzoni L, Galimberti G, Calò DG, Scotti E, Russo V (2013) Association between melanocortin 4 receptor (MC4R) gene haplotypes and carcass and production traits in Italian Large Whit pigs evaluated with a selective genotyping approach. Livestock Sci 157:48–56CrossRefGoogle Scholar
  19. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, Miller W, Kent WJ, Nekrutenko A (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15:1451–1455CrossRefGoogle Scholar
  20. 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 31:323–331CrossRefGoogle Scholar
  21. Goecks J, Nekrutenko A, Taylor J, Team The Galaxy (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11:R86.  https://doi.org/10.1186/gb-2010-11-8-r86 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gouy M, Rousselle Y, Thong-Chane A, Anglade A, Royaert S, Nibouche S, Costet L (2015) Genome wide association mapping of agro-morphological and disease resistance traits in sugarcane. Euphytica 202:269–284CrossRefGoogle Scholar
  23. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ, Eskin E (2008) Efficient control of population structure in model organism association mapping. Genetics 178:1709–1723CrossRefGoogle Scholar
  24. Kimura T, Kobayashi T, Munkhbat B, Oyungerel G, Bilegtsaikhan T, Anar D, Jambaldorj J, Munkhsaikhan S, Munkhtuvshin N, Hayashi H, Oka A, Inoue I, Inoko H (2008) Genome-wide association analysis with selective genotyping identifies candidate loci for adult height at 8q21.13 and 15q22.33-q23 in Mongolians. Hum Genet 123:655–660CrossRefGoogle Scholar
  25. Klosowski AC, Bespalhok Fiho JC, Ruaro L, May De Mio LL (2013) Inheritance of resistance to orange rust (Puccinia kuehnii) in sugarcane families from crosses between parents with different orange rust reactions. Sugar Tech 15:379–383CrossRefGoogle Scholar
  26. Köhler K, Bickeböller H (2005) Structured association tests in case–control studies. Ann Hum Genet 69:768 (Abstract) Google Scholar
  27. Lander ES (1996) The new genomics; global views of biology. Science 274:536–539CrossRefGoogle Scholar
  28. Magarey RC (2006) Economic effects of diseases; regional variation in Queensland. Proc Aust Soc Sugar Cane Technol 28:226–231Google Scholar
  29. Magarey RC, Willcox TG, Croft B, Cordingley A (2001) Orange rust, a major pathogen affecting crops of Q124 in Queensland in 2000. Proc Aust Soc Sugar Cane Technol 23:274–280Google Scholar
  30. Magarey RC, Staier T, Willcox TG (2002) Fungicides for control or orange rust in the 2001 Queensland crop. Proc Aust Soc Sugar Cane Technol 24:269–274Google Scholar
  31. Magarey RC, Bull JI, Neilsen WA, Camilleri JR, Magnanini AJ (2004) Relating cultivar resistance to sugarcane yield using breeding selection trial analyses; orange rust and yellow spot. Aust J Exp Agric 44:1057–1064CrossRefGoogle Scholar
  32. Mamanova L, Coffey AJ, Scott CE, Kozarewa I, Turner EH, Kumar A, Howard E, Shendure J, Turner DJ (2010) Target-enrichment strategies for next-generation sequencing. Nat Methods 7:111–118CrossRefGoogle Scholar
  33. Nishiyama MY, Ferreira SS, Tang PZ, Becker S, Pörtner-Taliana A, Souza GM (2014) Full-length enriched cDNA libraries and ORFeome analysis of sugarcane hybrid and ancestor genotypes. PLoS ONE 9:e107351CrossRefGoogle Scholar
  34. Peng B, Kimmel M (2007) Simulations provide support for the common disease-common variant hypothesis. Genetics 175:763–776CrossRefGoogle Scholar
  35. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principle components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909CrossRefGoogle Scholar
  36. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181CrossRefGoogle Scholar
  37. Raid RN, Comstock JC, Glynn NC (2009) Evaluation of fungicides for control of orange rust on sugarcane. J Am Soc Sugar Cane Technol 29:82 (Abstract) Google Scholar
  38. Raid RN, Comstock JC, Glynn NC (2011) Yield loss incited by orange rust (Puccinia kuehnii) on a highly susceptible sugarcane cultivar in Florida. J Am Soc Sugar Cane Technol 31:66 (Abstract) Google Scholar
  39. Satten GA, Flanders WD, Yang Q (2001) Accounting for unmeasured population substructure in case–control studies of genetic association using a novel latent-class model. Am J Hum Genet 68:466–477CrossRefGoogle Scholar
  40. Śaunak S, Johannes F, Broman KW (2009) Selective genotyping and phenotyping strategies in a complex trait context. Genetics 181:1613–1626CrossRefGoogle Scholar
  41. Sood SG, Comstock JC, Glynn NC (2009) Leaf whorl inoculation method for screening sugarcane rust resistance. Plant Dis 93:1335–1340CrossRefGoogle Scholar
  42. Sun Y, Wang J, Crouch JH, Xu Y (2010) Efficiency of selective genotyping for genetic analysis of complex traits and potential applications in crop improvement. Mol Breed 26:493–511CrossRefGoogle Scholar
  43. 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 Genomics 11:261CrossRefGoogle Scholar
  44. Wang YH, Upadhyaya HD, Burrell AM, Sahraeian SME, Klein RR, Klein PE (2013) Genetic structure and linkage disequilibrium in a diverse, representative collection of the C4 model plant, Sorghum bicolor. Genes Genomes Genet 3:783–793Google Scholar
  45. Wang X, Mace E, Hunt C, Cruickshank A, Henzell R, Parkes H, Jordan D (2014) Two distinct classes of QTL determine rust resistance in sorghum. BMC Plant Biol 14:366–379CrossRefGoogle Scholar
  46. Wei X, Jackson PA, Hermann S, Kilian A, Heller-Uszynska K, Deomano E (2010) Simultaneously accounting for population structure, genotype by environment interaction, and spatial variation in marker-trait associations in sugarcane. Genome 53:973–981CrossRefGoogle Scholar
  47. William HM, Trethowan R, Crosby-Galvan EM (2007) Wheat breeding assisted by markers: CIMMYT’s experience. Euphytica 157:307–319CrossRefGoogle Scholar
  48. Xing C, Xing G (2009) Power of selective genotyping in genome-wide association studies of quantitative traits. BMC Proc 3:S23CrossRefGoogle Scholar
  49. Yang J, Zaitlen NA, Goddard ME, Visscher PM, Price AL (2014) Advantages and pitfalls in the application of mixed-model association methods. Nat Genet 46:100–106CrossRefGoogle Scholar
  50. Yang X, Islam MS, Sood S, Maya S, Hanson E, Comstock J, Wang J (2018) Identifying quantitative trait loci (QTLs) and developing diagnostic markers linked to orange rust resistance in sugarcane (Saccharum spp.). Front Plant Sci 9:350.  https://doi.org/10.3389/fpls.2018.00350 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinf 13:134CrossRefGoogle Scholar
  52. You FM, Huo N, Gu YQ, Luo MC, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinf 9:253CrossRefGoogle Scholar
  53. Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2005) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208CrossRefGoogle Scholar
  54. Zhao D, Glynn NC, Glaz B, Comstock JC, Sood SG (2011) Orange rust effects on leaf photosynthesis and related characters of sugarcane. Plant Dis 95:640–647CrossRefGoogle Scholar
  55. Zhao D, Davidson RW, Baltazar B, Comstock JC (2015) Field evaluation of sugarcane orange rust for first clonal stage of the CP cultivar development program. Am J Agric Biol Sci 10:1–11CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Formerly USDA-ARS Sugarcane Field StationCanal PointUSA
  2. 2.Syngenta, Vero Beach Research CenterVero BeachUSA

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