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

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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.

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References

  • 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 4:903–907

    Article  CAS  Google Scholar 

  • 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 108:759–764

    Article  CAS  Google Scholar 

  • Aulchenko YS (2015) GenABEL tutorial. https://doi.org/10.5821/zenodo.19738

  • Aulchenko YS, Ripke S, Isaacs A, Van Duijn CM (2007a) GenABEL: an R library for genome-wide association analysis. Bioinformatics 23:1294–1296

    Article  CAS  Google Scholar 

  • 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 177:577–585

    Article  CAS  Google Scholar 

  • 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:R62

    Article  Google Scholar 

  • 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 205:185–201

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 23:2633–2635

    Article  CAS  Google Scholar 

  • 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 447:661–678

    Article  CAS  Google Scholar 

  • Clayton DG et al (2005) Population structure, differential bias and genomic control in a large-scale, case–control association study. Nat Genet 37:1243–1246

    Article  CAS  Google Scholar 

  • 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 125:825–836

    Article  CAS  Google Scholar 

  • 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 92:1059–1064

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 127:1719–1732

    Article  CAS  Google Scholar 

  • 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 94:409–418

    Article  CAS  Google Scholar 

  • FAOSTAT, Food and Agriculture Organization of the United Nations, Statistics Division. http://faostat3.fao.org/compare/E. Accessed 21 Sept 2017

  • 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 157:48–56

    Article  Google Scholar 

  • 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 15:1451–1455

    Article  CAS  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 31:323–331

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 202:269–284

    Article  Google Scholar 

  • 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 178:1709–1723

    Article  Google Scholar 

  • 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 123:655–660

    Article  CAS  Google Scholar 

  • 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 15:379–383

    Article  Google Scholar 

  • Köhler K, Bickeböller H (2005) Structured association tests in case–control studies. Ann Hum Genet 69:768 (Abstract)

    Google Scholar 

  • Lander ES (1996) The new genomics; global views of biology. Science 274:536–539

    Article  CAS  Google Scholar 

  • Magarey RC (2006) Economic effects of diseases; regional variation in Queensland. Proc Aust Soc Sugar Cane Technol 28:226–231

    Google Scholar 

  • 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 23:274–280

    Google Scholar 

  • Magarey RC, Staier T, Willcox TG (2002) Fungicides for control or orange rust in the 2001 Queensland crop. Proc Aust Soc Sugar Cane Technol 24:269–274

    Google Scholar 

  • 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 44:1057–1064

    Article  Google Scholar 

  • 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 7:111–118

    Article  CAS  Google Scholar 

  • 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:e107351

    Article  Google Scholar 

  • Peng B, Kimmel M (2007) Simulations provide support for the common disease-common variant hypothesis. Genetics 175:763–776

    Article  CAS  Google Scholar 

  • 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 38:904–909

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 68:466–477

    Article  CAS  Google Scholar 

  • Śaunak S, Johannes F, Broman KW (2009) Selective genotyping and phenotyping strategies in a complex trait context. Genetics 181:1613–1626

    Article  Google Scholar 

  • Sood SG, Comstock JC, Glynn NC (2009) Leaf whorl inoculation method for screening sugarcane rust resistance. Plant Dis 93:1335–1340

    Article  Google Scholar 

  • 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 26:493–511

    Article  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 Genomics 11:261

    Article  Google Scholar 

  • 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 3:783–793

    CAS  Google Scholar 

  • 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 14:366–379

    Article  CAS  Google Scholar 

  • 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 53:973–981

    Article  Google Scholar 

  • William HM, Trethowan R, Crosby-Galvan EM (2007) Wheat breeding assisted by markers: CIMMYT’s experience. Euphytica 157:307–319

    Article  Google Scholar 

  • Xing C, Xing G (2009) Power of selective genotyping in genome-wide association studies of quantitative traits. BMC Proc 3:S23

    Article  Google Scholar 

  • Yang J, Zaitlen NA, Goddard ME, Visscher PM, Price AL (2014) Advantages and pitfalls in the application of mixed-model association methods. Nat Genet 46:100–106

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 13:134

    Article  CAS  Google Scholar 

  • 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 9:253

    Article  Google Scholar 

  • 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 38:203–208

    Article  Google Scholar 

  • Zhao D, Glynn NC, Glaz B, Comstock JC, Sood SG (2011) Orange rust effects on leaf photosynthesis and related characters of sugarcane. Plant Dis 95:640–647

    Article  CAS  Google Scholar 

  • 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 10:1–11

    Article  Google Scholar 

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Authors and Affiliations

  1. Formerly USDA-ARS Sugarcane Field Station, 12990 US Highway 441 North, Canal Point, FL, 33438, USA

    Per McCord & Jack Comstock

  2. Syngenta, Vero Beach Research Center, 7145 58th Avenue, Vero Beach, FL, 32967, USA

    Neil Glynn

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  1. Per McCord
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Correspondence to Per McCord.

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Jack Comstock: retired.

Electronic supplementary material

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10681_2019_2340_MOESM1_ESM.tiff

Rating system utilized to evaluate sugarcane genotypes after artificial inoculation with orange rust urediniospores (TIFF 248 kb)

10681_2019_2340_MOESM2_ESM.tiff

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)

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McCord, P., Glynn, N. & Comstock, J. Identifying markers for resistance to sugarcane orange rust (Puccinia kuehnii) via selective genotyping and capture sequencing. Euphytica 215, 150 (2019). https://doi.org/10.1007/s10681-019-2340-6

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