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Marker-trait association and epistasis for brown rust resistance in sugarcane

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Abstract

Sugarcane brown rust, caused by Puccinia melanocephala, is one of the major sugarcane diseases. The detection of molecular markers associated to brown rust resistance and also of its epistatic interactions were investigated in a mapping population obtained by crossing the brown rust susceptible clone IACSP953018 and the resistant cultivar IACSP933046. Resistance was evaluated in a field trial in plant cane and first ratoon under natural infection and scored using a diagrammatic scale from 1 (most resistance) to 9 (most susceptible). A total of 488 single dose markers (amplified fragment length polymorphism AFLP, genomic microsatellite gSSR and expressed sequence tag derived microsatellites EST-SSRs) were evaluated through a single marker trait association approach for brown rust resistance. Sixty one putative quantitative trait alleles (QTA) for brown rust (30 in plant cane, 31 in ratoon cane; 10 of them was common for both crop years) were detected of which several were related to resistance. Twenty one (34 %) of the markers associated to QTA derived from ESTs. Some of them have similarity to genes/proteins related to disease response pathways. The estimates of the proportion of the total phenotypic variation (\(\hat{R}^{2}\)) explained by each significant main QTA effect ranged from 1.84 to 7.22 %, while the total explained variance estimates were 37.25 % (plant cane) and 43.26 % (ratoon cane) considering all main significant QTA effects. Fifty significant digenic epistatic interactions were suggested with the majority (68 %) contributing to increase brown rust resistance. Together, these probable epistatic effects explain 16.26 % (plant cane) and 17.22 % (ratoon cane) of the total phenotypic variance. Although evidence of epistasis was observed, linkage cannot be ruled out as the majority of the markers involved in the digenic interaction could not be addressed to any linkage group. The results suggest that epistasis may have an important contribution on sugarcane resistance to brown rust.

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References

  • Aitken KS, Jackson PA, McIntyre CL (2005) A combination of AFLP and SSR markers provides extensive map coverage and identification of homo(eo)logous linkage groups in a sugarcane cultivar. Theor Appl Genet 110:789–801

    Article  CAS  PubMed  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Contr 19:716–723

    Article  Google Scholar 

  • Al-janabi SM, Parmessur Y, Kross H, Dhayan S, Saumtally S, Ramdoyal K, Autrey LJC, Dookun-Saumtally A (2007) Identification of a major quantitative trait locus (QTL) for yellow spot (Mycovellosiella koepkei) disease resistance in sugarcane. Mol Breed 19:1–14

    Article  Google Scholar 

  • Alves AA, Rosado CCG, Faria DA, Guimarães LMS, Lau D, Brommonschenkel SH, Grattapaglia D, Alfenas AC (2012) Genetic mapping provides evidence for the role of additive and non-additive QTLs in the response of inter-specific hybrids of Eucalyptus to Puccinia psidii rust infection. Euphytica 183:27–38

    Article  CAS  Google Scholar 

  • Alwala S, Kimbeng CA, Veremis JC, Gravois KA (2008) Linkage mapping and genome analysis in a Saccharum interspecific cross using AFLP, SRAP and TRAP markers. Euphytica 164:37–51

    Article  CAS  Google Scholar 

  • Amorim L (1987) Metodologia de Avaliação da Ferrugem da Cana-de-Açúcar (Puccinia melanocephala). Boletim Técnico Coopersucar 39:13–16

    Google Scholar 

  • Asnaghi C, Roques D, Ruffel S, Kaye C, Hoarau JY, Télismart H, Girard JC, Raboin LM, Risterucci M, 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 

  • Barker GLA, Edwards KJ (2009) A genome-wide analysis of single nucleotide polymorphism diversity in the world’s major cereal crops. Plant Biotechnol J 7:312–317

  • Bonferroni CE (1936) Teoria statistica delle classi e calcolo delle probabilit. Pubblicazioni del R Istituto Superiore di Scienze Economiche e Commerciali di Firenze 8:3–62

    Google Scholar 

  • Calenge F, Drouet D, Denancé C, Van de Weg WE, Brisset MN, Paulin JP, Durel CE (2005) Identification of a major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theor Appl Genet 111:128–135

    Article  CAS  PubMed  Google Scholar 

  • Comstock JC, Wu KK, Schnell RJ (1992) Heritability of resistance to sugar cane rust. Sugar Cane 6:7–10

    Google Scholar 

  • Copersucar (1986) Ferrugem da cana-de-açúcar e sua constatação no município de Capivari. Boletim técnicoCopersucar. São Paulo: Cooperativa Central dos produtores de açúcar e álcool do Estado de São Paulo. Edição especial. Dezembro de 1986, pp 3–8

  • 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 Gen 125:825–836

    Article  CAS  Google Scholar 

  • Creste S, Tulmann Neto A, Figueira A (2001) Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gel by silver staining. Plant Mol Biol 19:299–306

    Article  CAS  Google Scholar 

  • D’Hont A, Grivet L, Feldmann P, Rao S, Berding N, Glaszmann JC (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 

  • 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 RFLP marker in sugarcane cultivar R570. Theor Appl Gen 92:1059–1064

    Article  CAS  Google Scholar 

  • Federer WT (1956) Augmented (or hoonuiaku) designs, vol 2. Hawaiian Planters Record, Honolulu, pp 191–208

    Google Scholar 

  • Fethi B, Mohamed EG (2012) Impact of epistasis in inheritance of quantitative traits in crops, agricultural science. In: Godwin Aflakpui (ed), ISBN: 978-953-51-0567-1, InTech. http://www.intechopen.com/books/agricultural-science/impact-of-epistasis-in-inheritance-of-quantitative-traits-in-crops. Accessed 13 Aug 2013

  • Fethi B, Hanbary C, Mohamed EG (2011) Genetic adaptability of inheritance of resistance to biotic and abiotic stress level on crop: role of epistasis. Afr J Biotechnol 10:19913–19917

    Google Scholar 

  • Garcia AAF, Kido EA, Meza AN, Souza HMB, Pinto LR, Pastina MM, Leite CS, da Silva JA, Ulian EC, Figueira AV, Souza AP (2006) Development of an integrated genetic map of a sugarcane (Saccharum spp.) commercial cross, based on a maximum-likelihood approach for estimation of linkage and linkage phases. Theor Appl Genet 112:298–314

    Article  CAS  PubMed  Google Scholar 

  • Garcia AAF, Wang S, Melchinger AE, Zeng ZB (2008) Quantitative trait loci mapping and the genetic basis of heterosis in maize and rice. Genetics 180:1707–1724

    Article  PubMed Central  PubMed  Google Scholar 

  • Garcia AAF, Mollinari M, Marconi TG, Serang OR, Silva RR, Vieira MLC, Vicentini R, Costa EA, Mancini MC, Garcia MOS, Pastina MM, Gazaffi R, Martins ERF, Dahmer N, Sforça DA, Silva CBC, Bundock P, Henry RJ, Souza GM, van Sluys MA, Landell MGA, Carneiro MS, Vincentz MAG, Pinto LR, Vencovsky R, Souza AP (2013) SNP genotyping allows an in-depth characterisation of the genome of sugarcane and other complex autopolyploids. Sci Rep 3:3399. doi:10.1038/srep03399

    Article  PubMed Central  PubMed  Google Scholar 

  • Glynn NC, Comstock JC, McCorkle K (2012) Screening for resistance to brown rust of sugarcane: use of Bru1 resistance gene prospects and challenges. J Am Soc Sugar Cane Tech 32:82

    Google Scholar 

  • Grivet L, Arruda P (2002) Sugarcane genomics: depicting the complex genome of an important tropical crop. Curr Opin Plant Biol 5:122–127

  • Grivet L, D’Hont A, Roques D, Feldmann P, Lanaud C, Glaszmann C (1996) RFLP mapping in cultivated sugarcane (Saccharum spp.): genome organization in a highly polyploidy and aneuploid interspecific hybrid. Genetics 142:987–1000

    PubMed Central  CAS  PubMed  Google Scholar 

  • Henning JA, Townsend MS, Gent DA, Bassil N, Matthews P, Buck E, Beatson R (2011) QTL mapping of powdery mildew susceptibility in hop (Humulus lupulus L.). Euphytica 180:411–420

    Article  Google Scholar 

  • Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–802

    Article  Google Scholar 

  • Hogarth DM, Ryan CC, Taylor PWJ (1993) Quantitative inheritance of rust resistance in sugar cane. Field Crops Res 34:187–193

    Article  Google Scholar 

  • Hoisington D, Khairallah M, Gonzalez-De-Leon D (1994) Laboratory protocols. CIMMYT, Mexico

    Google Scholar 

  • Holland JB (2001) Epistasis and plant breeding. In: Janick J (ed) Plant breeding reviews, vol 21, Wiley, Oxford, UK

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Hotta CT, Lembke CG, Domingues DS, Ochoa EA, Cruz GMQ, Melotto-Passarin DM, Marconi TG, Santos MO, Mollinari M, Margarido GRA, Crivellari AC, Santos WD, Souza AP, Hoshino AA, Carrer H, Souza AP, Garcia AAF, Buckeridge MS, Menossi M, van Sluys MA, Souza GM (2010) The biotechnology roadmap for sugarcane improvement. Trop Plant Biol 3:75–87

    Article  CAS  Google Scholar 

  • Hoy JW, Hollier CA (2009) Effect of brown rust on sugarcane yield in Louisiana. Plant Dis 11:1171–1174

    Article  Google Scholar 

  • Huang XQ, Roder MS (2004) Molecular mapping of powdery mildew resistance genes in wheat: a review. Euphytica 137:203–223

    Article  CAS  Google Scholar 

  • Hussain F, Ashra M, Hameed MA, Hussain N, Sial RA (2011) Genetic studies in wheat for leaf rust resistance (Puccinia recondita). Afr J Biotechnol 10:3051–3054

    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 polyploidy sugarcane (2n ~ 12x ~ 115). Genetics 180:649–660

    Article  PubMed Central  PubMed  Google Scholar 

  • Lokko Y, Danquah EY, Offei SK, Dixon AGO, Gedil MA (2005) Molecular markers associated with a new source of resistance to the cassava mosaic disease. Afr J Biotechnol 4:873–881

    CAS  Google Scholar 

  • Marconi TG, Costa EA, Miranda KM, Mancini MC, Cardoso-Silva CB, Oliveira KM, Pinto LR, Mollinari M, Garcia AAF, Souza AP (2011) Functional markers for gene mapping and genetic diversity studies in sugarcane. BMC Res Notes 4:264

    Article  PubMed Central  PubMed  Google Scholar 

  • Margarido GRA, Souza AP, Garcia AAF (2007) OneMap:software for genetic mapping in outcrossing species. Hereditas 144:78–79

    Article  CAS  PubMed  Google Scholar 

  • McIntyre CL, Casu RE, Drenth J, Knight D, Whan VA, Croft BJ, Jordan DR, Manners JM (2005) Resistance genes analogues in sugarcane and their association with quantitative trait loci for rust resistance. Genome 48:391–400

    Article  CAS  PubMed  Google Scholar 

  • Mudge J, Andersen WR, Kehrer RL, Fairbanks DJ (1996) A RAPD genetic map of Saccharum officinarum. Crop Sci 36:1362–1366

    Article  CAS  Google Scholar 

  • Oliveira KM, Pinto LR, Marconi TG, Margarido GRA, Pastina MM, Teixeira LHM, Figueira AV, Ulian EC, Garcia AAF, Souza AP (2007) Functional integrated genetic linkage map based on EST-markers for a sugarcane (Saccharum spp.) commercial cross. Mol Breed 20:189–208

    Article  CAS  Google Scholar 

  • Oliveira KM, Pinto LR, Marconi TG, Mollinari M, Ulian EC, Chabregas SM, Falco MC, Burnquist W, Garcia AA, Souza AP (2009) Characterization of new polymorphic functional markers for sugarcane. Genome 52:191–209

    Article  CAS  PubMed  Google Scholar 

  • Pan YB (2006) Highly polymorphic microsatellite DNA markers for sugarcane germplasm evaluation and variety identity testing. Sugar Technol 8:246–256

    Article  CAS  Google Scholar 

  • Pinto LR, Oliveira KM, Ulian EC, Garcia AAF, Souza AP (2004) Survey in the sugarcane expressed sequence tag data base (SUCEST) for simple sequence repeats. Genome 47:795–804

    Article  CAS  PubMed  Google Scholar 

  • Pinto LR, Garcia AAF, Pastina MM, Teixeira LHM, Bressiani JA, Ulian EC, Bidoia MAP, Souza AP (2010) Analysis of genomic and functional RFLP derived markers associated with sucrose content, fiber and yield QTLs in a sugarcane (Saccharum spp.) commercial cross. Euphytica 172:313–327

    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 

  • Province MA (1999) Sequential methods of analysis for genome scan. In: Rao DC, Province MA (eds) Dissection of complex traits. Academic Press, San Diego, p 583

    Google Scholar 

  • Raboin LM, Oliveira KM, Le Cunff L, Telismart H, Rogues 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 

  • Ramdoyal K, Sullivan S, Lim S, Chong LCY, Badaloo GH, Saumtally S, Domaingue R (2000) The genetics of rust resistance in sugar cane seedling populations. Theor Appl Genet 100:557–563

    CAS  Google Scholar 

  • Rosewarne GM, Singh RP, Huerta-Espino J, Rebetzke GJ (2008) Quantitative trait loci for slow-rusting resistance in wheat to leaf rust and stripe rust identified with multi-environment analysis. Theor Appl Genet 116:1027–1034

    Article  CAS  PubMed  Google Scholar 

  • Rossi M, Araujo PG, Paulet F, Garsmeur O, Dias VM, Chen H (2003) Genomic distribution and characterization of EST-derived resistance gene analogs (RGAs) in sugarcane. Mol Genet Genomics 269:406–419

  • Rott P, Bailey RA, Comstock JC, Croft BJ, Saumtally AS (2000) A guide to sugarcane disease. Repères, France

    Google Scholar 

  • SAS Institute (1989) SAS/STAT user’s guide. Version 6, 4th edn. SAS Institute, Cary

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Serang O, Mollinari M, Garcia AAF (2012) Efficient exact maximum a posteriori computation for Bayesian SNP genotyping in polyploids. PLoS One 7:e30906

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. PNAS 100:9440–9445

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tai PYP, Miller JD, Dean JL (1981) Inheritance of resistance to rust in sugarcane. Field Crops Res 4:261–268

    Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu LX, Morgounov A, Wanyera R, Keser M, Singh SK, Sorrells M (2012) Identification of Ug99 stem rust resistance loci in winter wheat germplasm using genome-wide association analysis. Theor Appl Genet 125:749–758

    Article  PubMed  Google Scholar 

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Acknowledgments

Authors are grateful to the Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP, grants 2005/55258-6). B.S. Gonçalves and C.N.F. Medeiros received Scientific Initiation fellowship from FAPESP (2007/54631-0; 2009/51121-7 respectively) and F.R.C. dos Santos received doctorate fellowship from FAPESP (2009/51392-0).

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Correspondence to Luciana R. Pinto.

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Santos, F.R.C., Pinto, L.R., Carlini-Garcia, L.A. et al. Marker-trait association and epistasis for brown rust resistance in sugarcane. Euphytica 203, 533–547 (2015). https://doi.org/10.1007/s10681-014-1257-3

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