Artículo

Zubrzycki, J.E.; Maringolo, C.A.; Filippi, C.V.; Quiróz, F.J.; Nishinakamasu, V.; Puebla, A.F.; Julio, A.D.R.; Escande, A.; Lia, V.V.; Heinz, R.A.; Hopp, H.E.; Cervigni, G.D.L.; Paniego, N.B. "Main and epistatic QTL analyses for Sclerotinia Head Rot resistance in sunflower" (2017) PLoS ONE. 12(12)
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Sclerotinia Head Rot (SHR), a disease caused by Sclerotinia sclerotiorum, is one of the most limiting factors in sunflower production. In this study, we identified genomic loci associated with resistance to SHR to support the development of assisted breeding strategies. We genotyped 114 Recombinant Inbred Lines (RILs) along with their parental lines (PAC2 –partially resistant–and RHA266 –susceptible–) by using a 384 single nucleotide polymorphism (SNP) Illumina Oligo Pool Assay to saturate a sunflower genetic map. Subsequently, we tested these lines for SHR resistance using assisted inoculations with S. sclerotiorum ascospores. We also conducted a randomized complete-block assays with three replicates to visually score disease incidence (DI), disease severity (DS), disease intensity (DInt) and incubation period (IP) through four field trials (2010–2014). We finally assessed main effect quantitative trait loci (M-QTLs) and epistatic QTLs (E-QTLs) by composite interval mapping (CIM) and mixed-model-based composite interval mapping (MCIM), respectively. As a result of this study, the improved map incorporates 61 new SNPs over candidate genes. We detected a broad range of narrow sense heritability (h 2 ) values (1.86–59.9%) as well as 36 M-QTLs and 13 E-QTLs along 14 linkage groups (LGs). On LG1, LG10, and LG15, we repeatedly detected QTLs across field trials; which emphasizes their putative effectiveness against SHR. In all selected variables, most of the identified QTLs showed high determination coefficients, associated with moderate to high heritability values. Using markers shared with previous Sclerotinia resistance studies, we compared the QTL locations in LG1, LG2, LG8, LG10, LG11, LG15 and LG16. This study constitutes the largest report of QTLs for SHR resistance in sunflower. Further studies focusing on the regions in LG1, LG10, and LG15 harboring the detected QTLs are necessary to identify causal alleles and contribute to unraveling the complex genetic basis governing the resistance. © 2017 Zubrzycki et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Registro:

Documento: Artículo
Título:Main and epistatic QTL analyses for Sclerotinia Head Rot resistance in sunflower
Autor:Zubrzycki, J.E.; Maringolo, C.A.; Filippi, C.V.; Quiróz, F.J.; Nishinakamasu, V.; Puebla, A.F.; Julio, A.D.R.; Escande, A.; Lia, V.V.; Heinz, R.A.; Hopp, H.E.; Cervigni, G.D.L.; Paniego, N.B.
Filiación:Instituto de Biotecnología, Centro de Investigaciones en Ciencias Agronómicas y Veterinarias, Instituto Nacional de Tecnología Agropecuaria, Hurlingham, Buenos Aires, Argentina
Laboratorio de Patología Vegetal, Unidad Integrada Universidad Nacional de Mar del Plata, Estación Experimental Agropecuaria INTA Balcarce, Balcarce, Buenos Aires, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas, Ciudad Autónoma de Buenos Aires, Argentina
Cátedra de Estadística y Biometría, Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba, Córdoba, Argentina
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos, Aires, Argentina
Centro de Estudios Fotosintéticos y Bioquímicos, Rosario, Santa Fe, Argentina
Biocódices,, San Martín, Buenos Aires, Argentina
Palabras clave:amplified fragment length polymorphism; Argentina; Article; breeding; controlled study; disease severity; epistasis; gene locus; gene mapping; genetic linkage; genotype; incidence; incubation time; inoculation; nonhuman; quantitative trait locus; restriction fragment length polymorphism; Sclerotinia sclerotiorum; scoring system; sequence tagged site; single nucleotide polymorphism; sunflower; Ascomycetes; chromosomal mapping; disease resistance; genetic marker; genetics; inbreeding; microbiology; phenotype; physiology; plant disease; quantitative trait locus; Ascomycota; Chromosome Mapping; Disease Resistance; Epistasis, Genetic; Genetic Linkage; Genetic Markers; Genotype; Helianthus; Inbreeding; Phenotype; Plant Diseases; Polymorphism, Single Nucleotide; Quantitative Trait Loci
Año:2017
Volumen:12
Número:12
DOI: http://dx.doi.org/10.1371/journal.pone.0189859
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CODEN:POLNC
CAS:Genetic Markers
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v12_n12_p_Zubrzycki

Referencias:

  • Gulya, T., Rashid, K.Y., Masirevic, S.M., Sunflower diseases (1997) Sunflower Technology and Production, pp. 263-379. , https://doi.org/10.2134/agronmonogr35.c6, Berglund DR, editor. American Society of Agronomy Monograph
  • Moschini, R.C., Escande, A.R., Pereyra, V.R., Pedraza, M.V., Quiroz, F., Troglia, C., Predicción de la inci-dencia de la podredumbre blanda del capítulo de girasol en base a factores ambientales y genéticos (2002) Rev Arg Agrometeorol, 2, pp. 51-57. , Spanish
  • Markell, S.G., Harveson, R.M., Block, C.C., Gulya, T.J., (2015) Sunflower Diseases, pp. 93-128. , Sunflower. Elsevier
  • Škorić, D., Sunflower breeding for resistance to abiotic and biotic stresses (2016) Abiotic and Biotic Stress in Plants—Recent Advances and Future Perspectives, , https://doi.org/10.5772/62159, Tech
  • Gentzbittel, L., Mestries, E., Mouzeyar, S., Mazeyrat, F., Badaoui, S., Vear, F., A composite map of expressed sequences and phenotypic traits of the sunflower (Helianthus annuus L.) genome (1999) Theor Appl Genet, 99, pp. 218-234. , https://doi.org/10.1007/s001220051228
  • Paniego, N., Echaide, M., Muñoz, M., Fernández, L., Torales, S., Faccio, P., Microsatellite isolation and characterization in sunflower (Helianthus annuus L.) (2002) Genome, 43, pp. 34-43. , https://doi.org/10.1139/G01-120
  • Tang, S., Yu, J.-K., Slabaugh, B., Shintani, K., Knapp, J., Simple sequence repeat map of the sunflower genome (2002) Theor Appl Genet, 105, pp. 1124-1136. , https://doi.org/10.1007/s00122-002-0989-y, PMID: 12582890
  • Tang, S., Kishore, V.K., Knapp, S.J., PCR-multiplexes for a genome-wide framework of simple sequence repeat marker loci in cultivated sunflower (2003) Theor Appl Genet, 107, pp. 6-19. , https://doi.org/10.1007/s00122-003-1233-0, PMID: 12835928
  • Yu, J.-K., Tang, S., Slabaugh, M.B., Heesacker, A., Cole, G., Herring, M., Towards a saturated molecular genetic linkage map for cultivated sunflower (2003) Crop Sci, 43, pp. 367-387. , https://doi.org/10.2135/cropsci2003.0367
  • Talia, P., Nishinakamasu, V., Hopp, H.E., Heinz, R.A., Paniego, N.B., Genetic mapping of EST-SSRs, SSR and InDels to improve saturation of genomic regions in a previously developed sunflower map (2010) Electron J Biotechnol, 13. , https://doi.org/10.2225/vol13-issue6-fulltext-14
  • Bachlava, E., Taylor, C.A., Tang, S., Bowers, J.E., Mandel, J.R., Burke, J.M., SNP Discovery and development of a high-density genotyping array for sunflower (2012) PLoS One, 7. , https://doi.org/10.1371/journal.pone.0029814, PMID: 22238659
  • Bowers, J.E., Bachlava, E., Brunick, R.L., Rieseberg, L.H., Knapp, S.J., Burke, J.M., Development of a 10,000 locus genetic map of the sunflower genome based on multiple crosses (2012) G3, 2, pp. 721-729. , https://doi.org/10.1534/g3.112.002659, Bethesda). PMID: 22870395
  • Mandel, J.R., Nambeesan, S., Bowers, J.E., Marek, L.F., Ebert, D., Rieseberg, L.H., Association mapping and the genomic consequences of selection in sunflower (2013) PLoS Genet, 9. , https://doi.org/10.1371/journal.pgen.1003378, Springer NM, editor. PMID: 23555290
  • Talukder, Z.I., Hulke, B.S., Qi, L., Scheffler, B.E., Pegadaraju, V., McPhee, K., Candidate gene association mapping of Sclerotinia stalk rot resistance in sunflower (Helianthus annuus L.) uncovers the importance of COI1 homologs (2014) Theor Appl Genet, 127, pp. 193-209. , https://doi.org/10.1007/s00122-013-2210-x, PMID: 24193356
  • Hulke, B.S., Grassa, C.J., Bowers, J.E., Burke, J.M., Qi, L., Talukder, Z.I., A unified single nucleotide polymorphism map of sunflower (L.) derived from current genomic resources (2015) Crop Sci, 55, pp. 1696-1702. , https://doi.org/10.2135/cropsci2014.11.0752
  • Livaja, M., Unterseer, S., Erath, W., Lehermeier, C., Wieseke, R., Plieske, J., Diversity analysis and genomic prediction of sclerotinia resistance in sunflower using a new 25 K SNP genotyping array (2015) Theor Appl Genet, 129, pp. 317-329. , https://doi.org/10.1007/s00122-015-2629-3, PMID: 26536890
  • Roux, F., Voisin, D., Badet, T., Balagué, C., Barlet, X., Huard-Chauveau, C., Resistance to phytopatho-gens e tutti quanti: Placing plant quantitative disease resistance on the map (2014) Mol Plant Pathol, 15, pp. 427-432. , https://doi.org/10.1111/mpp.12138, PMID: 24796392
  • Gentzbittel, L., Mouzeyar, S., Badaoui, S., Mestries, E., Vear, F., De Labrouhe, T.D., Cloning of molecular markers for disease resistance in sunflower, Helianthus annuus L (1998) Theor Appl Genet, 96, pp. 519-525. , https://doi.org/10.1007/s001220050769, Springer; PMID: 24710892
  • Maringolo, C., (2007) Regiones Cromosómicas Asociadas A Resistencia A Podredumbre Húmeda Del Capítulo De Girasol, , Sclerotinia sclerotiorum (Lib.) de Bary). Posgrado en Producción Vegetal. Universidad Nacional de Mar del Plata. Facultad de Ciencias Agrarias, Unidad Integrada Balcarce Argentina
  • Yue, B., Radi, S.A., Vick, B.A., Cai, X., Tang, S., Knapp, S.J., Identifying quantitative trait loci for resistance to sclerotinia head rot in two USDA sunflower germplasms (2008) Phytopathology, 98, pp. 926-931. , https://doi.org/10.1094/PHYTO-98-8-0926, PMID: 18943211
  • Bert, P.F., Dechamp-Guillaume, G., Serre, F., Jouan, I., De Labrouhe, D.T., Nicolas, P., Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.) (2004) Theor Appl Genet, 109, pp. 865-874. , https://doi.org/10.1007/s00122-004-1701-1, PMID: 15141292
  • Mestries, E., Gentzbittel, L., De Labrouhe, T.D., Nicolas, P., Vear, F., Analyses of quantitative trait loci associated with resistance to Sclerotinia sclerotiorum in sunflowers (Helianthus annuus L.) using molecular markers (1998) Mol Breed, 4, pp. 215-226. , https://doi.org/10.1023/A:1009694626992
  • Ingvarsson, P.K., Street, N.R., Association genetics of complex traits in plants (2011) New Phytol, 189, pp. 909-922. , https://doi.org/10.1111/j.1469-8137.2010.03593.x, PMID: 21182529
  • Desgroux, A., L’Anthoëne, V., Roux-Duparque, M., Rivière, J.-P., Aubert, G., Tayeh, N., Genome-wide association mapping of partial resistance to Aphanomyces euteiches in pea (2016) BMC Genomics, 17, p. 124. , https://doi.org/10.1186/s12864-016-2429-4, PMID: 26897486
  • Fusari, C.M., Rienzo, D.J.A., Troglia, C., Nishinakamasu, V., Moreno, M., Maringolo, C., Association mapping in sunflower for sclerotinia head rot resistance (2012) BMC Plant Biol, 12, p. 93. , https://doi.org/10.1186/1471-2229-12-93, PMID: 22708963
  • Gentzbittel, L., Vear, F., Zhang, Y.-X., Bervillé, A., Nicolas, P., Development of a consensus linkage RFLP map of cultivated sunflower (Helianthus annuus L.) (1995) Theor Appl Genet, 90, pp. 1079-1086. , https://doi.org/10.1007/BF00222925, PMID: 24173066
  • Escande, A.R., Laich, F.S., Pedraza, M.V., Field testing of honeybee-dispersed Trichoderma spp. To manage sunflower head rot (Sclerotinia sclerotiorum) (2002) Plant Pathol, 51, pp. 346-351. , https://doi.org/10.1046/j.1365-3059.2002.00723.x
  • Schneiter, A.A., Miller, J.F., Description of sunflower growth stages (1981) Crop Sci. Crop Science Society of America, 21, p. 901. , https://doi.org/10.2135/cropsci1981.0011183X002100060024x
  • Van Becelaere, G., Miller, J.F., Methods of inoculation of sunflower heads with Sclerotinia sclerotiorum (2004) Helia, 27, pp. 137-142. , https://doi.org/10.2298/HEL0441137V
  • Filippi, C.V., Zubrzycki, J.E., Rienzo, D.J.A., Quiroz, F., Fusari, C.M., Alvarez, D., Phenotyping sunflower genetic resources for sclerotinia head rot response: Assessing variability for disease resistance breeding (2017) Plant Dis, pp. PDIS–12–16–1784. , https://doi.org/10.1094/PDIS-12-16-1784-RE
  • Gonçalves, E., Carrasquinho, I., St. Aubyn, A., Martins, A., Broad-sense heritability in mixed models for grapevine initial selection trials (2013) Euphytica, 189, pp. 379-391. , https://doi.org/10.1007/s10681-012-0787-9
  • Rienzo, D.J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M., Robledo, C.W., (2015) InfoStat. Version 2015, , http://www.infostat.com.ar, Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina
  • Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., (2017) Nlme: Linear and Nonlinear Mixed Effects Models, , https://cran.r-project.org/package=nlme
  • Bates, D., Mächler, M., Bolker, B., Walker, S., Fitting linear mixed-effects models using lme4 J Stat Softw
  • (2015), 67. , https://doi.org/10.18637/jss.v067.i01; (2016) R: A Language and Environment for Statistical Computing, , http://www.r-project.org/, Vienna, Austria
  • Zubrzycki, J., Filippi, C., Fusari, C., Puebla, A., Fernandez, P., Hopp, H., Desarrollo e implementación de un ensayo de genotipificación masiva de SNPs en girasol (2012) Procedimiento Del XV Congreso Latinoamer-Icano De Genética, ALAG, , Rosario, Argentina
  • Filippi, C.V., Aguirre, N., Rivas, J.G., Zubrzycki, J., Puebla, A., Cordes, D., Population structure and genetic diversity characterization of a sunflower association mapping population using SSR and SNP markers (2015) BMC Plant Biol, 15, p. 52. , https://doi.org/10.1186/s12870-014-0360-x, PMID: 25848813
  • Fernandez, P., Soria, M., Blesa, D., DiRienzo, J., Moschen, S., Rivarola, M., Development, characterization and experimental validation of a cultivated sunflower (Helianthus annuus L.) gene expression oligo-nucleotide microarray (2012) PLoS One, 7. , https://doi.org/10.1371/journal.pone.0045899, PMID: 23110046
  • Fusari, C.M., Lia, V.V., Hopp, H.E., Heinz, R.A., Paniego, N.B., Identification of single nucleotide polymorphisms and analysis of linkage disequilibrium in sunflower elite inbred lines using the candidate gene approach (2008) BMC Plant Biol, 8, p. 7. , https://doi.org/10.1186/1471-2229-8-7, PMID: 18215288
  • Kolkman, J.M., Berry, S.T., Leon, A.J., Slabaugh, M.B., Tang, S., Gao, W., Single nucleotide polymorphisms and linkage disequilibrium in sunflower (2007) Genetics, 177, pp. 457-468. , https://doi.org/10.1534/genetics.107.074054, PMID: 17660563
  • Fan, J.-B., Gunderson, K.L., Bibikova, M., Yeakley, J.M., Chen, J., Garcia, W., Illumina universal bead arrays (2006) Methods Enzymol, 410, pp. 57-73. , https://doi.org/10.1016/S0076-6879(06)10003-8, PMID: 16938546
  • Lepoittevin, C., Frigerio, J.-M., Garnier-Géré, P., Salin, F., Cervera, M.-T., Vornam, B., In vitro vs in silico detected SNPs for the development of a genotyping array: What can we learn from a non-model species? (2010) PLoS One, 5. , https://doi.org/10.1371/journal.pone.0011034, PMID: 20543950
  • Roorkiwal, M., Sawargaonkar, S.L., Chitikineni, A., Thudi, M., Saxena, R.K., Upadhyaya, H.D., Single nucleotide polymorphism genotyping for breeding and genetics applications in chickpea and pigeon-pea using the BeadXpress platform (2013) Plant Genome, 6, pp. 1-10. , https://doi.org/10.3835/plantgenome2013.05.0017
  • Zubrzycki, J., Fusari, C., Maringolo, C., DiRienzo, J., Cervigni, G., Nishinakamasu, V., Biparental QTL and association mapping for sclerotinia head rot resistance in cultivated sunflower (2012) Proceeding of The 18th International Sunflower Conference, , http://www.asagir.org.ar/asagir2008/buscar_congreso.asp
  • Fusari, C.M., Lia, V.V., Nishinakamasu, V., Zubrzycki, J.E., Puebla, A.F., Maligne, A.E., Single nucleotide polymorphism genotyping by heteroduplex analysis in sunflower (Helianthus annuus L.) (2010) Mol Breed, 28, pp. 73-89. , https://doi.org/10.1007/s11032-010-9462-9
  • Schuster, I., Cruz, C., (2004) Estatística Genômica Aplicada A Populações Derivadas De Cruzamentos Controla-Dos, , 1st ed. UFV, editor. Viçosa, MG, Brasil
  • Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: A practical and powerful approach to multiple testing (1995) J R Stat Soc Ser B Methodol, 57, pp. 289-300. , JSTOR
  • Van Ooijen, J.W., Voorrips, V.E., JoinMap 3.0, Software for the calculation of genetic linkage maps (2001) Plant Research International, , Wageningen, The Netherlands
  • Kiani, S., Talia, P., Maury, P., Grieu, P., Heinz, R., Perrault, A., Genetic analysis of plant water status and osmotic adjustment in recombinant inbred lines of sunflower under two water treatments (2007) Plant Sci, 172, pp. 773-787. , https://doi.org/10.1016/j.plantsci.2006.12.007
  • Kosambi, D.D., The estimation of map distances from recombination values (1943) Ann Eugen, 12, pp. 172-175. , https://doi.org/10.1111/j.1469-1809.1943.tb02321.x, Wiley Online Library
  • Haldane, J.B., Waddington, C.H., Inbreeding and Linkage (1931) Genetics, 16, pp. 357-374. , PMID: 17246626
  • Voorrips, R.E., MapChart: Software for the graphical presentation of linkage maps and QTLs (2002) J Hered, 93, pp. 77-78. , https://doi.org/10.1093/jhered/93.1.77, PMID: 12011185
  • Wang, S., Basten, C., Zeng, Z., (2012) Windows QTL Cartographer, , http://statgen.ncsu.edu/qtlcart/WQTLCart.htm, Version 2.5. Raleigh, NC
  • Jansen, R.C., Stam, P., High resolution of quantitative traits into multiple loci via interval mapping (1994) Genetics, 136, pp. 1447-1455. , PMID: 8013917
  • Doerge, R.W., Churchill, G.A., Permutation tests for multiple loci affecting a quantitative character (1996) Genetics, 142, pp. 285-294. , PMID: 8770605
  • Yang, J., Hu, C., Hu, H., Yu, R., Xia, Z., Ye, X., QTLNetwork: Mapping and visualizing genetic architecture of complex traits in experimental populations (2008) Bioinformatics, 24, pp. 721-723. , https://doi.org/10.1093/bioinformatics/btm494, PMID: 18202029
  • Yang, J., Zhu, J., Williams, R.W., Mapping the genetic architecture of complex traits in experimental populations (2007) Bioinformatics, 23, pp. 1527-1536. , https://doi.org/10.1093/bioinformatics/btm143, PMID: 17459962
  • McCouch, S.R., Cho, Y.G., Yano, M., Paul, E., Blinstrub, M., Morishima, H., Report on QTL nomenclature (1997) Rice Genet Newsletters, 14, pp. 11-13
  • Vear, F., De Labrouhe, T.D., Recurrent selection for resistance to Sclerotinia sclerotiorum in sunflowers using artificial infections (1984) Agronomie, 4, pp. 789-794. , https://doi.org/10.1051/agro:19840811
  • Pedraza, M.V., Pereyra, V.R., Infection courts and length of susceptible period related to sunflower head rot (Sclerotinia sclerotiorum) resistance (2004) Helia, 27, pp. 171-182. , https://doi.org/10.2298/HEL0440171P
  • Castaño, F., Vear, F., De Labrouhe, T.D., The genetics of resistance in sunflower capitula to Sclerotinia sclerotiorum measured by mycelium infections combined with ascospore tests (2001) Euphytica, 122, pp. 373-380. , https://doi.org/10.1023/A:1012970101508
  • Vear, F., Serre, F., Roche, S., Walser, P., De Labrouhe, T.D., Improvement of Sclerotinia sclerotiorum head rot resistance in sunflower by recurrent selection of a restorer population (2007) Helia, 30, pp. 1-12
  • Giussani, A., Castaño, F., Rodríguez, R., Quiróz, F., White rot resistance, seed weight and seed oil content in sunflower test crosses (2008) Proceeding of 17 th International Sunflower Conference, pp. 539-544. , Cordoba, Spain
  • Castaño, F., Giussani, M.A., Effectiveness of components of partial resistance in assessing white rot of sunflower head (2009) Helia, 32, pp. 59-68. , https://doi.org/10.2298/HEL0950059C
  • Bioley, J.P., Jay, M., Fiasson, J.L., Biochemical mechanisms of the secondary mechanism in the reaction of cultivated plants to fungi pathogens (1987) Sclerotinia Sclerotiorum in Sunflower: Study of A Biochemical Way for Looking for Resistance, pp. 7-19. , fs. Tech. CETIOM
  • Abawi, G.S., Epidemiology of diseases caused by sclerotinia species (1979) Phytopathology, 69, p. 899. , https://doi.org/10.1094/Phyto-69-899
  • Vear, F., Willefer, D., Walser, P., Serre, F., De Labrouhe, T.D., Reaction of sunflower lines to a series of Sclerotinia sclerotiorum isolates (2004) Proceeding of The 16th International Sunflower Conference, pp. 135-140. , Fargo, North Dakota, USA
  • Kiani, S.P., Maury, P., Sarrafi, A., Grieu, P., QTL analysis of chlorophyll fluorescence parameters in sunflower (Helianthus annuus L.) under well-watered and water-stressed conditions (2008) Plant Sci, 175, pp. 565-573. , https://doi.org/10.1016/j.plantsci.2008.06.002
  • Darvishzadeh, R., Kiani, S.P., Dechamp-Guillaume, G., Gentzbittel, L., Sarrafi, A., Quantitative trait loci associated with isolate specific and isolate nonspecific partial resistance to Phoma macdonaldii in sunflower (2007) Plant Pathol, 56, pp. 855-861. , https://doi.org/10.1111/j.1365-3059.2007.01620.x
  • Al-Chaarani, G.R., Gentzbittel, L., Huang, X.Q., Sarrafi, A., Genotypic variation and identification of QTLs for agronomic traits, using AFLP and SSR markers in RILs of sunflower (Helianthus annuus L.) (2004) Theor Appl Genet, 109, pp. 1353-1360. , https://doi.org/10.1007/s00122-004-1770-1, PMID: 15365625
  • Berrios, F., Alibert, K.G., Berrios, F., Gentzbittel, L., Kayyal, H., Alibert, G., AFLP mapping of QTLs for in vitro organogenesis traits using recombinant inbred lines in sunflower (Helianthus annuus L.) (2000) Theor Appl Genet, 33, pp. 1299-1306. , https://doi.org/10.1007/s001220051610
  • Rönicke, S., Hahn, V., Vogler, A., Friedt, W., Quantitative Trait Loci Analysis of Resistance to Sclerotinia sclerotiorum in Sunflower (2005) Phytopathology, 95, pp. 834-839. , https://doi.org/10.1094/PHYTO-95-0834, PMID: 18943017
  • Sebastian, R.L., Howell, E.C., King, G.J., Marshall, D.F., Kearsey, M.J., An integrated AFLP and RFLP Brassica oleracea linkage map from two morphologically distinct doubled-haploid mapping populations (2000) Theor Appl Genet, 100, pp. 75-81. , https://doi.org/10.1007/s001220050011
  • Qi, L.L., Long, Y.M., Ma, G.J., Markell, S.G., Map saturation and SNP marker development for the rust resistance genes (R 4, R 5, R 13a, and R 13b) in sunflower (Helianthus annuus L.) (2015) Mol Breed, 35, p. 196. , https://doi.org/10.1007/s11032-015-0380-8
  • Bert, P.F., Jouan, I., De Labrouhe, T.D., Serre, F., Nicolas, P., Vear, F., Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.) 1. QTL involved in resistance to Sclerotinia sclerotiorum and Diaporthe helianthi (2002) Theor Appl Genet Theor und Angew Genet, 105, pp. 985-993. , https://doi.org/10.1007/s00122-002-1004-3, PMID: 12582925
  • Micic, Z., Hahn, V., Bauer, E., Melchinger, A.E., Knapp, S.J., Tang, S., Identification and validation of QTL for Sclerotinia midstalk rot resistance in sunflower by selective genotyping (2005) Theor Appl Genet, 111, pp. 233-242. , https://doi.org/10.1007/s00122-005-2004-x, PMID: 15947909
  • Davar, R., Darvishzadeh, R., Majd, A., Ghosta, Y., Sarrafi, A., QTL mapping of partial resistance to basal stem rot in sunflower using recombinant inbred lines (2010) Phytopathol Medit, 49, pp. 330-341
  • Upadyayula, N., Da Silva, H.S., Bohn, M.O., Rocheford, T.R., Genetic and QTL analysis of maize tassel and ear inflorescence architecture (2006) Theor Appl Genet, 112, pp. 592-606. , https://doi.org/10.1007/s00122-005-0133-x, PMID: 16395569
  • Micic, Z., Hahn, V., Bauer, E., Schön, C.C., Knapp, S.J., Tang, S., QTL mapping of Sclerotinia midstalk-rot resistance in sunflower (2004) Theor Appl Genet, 109, pp. 1474-1484. , https://doi.org/10.1007/s00122-004-1764-z, PMID: 15480534
  • Jouan, I., Bert, P.F., Cambon, F., Perrault, A., De Labrouhe, T.D., Nicolas, P., The relations between the recessive gene for apical branching (b1) and some disease resistance and agronomic characters (2000) Proceedings of The 15th International Sunflower Conference, pp. K54-K59. , Toulouse
  • Filippi, C., (2015) Diversidad Genómica Y Mapeo Por Asociación para La Resistencia A La Podredumbre Húmeda Del Capítulo Causada Por Sclerotinia Sclerotiorum En Girasol, , Tesis de Doctorado. Universidad de Buenos Aires
  • Jannink, J.-L., Identifying Quantitative Trait Locus by Genetic Background Interactions in Association Studies (2007) Genetics, 176, pp. 553-561. , https://doi.org/10.1534/genetics.106.062992, PMID: 17179077
  • Beavis, W.D., Smith, O.S., Grant, D., Fincher, R., Identification of Quantitative Trait Loci Using a Small Sample of Topcrossed and F4 Progeny from Maize (1994) Crop Sci, 34, p. 882. , https://doi.org/10.2135/cropsci1994.0011183X003400040010x
  • Desta, Z.A., Ortiz, R., Genomic selection: Genome-wide prediction in plant improvement (2014) Trends Plant Sci, 19, pp. 592-601. , https://doi.org/10.1016/j.tplants.2014.05.006, PMID: 24970707

Citas:

---------- APA ----------
Zubrzycki, J.E., Maringolo, C.A., Filippi, C.V., Quiróz, F.J., Nishinakamasu, V., Puebla, A.F., Julio, A.D.R.,..., Paniego, N.B. (2017) . Main and epistatic QTL analyses for Sclerotinia Head Rot resistance in sunflower. PLoS ONE, 12(12).
http://dx.doi.org/10.1371/journal.pone.0189859
---------- CHICAGO ----------
Zubrzycki, J.E., Maringolo, C.A., Filippi, C.V., Quiróz, F.J., Nishinakamasu, V., Puebla, A.F., et al. "Main and epistatic QTL analyses for Sclerotinia Head Rot resistance in sunflower" . PLoS ONE 12, no. 12 (2017).
http://dx.doi.org/10.1371/journal.pone.0189859
---------- MLA ----------
Zubrzycki, J.E., Maringolo, C.A., Filippi, C.V., Quiróz, F.J., Nishinakamasu, V., Puebla, A.F., et al. "Main and epistatic QTL analyses for Sclerotinia Head Rot resistance in sunflower" . PLoS ONE, vol. 12, no. 12, 2017.
http://dx.doi.org/10.1371/journal.pone.0189859
---------- VANCOUVER ----------
Zubrzycki, J.E., Maringolo, C.A., Filippi, C.V., Quiróz, F.J., Nishinakamasu, V., Puebla, A.F., et al. Main and epistatic QTL analyses for Sclerotinia Head Rot resistance in sunflower. PLoS ONE. 2017;12(12).
http://dx.doi.org/10.1371/journal.pone.0189859