Potential of a tomato MAGIC population to decipher the genetic control of quantitative traits and detect causal variants in the resequencing era

Plant Biotechnology Journal

Volumn 13, Issue 4, 2015, Pages 565-577

  Pascual, Laura ^a,e   Desplat, Nelly ^a,f   Huang, Bevan E ^b   Desgroux, Aurore ^a,g   Bruguier, Laure ^c   Bouchet, Jean Paul ^a   Le, Quang H ^d   Chauchard, Betty ^c   Verschave, Philippe ^c   Causse, Mathilde ^a  

^a Researches Center of Avignon   (France)

^b CSIRO   (Australia)

^c Clause and Cie   (France)

^d Route d'Ennezat   (France)

^e UNIVERSITY OF BARCELONA   (Spain)

^f GM Trait Discovery Biogemma Centre de Recherche de Chappes   (France)

^g Universite Rennes 1   (France)

Author keywords

Multiparental population; QTL; Resequencing; SNP; Solanum lycopersicum

Indexed keywords

LYCOPERSICON ESCULENTUM;

GENETICS; PLANT GENE; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; TOMATO;

GENES, PLANT; LYCOPERSICON ESCULENTUM; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

EID: 84928183520     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12282     Document Type: Article

References (52)

1. Bandillo, N., Raghavan, C., Muyco, P.A., Sevilla, M.A.L., Lobina, I.T., Dilla-Ermita, C.J., Tung, C.W., McCouch, S., Thomson, M., Mauleon, R., Singh, R.K., Gregorio, G., Redoña, E. and Leung, H. (2013) Multi-parent advanced generation inter-cross (MAGIC) populations in rice: progress and potential for genetics research and breeding. Rice, 6, 11.
2. Bardol, N., Ventelon, M., Mangin, B., Jasson, S., Loywick, V., Couton, F., Derue, C., Blanchard, P., Charcosset, A. and Moreau, L. (2013) Combined linkage and linkage disequilibrium QTL mapping in multiple families of maize (Zea mays L.) line crosses highlights complementaries between models based on parental haplotype and single locus polymorphism. Theor. Appl. Genet. 126, 2717-2136.
3. Benjamini, Y. and Hochberg, Y. (2000) On the adaptive control of the false discovery rate in multiple testing with independent statistics. J. Educ. Behav. Stat. 25, 60-83.
4. Blanca, J., Canizares, J., Cordero, L., Pascual, L., Diez, M.J. and Nuez, F. (2012) Variation revealed by SNP genotyping and morphology provides insight into the origin of the tomato. PLoS ONE, 7, e48198.
5. Bradbury, P.J., Zhang, D., Kroon, D.E., Casstevens, T.M., Ramdoss, Y. and Buckler, E.S. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633-2635.
6. Causse, M., Duffe, P., Gomez, M.C., Buret, M., Damidaux, R., Zamir, D., Gur, A., Chevalier, C., Lemaire-Chamley, M. and Rothan, C. (2004) A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J. Exp. Bot. 55, 1671-1685.
7. Causse, M., Desplat, N., Pascual, L., Le Paslier, M.C., Sauvage, C., Bauchet, G., Bérard, A., RémiBounon, R., Tchoumakov, M., Brunel, D. and Bouchet, J.P. (2013) Whole genome profiles of nucleotide variations reveal breeding and introgression events in 8 lines of tomato. BMC Genomics, 14, 791.
8. Cavanagh, C., Morell, M., Mackay, I. and Powell, W. (2008) From mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. Curr. Opin. Plant Biol. 11, 215-221.
9. Chakrabarti, M., Zhang, N., Sauvage, C., Muños, S., Blanca, J., Cañizares, J., Diez, M.J., Schneider, R., Mazourek, M., McClead, J., Causse, M. and van der Knaap, E. (2013) A cytochrome P450 regulates a domestication trait in cultivated tomato. Proc. Natl Acad. Sci. USA, 110, 17125-17130.
10. Clarke, J.H., Mithen, R., Brown, J.K. and Dean, C. (1995) QTL analysis of flowering time in Arabidopsis thaliana. Mol. Gen. Genet. 248, 278-286.
11. Darvasi, A. and Soller, M. (1995) Advanced intercross lines, an experimental population for fine genetic mapping. Genetics, 141, 199-1207.
12. Evanno, G., Regnaut, S. and Goudet, J. (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 14, 2611-2620.
13. Fluidigm (2011) Fluidigm SNP Genotyping Analysis. San Francisco: Fluidigm Corp.
14. Frary, A., Nesbitt, T.C., Grandillo, S., Knaap, E., Cong, B., Liu, J., Meller, J., Elber, R., Alpert, K.B. and Tanksley, S.D. (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science, 289, 547685-547688.
15. Giovannoni, J.J. (2004) Genetic regulation of fruit development and ripening. Plant Cell, 16, S170-S180.
16. Grandillo, S. and Tanksley, S.D. (1996) QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theor. Appl. Genet. 92, 935-951.
17. Grandillo, S., Ku, H.M. and Tanksley, S.D. (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor. Appl. Genet. 99, 978-987.
18. Hall, D., Tegstrom, C. and Ingvarsson, P.K. (2010) Using association mapping to dissect the genetic basis of complex traits in plants. Brief. Funct. Genomics, 9, 157-165.
19. Hardy, O.J. and Vekemans, X. (2002) SPAGeDi: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol. Ecol. Notes, 2, 618-620.
20. Huang, B.E. and George, A.W. (2011) R/mpMap: a computational platform for the genetic analysis of multiparent recombinant inbred lines. Bioinformatics, 27, 727-729.
21. Huang, X., Zhao, Y., Wei, X., Li, C., Wang, A., Zhao, Q., Li, W., Guo, Y., Deng, L., Zhu, C., Fan, D., Lu, Y., Weng, Q., Liu, K., Zhou, T., Jing, Y., Si, L., Dong, G., Huang, T., Lu, T., Feng, Q., Qian, Q., Li, J. and Han, B. (2012a) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat. Genet. 44, 32-39.
22. Huang, B.E., George, A.W., Forrest, K.L., Kilian, A., Hayden, M.J., Morell, M.K. and Cavanagh, C.R. (2012b) A multiparent advanced generation inter-cross population for genetic analysis in wheat. Plant Biotechnol. J. 10, 826-839.
23. Keurentjes, J.J., Bentsink, L., Alonso-Blanco, C., Hanhart, C.J., Blankestijn-De Vries, H., Effgen, S., Vreugdenhil, D. and Koornneef, M. (2007) Development of a near-isogenic line population of Arabidopsis thaliana and comparison of mapping power with a recombinant inbred line population. Genetics, 175, 891-905.
24. van der Knaap, E. and Tanksley, S.D. (2003) The making of a bell pepper-shaped tomato fruit: identification of loci controlling fruit morphology in Yellow Stuffer tomato. Theor. Appl. Genet. 107, 139-147.
25. Korte, A. and Farlow, A. (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods, 9, 29.
26. Kover, P.X. and Mott, R. (2012) Mapping the genetic basis of ecologically and evolutionarily relevant traits in Arabidopsis thaliana. Curr. Opin. Plant Biol. 15, 212-217.
27. Kover, P.X., Valdar, W. and Trakalo, J. (2009) A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genet. 5, 7.
28. Miller, J.C. and Tanksley, S.D. (1990) RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theor. Appl. Genet. 80, 437-448.
29. Mitchell-Olds, T. (2010) Complex-traits analysis in plants. Genome Biol. 10, 113.
30. Morell, P.L., Buckler, E.S. and Ross-Ibarra, J. (2012) Crop genomics: advances and applications. Nat. Rev. Genet. 13, 85-96.
31. Mott, R., Talbot, C.J., Turri, M.G., Collins, A.C. and Flint, J. (2000) A method for fine mapping quantitative trait loci in outbred stocks. Proc. Natl Acad. Sci. USA, 97, 12649-12654.
32. Pascual, L., Xu, J., Biais, B., Maucourt, M., Ballias, P., Bernillon, S., Deborde, C., Jacob, D., Desgroux, A., Faurobert, M., Bouchet, J.P., Gibon, Y., Moing, A. and Causse, M. (2013) Deciphering genetic diversity and inheritance of tomato fruit weight and composition through a systems biology approach. J. Exp. Bot. 64, 5737-5752.
33. Pollard, K.S., Gilbert, N.H., Ge, Y., Taylor, S. and Dudoit, S. (2012) multtest: Resampling-based multiple hypothesis testing. R package version 2.14.0.
34. Price, A.H. (2006) Believe it or not, QTLs are accurate!. Trends Plant Sci. 11, 213-216.
35. Pritchard, J.K., Stephens, M. and Donelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
36. Rakshit, S., Rakshit, A. and Patil, J.V. (2012) Multiparent intercross populations in analysis of quantitative traits. J. Genet. 91, 111-117.
37. Ranc, N., Munos, S., Santoni, S. and Causse, M. (2008) A clarified position for Solanum lycopersicum var. cerasiforme in the evolutionary history of tomatoes (Solanaceae). BMC Plant Biol. 8, 130.
38. Ranc, N., Muños, S., Xu, J., Le Paslier, M.C., Chauveau, A., Bounon, R., Rolland, S., Bouchet, J.P., Brunel, D. and Causse, M. (2012) Genome-wide association mapping in tomato (Solanum lycopersicum) is possible using genome admixture of Solanum lycopersicum var. cerasiforme. G3, 2, 853-864.
39. Rockman, M.V. and Kruglyak, L. (2008) Breeding designs for recombinant inbred advanced intercross lines. Genetics, 179, 1069-1078.
40. Rosyara, U.R., C.A.M. Bink, M., van de Weg, E., Zhang, G., Wang, D., Sebolt, A., Dirlewanger, E., Quero-Garcia, J., Schuster, M. and Iezzoni, A.M. (2013) Fruit size QTL identification and the prediction of parental QTL genotypes and breeding values in multiple pedigreed populations of sweet cherry. Mol. Breed. 32, 875-887.
41. Saliba-Colombani, V., Causse, M., Langlois, D., Philouze, J. and Buret, M. (2001) Genetic analysis of organoleptic quality in fresh market tomato. 1. Mapping QTLs for physical and chemical traits. Theor. Appl. Genet. 102, 259-272.
42. Sauvage, C., Segura, V., Bauchet, G., Stevens, R., Thi Do, P., Nikoloski, Z., Fernie, A.R. and Causse, M. (2014) Genome wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol. 165, 1120-1132.
43. Sim, S.C., Durstewitz, G., Plieske, J., Wieseke, R., Ganal, M.W., Van Deynze, A., Hamilton, J.P., Buell, C.R., Causse, M., Wijeratne, S. and Francis, D.M. (2012a) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS ONE, 7, e45520.
44. Sim, S.C., Van Deynze, A., Stoffel, K., Douches, D.S., Zarka, D., Ganal, M.W., Chetelat, R.T., Hutton, S.F., Scott, J.W., Gardner, R.G., Panthee, D.R., Mutschler, M., Myers, J.R. and Francis, D.M. (2012b) High-density SNP genotyping of tomato (Solanum lycopersicum L.) reveals patterns of genetic variation due to breeding. PLoS ONE, 7, e40563.
45. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635-641.
46. Valdar, W., Flint, J. and Mott, R. (2006) Simulating the collaborative cross: power of QTL detection and mapping resolution in large sets of recombinant inbred strains of mice. Genetics, 172, 1783-1797.
47. Visscher, P.M., Brown, M.A., McCarthy, M.I. and Yang, J. (2012) Five years of GWAS Discovery. Am. J. Hum. Genet. 90, 7-24.
48. Xu, J., Ranc, N., Muños, S., Rolland, S., Bouchet, J.P., Desplat, N., Le Paslier, M.C., Liang, Y., Brunel, D. and Causse, M. (2013) Phenotypic diversity and association mapping for fruit quality traits in cultivated tomato and related species. Theor. Appl. Genet. 126, 567-581.
49. Yalchin, B., Flint, J. and Mott, R. (2005) Using progenitor strain information to identify quantitative trait nucleotides in out bred mice. Genetics, 171, 673-681.
50. Yu, J., Pressoir, G., Briggs, W.H., Vroh Bi, I., Yamasaki, M., Doebley, J.F., McMullen, M.D., Gaut, B.S., Nielsen, D.M., Holland, J.B., Kresovich, S. and Buckler, E.S. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38, 203-208.
51. Yu, J., Holland, J.B., McMullen, M.D. and Buckler, E.S. (2008) Genetic design and statistical power of nested association mapping in maize. Genetics, 178, 539-551.
52. Zamir, D. (2001) Improving plant breeding with exotic genetic libraries. Nat. Rev. Genet. 2, 983-989.