Structural characterization and mapping of functional EST-SSR markers in Theobroma cacao

Tree Genetics and Genomes

Volumn 7, Issue 4, 2011, Pages 799-817

  Fouet, Olivier ^a   Allegre, Mathilde ^a   Argout, Xavier ^a   Jeanneau, Mélanie ^a   Lemainque, Arnaud ^b   Pavek, Sylvana ^b   Boland, Anne ^b   Risterucci, Ange Marie ^a   Loor, Gaston ^c   Tahi, Mathias ^d   Sabau, Xavier ^a   Courtois, Brigitte ^a   Lanaud, Claire ^a  

^a CIRAD   (France)

^b CENTRE NATIONAL DE GÉNOTYPAGE   (France)

^c EET Pichilingue INIAP ^*  (Ecuador)

^d CNRA   (France)

Author keywords

Candidate genes; EST SSR; Genetic map; Theobroma cacao

Indexed keywords

THEOBROMA CACAO;

EID: 79960598877     PISSN: 16142942     EISSN: 16142950     Source Type: Journal    
DOI: 10.1007/s11295-011-0375-5     Document Type: Article

References (81)

1. Aggarwal RK, Hendre PS, Varshney RK, Bhat PR, Krishnakumar V, Singh L (2007) Identification, characterization and utilization of EST-derived genic microsatellite markers for genome analyses of coffee and related species. Theor Appl Genet 114(2): 359-372.
2. Aime MC, Phillips-Mora W (2005) The causal agents of witches' broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia 97(5): 1012-1022.
3. Argout X, Fouet O, Wincker P, Gramacho K, Legavre T, Sabau X, Risterucci A-M, Da Silva C, Cascardo J, Allegre M, Kuhn D, Verica J, Courtois B, Loor R, Regis B, Sounigo O, Ducamp M, Guiltinan M, Ruiz M, Alemanno L, Machado R, Phillips W, Schnell R, Gilmour M, Rosenquist E, Butler D, Maximova S, Lanaud C (2008) Towards the understanding of the cocoa transcriptome: production and analysis of an exhaustive dataset of ESTs of Theobroma cacao generated from various tissues and under various conditions. BMC Genomics 9(1): 512.
4. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 25(1): 25-29.
5. Barreneche T, Bodenes C, Lexer C, Trontin JF, Fluch S, Streiff R, Plomion C, Roussel G, Steinkellner H, Burg K, Favre JM, Glossl J, Kremer A (1998) A genetic linkage map of Quercus robur L. (pedunculate oak) based on RAPD, scar, microsatellite, minisatellite, isozyme and 5S rDNA markers. Theor Appl Genet 97(7): 1090-1103.
6. Beckman JS, Soller M (1990) Toward a unified approach to the genetic mapping of eukaryotes based on sequence-tagged microsatellite sites. Biotechnology 8: 930-932.
7. Borrone JW, Brown S, Khun DV, Motamayor JC, Schnell RD (2007) Microsatellite markers developed from Theobroma cacao l. Expressed sequence tags. Mol Ecol Notes 7: 236-239.
8. Brown J, Sautter R, Olano C, Borrone J, Kuhn D, Motamayor J, Schnell R (2008) A composite linkage map from three crosses between commercial clones of cacao, Theobroma cacao L. Trop Plant Biol 1(2): 120-130.
9. Brown JS, Phillips-Mora W, Power EJ, Krol C, Cervantes-Martinez C, Motamayor JC, Schnell RJ (2007) Mapping QTLs for resistance to frosty pod and black pod diseases and horticultural traits in Theobroma cacao L. Crop Sci 47(5): 1851-1858.
10. Brown JS, Schnell RJ, Motamayor JC, Lopes U, Kuhn DN, Borrone JW (2005) Resistance gene mapping for witches' broom disease in Theobroma cacao L. In an f-2 population using SSR markers and candidate genes. J Am Soc Hortic Sci 130(3): 366-373.
11. Cheesman EE (1944) Notes on the nomenclature, classification and possible relationships of cocoa populations. Trop Agric 21: 144-159.
12. Chen JF, Hu JG, Vick BA, Jan CC (2006) Molecular mapping of a nuclear male-sterility gene in sunflower (Helianthus annuus L.) using trap and SSR markers. Theor Appl Genet 113(1): 122-127.
13. Cho YG, Ishii T, Temnykh S, Chen X, Lipovich L, McCouch SR, Park WD, Ayres N, Cartinhour S (2000) Diversity of microsatellites derived from genomic libraries and genbank sequences in rice (Oryza sativa L.). Theor Appl Genet 100(5): 713-722.
14. Clement D, Risterucci AM, Motamayor JC, N'Goran J, Lanaud C (2003) Mapping QTL for yield components, vigor, and resistance to Phytophthora palmivora in Theobroma cacao L. Genome 46(2): 204-212.
15. Cocoa market update (2009). Available at: http://www. Worldcocoafoundation. Org/learn-about-cocoa/cocoa-market. Html.
16. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2go: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18): 3674-3676.
17. Cordeiro G, Casu R, McIntyre C, Manners J, Henry R (2001) Microsatellite markers from sugarcane (saccharum spp.) ESTs cross transferable to erianthus and sorghum. Plant Science 160(6): 1115-1123.
18. Crouzillat D, Lerceteau E, Petiard V, Morera J, Rodriguez H, Walker D, Phillips W, Ronning C, Schnell R, Osei J, Fritz P (1996) Theobroma cacao L: a genetic linkage map and quantitative trait loci analysis. Theor Appl Genet 93(1-2): 205-214.
19. Crouzillat D, Menard B, Mora A, Phillips W, Petiard V (2000) Quantitative trait analysis in Theobroma cacao using molecular markers-yield QTL detection and stability over 15 years. Euphytica 114(1): 13-23.
20. Decroocq V, Favé MG, Hagen L, Bordenave L, Decroocq S (2003) Development and transferability of apricot and grape EST microsatellite markers across taxa. Theor Appl Genet 106(5): 912-922.
21. Dettori MT, Quarta R, Verde I (2001) A peach linkage map integrating RFLPs, SSRs, RAPDs, and morphological markers. Genome 44(5): 783-790.
22. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5(6): 435-445.
23. Eujayl I, Sorrells M, Baum M, Wolters P, Powell W (2001) Assessment of genotypic variation among cultivated durum wheat based on EST-SSRs and genomic SSRs. Euphytica 119(1-2): 39-43.
24. Eujayl I, Sorrells ME, Baum M, Wolters P, Powell W (2002) Isolation of EST-derived microsatellite markers for genotyping the a and b genomes of wheat. Theor Appl Genet 104(2-3): 399-407.
25. Figueira A, Janick J, Goldsbrough P (1992) Genome size and DNA polymorphism in Theobroma cacao. J Am Soc Hortic Sci 117(4): 673-677.
26. Flament MH, Kebe I, Clément D, Pieretti I, Risterucci AM, N'Goran JA, Cilas C, Despréaux D, Lanaud C (2001) Genetic mapping of resistance factors to Phytophthora palmivora in cocoa. Genome 44(1): 79-85.
27. Fritz-Laylin LK, Krishnamurthy N, Tör M, Sjölander KV, Jones JDG (2005) Phylogenomic analysis of the receptor-like proteins of rice and arabidopsis. Plant Physiol 138(2): 611-623.
28. Gebhart C, Ritter E, Debener T, Schachtschabel U, Walkemeier B, Urig H, Salamini F (1989) RFLP analysis and linkage mapping of Solanum tuberosum. Theor Appl Genet 78: 65-75.
29. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137(4): 1121-1137.
30. Guo W, Cai C, Wang C, Han Z, Song X, Wang K, Niu X, Wang C, Lu K, Shi B, Zhang T (2007) A microsatellite-based, gene-rich linkage map reveals genome structure, function and evolution in gossypium. Genetics 176(1): 527-541.
31. Gupta PK, Rustgi S (2004) Molecular markers from the transcribed/expressed region of the genome in higher plants. Funct Integr Genomics 4(3): 139-162.
32. Gupta S, Prasad M (2009) Development and characterization of genic SSR markers in Medicago truncatula and their transferability in leguminous and non-leguminous species. Genome 52(9): 761-771.
33. Hackauf B, Wehling P (2002) Identification of microsatellite polymorphisms in an expressed portion of the rye genome. Plant Breed 121(1): 17-25.
34. Hall MC, Willis JH (2005) Transmission ratio distortion in intraspecific hybrids of Mimulus guttatus: implications for genomic divergence. Genetics 170(1): 375-386.
35. Han ZG, Guo WZ, Song XL, Zhang TZ (2004) Genetic mapping of EST-derived microsatellites from the diploid gossypium arboreum in allotetraploid cotton. Mol Genet Genomics 272(3): 308-327.
36. Jones PG, Allaway D, Gilmour DM, Harris C, Rankin D, Retzel ER, Jones CA (2002) Gene discovery and microarray analysis of cacao (Theobroma cacao L.) varieties. Planta 216(2): 255-264.
37. Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12: 172-175.
38. Lanaud C, Hamon P, Duperray C (1992) Estimation of nuclear-DNA content of Theobroma cacao L. by flow-cytometry. Cafe Cacao The 36(1): 3-8.
39. Lanaud C, Risterucci AM, Ngoran AKJ, Clement D, Flament MH, Laurent V, Falque M (1995) A genetic linkage map of Theobroma cacao L. Theor Appl Genet 91(6-7): 987-993.
40. Lanaud C, Risterucci AM, Pieretti I, Falque M, Bouet A, Lagoda PJ (1999) Isolation and characterization of microsatellites in Theobroma cacao L. Mol Ecol 8(12): 2141-2143.
41. Lanaud C, Fouet O, Clement D, Boccara M, Risterucci AM, Surujdeo-Maharaj S, Legavre T, Argout X (2009) A meta-QTL analysis of disease resistance traits of Theobroma cacao L. Mol Breed 24(4): 361-374.
42. Laurent V, Risterucci AM, Lanaud C (1993a) Chloroplast and mitochondrial DNA diversity in Theobroma cacao. Theor Appl Genet 87(1-2): 81-88.
43. Laurent V, Risterucci AM, Lanaud C (1993b) Variability for nuclear ribosomal genes within Theobroma cacao. Heredity 71: 96-103.
44. Leal GA, Albuquerque PSB, Figueira A (2007) Genes differentially expressed in Theobroma cacao associated with resistance to witches' broom disease caused by Crinipellis perniciosa. Mol Plant Pathol 8(3): 279-292.
45. Lee JM, Nahm SH, Kim YM, Kim BD (2004) Characterization and molecular genetic mapping of microsatellite loci in pepper. Theor Appl Genet 108(4): 619-627.
46. Lerceteau E, Robert T, Petiard V, Crouzillat D (1997) Evaluation of the extent of genetic variability among Theobroma cacao accessions using RAPD and RFLP markers. Theor Appl Genet 95(1-2): 10-19.
47. Lima LS, Gramacho KP, Pires JL, Clement D, Lopes UV, Carels N, Gesteira A, Gaiotto FA, Cascardo JC, Micheli F (2010) Development, characterization, validation, and mapping of SSRs derived from Theobroma cacao L.-Moniliophthora perniciosa interaction ESTs. Tree Genet Genomes 4: 1-14.
48. Litt M, Luty JA (1989) A hypervariable microsatellite revealed by in vitro amplification of a dinucleotide repeat within the cardiac muscle actin gene. Am J Hum Genet 44(3): 397-401.
49. Lu H, Romero-Severson J, Bernardo R (2002) Chromosomal regions associated with segregation distortion in maize. Theor Appl Genet 105(4): 622-628.
50. Luro FL, Costantino G, Terol J, Argout X, Allario T, Wincker P, Talon M, Ollitrault P, Morillon R (2008) Transferability of the EST-SSRs developed on nules clementine (Citrus clementina hort ex tan) to other citrus species and their effectiveness for genetic mapping. BMC Genomics 9: 287.
51. Marcus JP, Green JL, Goulter KC, Manners JM (1999) A family of antimicrobial peptides is produced by processing of a 7 s globulin protein in Macadamia integrifolia kernels. Plant J For Cell Mol Biol 19(6): 699-710.
52. Melan MA, Dong X, Endara ME, Davis KR, Ausubel FM, Peterman TK (1993) An Arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiol 101(2): 441-450.
53. Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30(2): 194-200.
54. Motamayor JC, Lachenaud P, da Silva E, Mota JW, Loor R, Kuhn DN, Brown JS, Schnell RJ (2008) Geographic and genetic population differentiation of the amazonian chocolate tree (Theobroma cacao L.). PLoS ONE 3(10): e3311.
55. Ogundiwin EA, Peace CP, Gradziel TM, Parfitt DE, Bliss FA, Crisosto CH (2009) A fruit quality gene map of Prunus. BMC Genomics 10: 587.
56. Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD (1988) Resolution of quantitative traits into mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335: 721-726.
57. Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85(8): 2444-2448.
58. Pinto LR, Oliveira KM, Ulian EC, Garcia AAF, de Souza AP (2004) Survey in the sugarcane expressed sequence tag database (SUCEST) for simple sequence repeats. Genome/National Research Council Canada 47(5): 795-804.
59. Poncet V, Rondeau M, Tranchant C, Cayrel A, Hamon S, de Kochko A, Hamon P (2006) SSR mining in coffee tree EST databases: Potential use of EST-SSRs as markers for the coffea genus. Mol Genet Genomics 276(5): 436-449.
60. Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12(1): 29-36.
61. Powell W, Machray GC, Provan J (1996) Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1(7): 215-222.
62. Pugh T, Fouet O, Risterucci AM, Brottier P, Abouladze M, Deletrez C, Courtois B, Clement D, Larmande P, N'Goran JAK, Lanaud C (2004) A new cacao linkage map based on codominant markers: development and integration of 201 new microsatellite markers. Theor Appl Genet 108(6): 1151-1161.
63. Queiroz VT, Guimaraes CT, Anhert D, Schuster I, Daher RT, Pereira MG, Miranda VRM, Loguercio LL, Barros EG, Moreira MA (2003) Identification of a major QTL in cocoa (Theobroma cacao L.) associated with resistance to witches' broom disease. Plant Breed 122(3): 268-272.
64. Ribeiro SFF, Agizzio AP, Machado OLT, Neves-Ferreira AGC, Oliveira MA, Fernandes KVS, Carvalho AO, Perales J, Gomes VM (2007) A new peptide of melon seeds which shows sequence homology with vicilin: partial characterization and antifungal activity. Sci Hortic 111(4): 399-405.
65. Riju A, Rajesh MK, Sherin PTPF, Chandrasekar A, Apshara SE, Arunachalam V (2009) Mining of expressed sequence tag libraries of cacao for microsatellite markers using five computational tools. J Genet 88: 217-225.
66. Rimbach G, Melchin M, Moehring J, Wagner AE (2009) Polyphenols from cocoa and vascular health-a critical review. Int J Mol Sci 10(10): 4290-4309.
67. Risterucci AM, Grivet L, N'Goran JAK, Pieretti I, Flament MH, Lanaud C (2000) A high-density linkage map of Theobroma cacao L. Theor Appl Genet 101(5-6): 948-955.
68. Risterucci AM, Paulin D, Ducamp M, N'Goran JAK, Lanaud C (2003) Identification of QTLs related to cocoa resistance to three species of Phytophthora. Theor Appl Genet 108(1): 168-174.
69. Rozen SaS H (2000) Primer3 on the www for general users and for biologist programmers. Meth Mol Biol 132: 365-386.
70. Sorrells ME, Wilson WA (1997) Direct classification and selection of superior alleles for crop improvement. Crop Sci 37(3): 691-697.
71. Stintzi A, Heitz T, Prasad V, Wiedemannmerdinoglu S, Kauffmann S, Geoffroy P, Legrand M, Fritig B (1993) Plant pathogenesis-related proteins and their role in defense against pathogens. Biochimie 75(8): 687-706.
72. Temnykh S, Park WD, Ayres N, Cartinhour S, Hauck N, Lipovich L, Cho YG, Ishii T, McCouch SR (2000) Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.). Theor Appl Genet 100(5): 697-712.
73. Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR markers in barley (Hordeum vulgare L.). Theor Appl Genet 106(3): 411-422.
74. van Ooijen JW (2006) Joinmap, software for the calculation of genetic linkage maps, version 4, Wageningen, The Netherlands.
75. Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23(1): 48-55.
76. Verica JA, Maximova SN, Strem MD, Carlson JE, Bailey BA, Guiltinan MJ (2004) Isolation of ESTs from cacao (Theobroma cacao L.) leaves treated with inducers of the defense response. Plant Cell Rep 23(6): 404-413.
77. Véronési C, Rickauer M, Fournier J, Pouénat ML, Esquerré-Tugayé MT (1996) Lipoxygenase gene expression in the tobacco-Phytophthora parasitica nicotianae interaction. Plant Physiol 112(3): 997-1004.
78. Voigt J, Heinrichs H, Voigt G, Bieh B (1994) Cocoa-specific aroma precursors are generated by proteolytic digestion of the vicilin-like globulin of cocoa seeds. Food Chem 50(2): 177-184.
79. Wang X, Bunkers GJ, Walters MR, Thoma RS (2001) Purification and characterization of three antifungal proteins from cheeseweed (Malva parviflora). Biochem Biophys Res Commun 282(5): 1224-1228.
80. Wasmuth JD, Blaxter ML (2004) Prot4est: translating expressed sequence tags from neglected genomes. BMC Bioinform 5: 187.
81. Whitlock BA, Bayer C, Baum DA (2001) Phylogenetic relationships and floral evolution of the Byttnerioideae (Sterculiaceae or Malvaceae s. l.) based on sequences of the chloroplast gene, ndhF. Syst Bot 26(2): 420-437.