A dense SNP genetic map constructed using restriction site-associated DNA sequencing enables detection of QTLs controlling apple fruit quality

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Sun, Rui ^a   Chang, Yuansheng ^a   Yang, Fengqiu ^b   Wang, Yi ^a   Li, Hui ^a   Zhao, Yongbo ^b   Chen, Dongmei ^b   Wu, Ting ^a   Zhang, Xinzhong ^a   Han, Zhenhai ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF CEREAL AND OIL CROPS   (China)

Author keywords

Apple; Candidate genes; Fruit quality traits; Genetic maps; QTL; RADseq; SNP

Indexed keywords

SUGAR; GENETIC MARKER;

ACIDITY; APPLE; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; FRUIT FIRMNESS; FRUIT RIPENING; GENE EXPRESSION; HORTICULTURE; NONHUMAN; PHENOTYPE; PLANT BREEDING; PLANT GENE; PLANT GENOME; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; REAL TIME POLYMERASE CHAIN REACTION; RESTRICTION SITE; SEEDLING; SINGLE NUCLEOTIDE POLYMORPHISM; WEIGHT; CHROMOSOMAL MAPPING; FOOD QUALITY; FRUIT; GENETIC LINKAGE; GENETIC MARKER; GENETICS; GENOTYPE; MALUS; QUANTITATIVE TRAIT; REPRODUCIBILITY;

CHROMOSOME MAPPING; FOOD QUALITY; FRUIT; GENES, PLANT; GENETIC LINKAGE; GENETIC MARKERS; GENOTYPE; MALUS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE; REPRODUCIBILITY OF RESULTS;

EID: 84946477447     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1946-x     Document Type: Article

References (70)

1. Liebhard R, Koller B, Gianfranceschi L, Gessler C. Creating a saturated reference map for the apple (Malus × domestica Borkh.) genome. Theor Appl Genet. 2003;106:1497-508.
2. Kenis K, Keulemans J. Genetic linkage maps of two apple cultivars (Malus × domestica Borkh.) based on AFLP and microsatellite markers. Mol Breeding. 2005;15:205-19.
3. Celton JM, Tustin DS, Chagné D, Gardiner SE. Construction of a dense genetic linkage map for apple rootstocks using SSRs developed from Malus ESTs and Pyrus genomic sequences. Tree Genet Genomes. 2009;5:93-107.
4. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, et al. The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet. 2010;42:833-9.
5. Antanaviciute L, Fernández-Fernández F, Jansen J, Banchi E, Evans KM, Viola R, et al. Development of a dense SNP-based linkage map of an apple rootstock progeny using the Malus Infinium whole genome genotyping array. BMC Genomics. 2012;13:203.
6. Clark MD, Schmitz CA, Rosyara UR, Luby JJ, Bradeen JM. A consensus 'Honeycrisp' apple (Malus × domestica) genetic linkage map from three full-sib progeny populations. Tree Genet Genomes. 2014;10:627-39.
7. Hackett CA. Statistical methods for QTL mapping in cereals. Plant Mol Biol. 2002;48:585-99.
8. Sorkheh K, Malysheva-Otto LV, Wirthensohn MG, Tarkesh-Esfahani S, Martinez-Gomez P. Linkage disequilibrium, genetic association mapping and gene localization in crop plants. Genet Mol Biol. 2008;31:805-14.
9. Khan MA, Korban SS. Association mapping in forest trees and fruit crops. J Exp Bot. 2012;63:4045-60.
10. Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, et al. The genome of the pear (Pyrusbretschneideri Rehd.). Genome Res. 2013;23:396-408.
11. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nat. 2007;449:463-7.
12. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, et al. The draft genome of sweet orange (Citrus sinensis). Nat Genet. 2013;45:59-66.
13. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet. 2011;12:499-510.
14. Miller MR, Dunham JP, Amores A, Cresko WA, Johnson EA. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res. 2007;17:240-8.
15. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One. 2008;3:e3376.
16. Baxter SW, Davey JW, Johnston JS, Shelton AM, Heckel DG, Jiggins CD, et al. Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism. PLoS One. 2011;6:e19315.
17. Pfender WF, Saha MC, Johnson EA, Slabaugh MB. Mapping with RAD (restriction-site associated DNA) markers to rapidly identify QTL for stem rust resistance in Loliumperenne. Theor Appl Genet. 2011;122:1467-80.
18. Wu J, Li LT, Li M, Khan MA, Li XG, Chen H, et al. High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. J Exp Bot. 2014;65(20):5771-81.
19. Chutimanitsakun Y, Nipper RW, Cuesta-Marcos A, Cistué L, Corey A, Filichkina T, et al. Construction and application for QTL analysis of a Restriction Site Associated DNA (RAD) linkage map in barley. BMC Genomics. 2011;12:4.
20. Yang H, Tao Y, Zheng Z, Li C, Sweetingham MW, Howieson JG. Application of next-generation sequencing for rapid marker development in molecular plant breeding: a case study on anthracnose disease resistance in Lupinusangustifolius L. BMC Genomics. 2012;13:318.
21. Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C. Mapping quantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol Biol. 2003;52:511-26.
22. Kenis K, Keulemans J, Davey MW. Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes. 2008;4:647-61.
23. Zhang Q, Ma BQ, Li H, Chang YS, Han YY, Li J, et al. Identification, characterization, and utilization of genome-wide simple sequence repeats to identify a QTL for acidity in apple. BMC Genomics. 2012;13:537.
24. Brown AG, Harvey DM. Nature and inheritance of sweetness and acidity in cultivated apple. Euphytica. 1971;20:68-80.
25. Visser T, Verhaegh JJ. Inheritance and selection of some fruit characters of apple. I. Inheritance of low and high acidity. Euphytica. 1978;27:753-60.
26. Xu K, Wang A, Brown S. Genetic characterization of the Ma locus with pH and titratable acidity in apple. Mol Breeding. 2012;30:899-912.
27. Maliepaard C, Alston FH, van Arkel G, Brown LM, Chevreau E, Dunemann F, et al. Aligning male and female linkage maps of apple (Maluspumila Mill.) using multi-allelic markers. Theor Appl Genet. 1998;97:60-73.
28. Kumar S, Chagne D, Bink MC, Volz RK, Whitworth C, Carlisle C. Genomic selection for fruit quality traits in apple (Malus × domestica Borkh.). PLoS One. 2012;7:e36674.
29. Visser T, Schaap AA, De Vries DP. Acidity and sweetness in apple and pear. Euphytica. 1968;17:153-67.
30. Guan YZ, Evans KM, Peace C, Luby JJ, Brown SK, Schmitz CA, et al. Phenotypic diversity and QTL detection of individual sugars in RosBREED apple germplasm [abstract]. San Diego, CA: International Plant & Animal Genome XXI Conference; 2013.
31. Devoghalaere F, Doucen T, Guitton B, Keeling J, Payne W, Ling TJ, et al. A genomics approach to understanding the role of auxin in apple (Malus × domestica) fruit size control. BMC Plant Biol. 2012;12:7.
32. Longhi S, Moretto M, Viola R, Velasco R, Costa F. Comprehensive QTL mapping survey dissects the complex fruit texture physiology in apple (Malus × domestica Borkh.). J Exp Bot. 2012;63:1107-21.
33. Longhi S, Hamblin MT, Trainotti L, Peace CP, Velasco R, Costa F. A candidate gene based approach validates Md-PG1 as the main responsible for a QTL impacting fruit texture in apple (Malus × domestica Borkh). BMC Plant Biol. 2013;13:37.
34. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH. Stacks: building and genotyping Loci de novo from short-read sequences. G3-Genes Genom Genet. 2011;1(3):171-82.
35. Van Ooijen JW. JoinMap 4, Software for the calculation of genetic linkage maps in experimental populations. Wageningen, Netherlands: Kyazma BV; 2006.
36. Wu JH, Gao HY, Zhao L, Liao XJ, Chen F, Wang ZF, et al. Chemical compositional characterization of some apple cultivars. Food Chem. 2007;103:88-93.
37. Van Ooijen JW. MapQTL 6.0, Software for the mapping of quantitative trait loci in experimental populations of diploid species. Wageningen, Netherlands: Kyazma BV; 2009.
38. Zhang YG, Cheng JH, Xu XF, Li TZ. Comparison of methods for total RNA isolation from Malusxiaojinensis LD-PCR amplification. Biotechnol Inform. 2005;4:50-3.
39. Li TY, Wang Y, Zhang XZ, Han ZH. Isolation and characterization of ARRO-1 genes from apple rootstocks in response to auxin treatment. Plant Mol Biol Rep. 2012;30:1408-14.
40. Hackett CA, Broadfoot LB. Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps. Heredity. 2003;90:33-8.
41. Celton JM, Kelner JJ, Martinez S, Bechti A, KhelifiTouhami A, James MJ, et al. Fruit self-thinning: a trait to consider for genetic improvement of apple tree. PLoS One. 2014;9:e91016.
42. Quinones PM, Urquiza GC, Zerbini PA, Zerbini FM. Molecular diversity of begomoviruses in the pepper crop in Cuba. Rev Prot Veget. 2014;29:57-61.
43. Chagné D, Gasic K, Crowhurst RN, Han YP, Bassett HC, Bowatte DR, et al. Development of a set of SNP markers present in expressed genes of the apple. Genomics. 2008;92:353-8.
44. Han YP, Chagné D, Gasic K, Rikkerink EHA, Beever JE, Gardiner SE, et al. BAC-end sequence-based SNPs and Bin mapping for rapid integration of physical and genetic maps in apple. Genomics. 2009;93:282-8.
45. Chagné D, Crowhurst RN, Troggio M, Davey MW, Gilmore B, Lawley C, et al. Genome-wide SNP detection, validation, and development of an 8 K SNP array for apple. PLoS One. 2012;7(2):e31745.
46. Khan MA, Han YP, Zhao YF, Korban SS. A high-throughput apple SNP genotyping platform using the GoldenGate™ assay. Gene. 2012;494:196-201.
47. Bianco L, Cestaro A, Sargent DJ, Banchi E, Derdak S, Guardo MD, et al. Development and validation of a 20 K Single Nucleotide Polymorphism (SNP) whole genome genotyping array for apple (Malus × domestica Borkh). PLoS One. 2014;9(10):e110377.
48. Han YP, Zheng DM, Vimolmangkang S, Khan MA, Beever JE, Korban SS. Integration of physical and genetic maps in apple confirms whole-genome and segmental duplications in the apple genome. J Exp Bot. 2011;62:5117-30.
49. Fernández-Fernández F, Antanaviciute L, van Dyk MM, Tobutt KR, Evans KM, Rees DJG, et al. A genetic linkage map of an apple rootstock progeny anchored to the Malus genome sequence. Tree Genet Genomes. 2012;8:991-1002.
50. Khan MA, Han Y, Zhao YF, Troggio M, Korban SS. A multi-population consensus genetic map reveals inconsistent marker order among maps likely attributed to structural variations in the apple genome. PLoS One. 2012;7:e47864.
51. Park SW, Jung JK, Choi EA, Kwon JK, Kang JH, Jahn M, et al. An EST-based linkage map reveals chromosomal translocation in Capsicum. Mol Breeding. 2014;34:963-75.
52. Jiang J, Gill BS. Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome. 2006;49:1057-68.
53. Yao YX, Li M, Liu Z, You CX, Wang DM, Zhai H, et al. Molecular cloning of three malic acid related genes MdPEPC, MdVHA-A, MdcyME and their expression analysis in apple fruits. Sci Hortic. 2009;122:404-8.
54. Yao YX, Li M, Zhai H, You CX, Hao YJ. Isolation and characterization of an apple cytosolic malate dehydrogenase gene reveal its function in malate synthesis. J Plant Physiol. 2011;168:474-80.
55. Harada T, Sunako T, Wakasa Y, Soejima J, Satoh T, Niizeki M. An allele of the 1-aminocyclopropane-1-carboxylate synthase gene (Md-ACS1) accounts for the low level of ethylene production in climacteric fruits of some apple cultivars. Theor Appl Genet. 2000;101:742-6.
56. Brummell DA, Harpster MH. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol. 2001;47:311-39.
57. White PJ. Recent advances in fruit development and ripening: an overview. J Exp Bot. 2002;53:1995-2000.
58. Costa F, Stella S, Van de Weg WE, Guerra W, Cecchinel M, Dallavia J, et al. Role of the genes Md-ACO1 and Md-ACS1 in ethylene production and shelf life of apple (Malus × domestica Borkh). Euphytica. 2005;141:181-90.
59. Potts SM, Khan MA, Han Y, Kushad MM, Korban SS. Identification of quantitative trait loci (QTLs) for fruit quality traits in apple. Plant Mol Biol Rep. 2014;32:109-16.
60. Chang YS, Sun R, Sun HH, Zhao YB, Han YP, Chen DM, et al. Mapping of quantitative trait loci corroborates independent genetic control of apple size and shape. Sci Hortic. 2014;174:126-32.
61. Song XJ, Huang W, Shi M, Zhu MZ, Lin HX. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet. 2007;39:623-30.
62. Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, et al. Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol. 2008;8:16.
63. Malladi A, Hirst PM. Increase in fruit size of a spontaneous mutant of 'Gala' apple (Malus × domestica Borkh.) is facilitated by altered cell production and enhanced cell size. J Exp Bot. 2010;61:3003-13.
64. Van Ooijen JW. Accuracy of mapping quantitative trait loci in autogamous species. Theor Appl Genet. 1992;84:803-11.
65. Jansen RC, Van ooijen JW, Stam P, Lister C, Dean C. Genotype-by-environment interaction in genetic mapping of multiple quantitative trait loci. Theor Appl Genet. 1995;91:33-7.
66. Bastiaanse H, Bassett HCM, Kirk C, Gardiner SE, Deng C, Groenworld R et al. Scab resistance in 'Geneva' apple is conditioned by a resistance gene cluster with complex genetic control. Mol Plant Pathology 2015. doi: 10.1111/mpp.12269.
67. Chagné D, Dayatilake D, Diack R, Oliver M, Ireland H, Watson A, et al. Genetic and environmental control of fruit maturation, dry matter and firmness in apple (Malus × domestica Borkh.). Hort Res. 2014;1:14046.
68. Bai Y, Dougherty L, Li MJ, Fazio G, Cheng LL, Xu KN. A natural mutation-led truncation in one of the two aluminum-activated malate transporter-like genes at the Ma locus is associated with low fruit acidity in apple. Mol Genet Genomics. 2012;287:663-78.
69. Chagné D, Krieger C, Rassam M, Sullivan M, Fraser J, André C, et al. QTL and candidate gene mapping for polyphenolic composition in apple fruit. BMC Plant Biol. 2012;12:12.
70. Zhu MT, Wang R, Kong PH, Zhang XZ, Wang Y, Wu T at al. Development of a dot blot macroarray and its use in gene expression marker-assisted selection for iron deficiency tolerant apple rootstocks. Euphytica 2015, doi 10.1007/s10681-015-1354-y.