Molecular Breeding

, Volume 30, Issue 2, pp 899–912 | Cite as

Genetic characterization of the Ma locus with pH and titratable acidity in apple

Article

Abstract

Apple fruit flavor is greatly affected by the level of malic acid, which is the major organic acid in mature apple fruit. To understand the genetic and molecular basis of apple fruit acidity, fruit juice pH and/or titratable acidity (TA) were measured in two half-sib populations GMAL 4595 [Royal Gala × PI (Plant Introduction) 613988] and GMAL 4590 (Royal Gala × PI 613971) of 438 trees in total. The maternal parent Royal Gala is a commercial variety and the paternal parents are two M. sieversii (the progenitor species of domestic apple) elite accessions. The low-acid trait segregates recessively and the overall acidity variations in the two populations were primarily controlled by the Ma (malic acid) locus, a major gene discovered in the 1950s (Nybom in Hereditas 45:332–350, 1959) and later mapped to linkage group 16 (Maliepaard et al. in Theor Appl Genet 97:60–73, 1998). The allele Ma has a strong additive effect in increasing fruit acidity and is incompletely dominant over ma. QTL (quantitative trait locus) analyses in GMAL 4595 mapped the major QTL Ma in both Royal Gala and PI 613988, the effects of which explained 17.0–42.3% of the variation in fruit pH and TA. In addition, two minor QTL, tentatively designated M2 and M3, were also detected for fruit acidity, with M2 on linkage group 6 of Royal Gala and M3 on linkage group 1 of PI 613988. By exploring the genome sequences of apple, eight new simple sequence repeat markers tightly linked to Ma were developed, leading to construction of a fine genetic map of the Ma locus that defines it to a physical region no larger than 150 kb in the Golden Delicious genome.

Keywords

Apple Fruit acidity Ma pH QTL Fine mapping 

Notes

Acknowledgments

The authors would like to sincerely thank Dr. Lailiang Cheng, and the two anonymous reviewers for their critical review of this manuscript, Mr. Phil Forsline and Dr. Herb Aldwinckle for developing the two mapping populations, Mr. Tuanhui Bai for his assistance in fruit evaluation and The New York State Apple Research and Development Program for partial funding support.

Supplementary material

11032_2011_9674_MOESM1_ESM.pdf (670 kb)
Supplementary material 1 (PDF 631 kb)

References

  1. Beruter J (2004) Carbohydrate metabolism in two apple genotypes that differ in malate accumulation. J Plant Physiol 161:1011–1029PubMedCrossRefGoogle Scholar
  2. Blanpied GD, Silsby KJ (1992) Predicting harvest date windows for apples. Information Bulletin 221. Cornell Cooperative Extension, Cornell University, IthacaGoogle Scholar
  3. Boudehri K, Bendahmane A, Cardinet G, Troadec C, Moing A, Dirlewanger E (2009) Phenotypic and fine genetic characterization of the D locus controlling fruit acidity in peach. BMC Plant Biol 9:14CrossRefGoogle Scholar
  4. Brown AG, Harvey DM (1971) Nature and inheritance of sweetness and acidity in cultivated apple. Euphytica 20:68–80CrossRefGoogle Scholar
  5. Davey MW, Kenis K, Keulemans J (2006) Genetic control of fruit vitamin C contents. Plant Physiol 142:343–351PubMedCrossRefGoogle Scholar
  6. Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldere F, Cosson P, Howad W, Arus P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 101:9891–9896PubMedCrossRefGoogle Scholar
  7. Etienne C, Moing A, Dirlewanger E, Raymond P, Monet R, Rothan C (2002a) Isolation and characterization of six peach cDNAs encoding key proteins in organic acid metabolism and solute accumulation: involvement in regulating peach fruit acidity. Physiol Plant 114:259–270PubMedCrossRefGoogle Scholar
  8. Etienne C, Rothan C, Moing A, Plomion C, Bodenes C, Svanella-Dumas L, Cosson P, Pronier V, Monet R, Dirlewanger E (2002b) Candidate genes and QTLs for sugar and organic acid content in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 105:145–159PubMedCrossRefGoogle Scholar
  9. Fang DQ, Federici CT, Roose ML (1997) Development of molecular markers linked to a gene controlling fruit acidity in citrus. Genome 40:841–849PubMedCrossRefGoogle Scholar
  10. Forsline PL, Aldwinckle HS, Dickson EE, Luby JJ, Hokanson SC (2003) Collection, maintenance, characterization and utilization of wild apples of central Asia. Hort Rev 29:1–61Google Scholar
  11. Fulton TM, Bucheli P, Voirol E, Lopez J, Petiard V, Tanksley SD (2002) Quantitative trait loci (QTL) affecting sugars, organic acids and other biochemical properties possibly contributing to flavor, identified in four advanced backcross populations of tomato. Euphytica 127:163–177CrossRefGoogle Scholar
  12. Guerra M, Sanz MA, Casquero PA (2010) Influence of storage conditions on the sensory quality of a high acid apple. Int J Food Sci Technol 45:2352–2357CrossRefGoogle Scholar
  13. Harker FR, Marsh KB, Young H, Murray SH, Gunson FA, Walker SB (2002) Sensory interpretation of instrumental measurements 2: sweet and acid taste of apple fruit. Postharvest Biol Tec 24:241–250CrossRefGoogle Scholar
  14. Jalikop SH (2007) Linked dominant alleles or inter-locus interaction results in a major shift in pomegranate fruit acidity of ‘Ganesh’ × ‘Kabul Yellow’. Euphytica 158:201–207CrossRefGoogle Scholar
  15. Kenis K, Keulemans J, Davey M (2008) Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes 4:647–661CrossRefGoogle Scholar
  16. Kouassi A, Durel C-E, Costa F, Tartarini S, van de Weg E, Evans K, Fernandez–Fernandez F, Govan C, Boudichevskaja A, Dunemann F, Antofie A, Lateur M, Stankiewicz-Kosyl M, Soska A, Tomala K, Lewandowski M, Rutkovski K, Zurawicz E, Guerra W, Laurens F (2009) Estimation of genetic parameters and prediction of breeding values for apple fruit-quality traits using pedigreed plant material in Europe. Tree Genet Genomes 5:659–672CrossRefGoogle Scholar
  17. Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus xdomestica Borkh.). Plant Mol Biol 52:511–526PubMedCrossRefGoogle Scholar
  18. Maliepaard C, Alston FH, van Arkel G, Brown LM, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, van Heusden AW, Janse J, Laurens F, Lynn JR, Manganaris AG, den Nijs APM, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink-van Ginkel M, King GJ (1998) Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97:60–73CrossRefGoogle Scholar
  19. Nielsen SS (2010) Food analysis laboratory manual. Springer, New YorkCrossRefGoogle Scholar
  20. Nybom N (1959) On the inheritance of acidity in cultivated apples. Hereditas 45:332–350CrossRefGoogle Scholar
  21. Oraguzie N, Alspach P, Volz R, Whitworth C, Ranatunga C, Weskett R, Harker R (2009) Postharvest assessment of fruit quality parameters in apple using both instruments and an expert panel. Postharvest Biol Tec 52:279–287CrossRefGoogle Scholar
  22. Patocchi A, Vinatzer BA, Gianfranceschi L, Tartarini S, Zhang HB, Sansavini S, Gessler C (1999) Construction of a 550 kb BAC contig spanning the genomic region containing the apple scab resistance gene Vf. Mol Gen Genet 262:884–891PubMedCrossRefGoogle Scholar
  23. Sargent D, Marchese A, Simpson D, Howad W, Fernández-Fernández F, Monfort A, Arús P, Evans K, Tobutt K (2009) Development of “universal” gene-specific markers from Malus spp. cDNA sequences, their mapping and use in synteny studies within Rosaceae. Tree Genet Genomes 5:133–145CrossRefGoogle Scholar
  24. Schouten H, van de Weg W, Carling J, Khan S, McKay S, van Kaauwen M, Wittenberg A, Koehorst-van Putten H, Noordijk Y, Gao Z, Rees D, Van Dyk M, Jaccoud D, Considine M, Kilian A (2011) Diversity arrays technology (DArT) markers in apple for genetic linkage maps. Mol Breed (online). doi: 10.1007/s11032-011-9579-5
  25. Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus xdomestica Borkh.) genome. Tree Genet Genomes 2:202–224CrossRefGoogle Scholar
  26. Sweetman C, Deluc LG, Cramer GR, Ford CM, Soole KL (2009) Regulation of malate metabolism in grape berry and other developing fruits. Phytochemistry 70:1329–1344PubMedCrossRefGoogle Scholar
  27. Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0, Software for the calculation of QTL positions on genetic maps. Plant Research International, WageningenGoogle Scholar
  28. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D et al (2010) The genome of the domesticated apple (Malus xdomestica Borkh.). Nat Genet 42:833–839PubMedCrossRefGoogle Scholar
  29. Vinatzer BA, Patocchi A, Gianfranceschi L, Tartarini S, Zhang HB, Gessler C, Sansavini S (2001) Apple contains receptor-like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes cosegregating with Vf apple scab resistance. Mol Plant Microbe Interact 14:508–515PubMedCrossRefGoogle Scholar
  30. Visser T, Verhaegh JJ (1978) Inheritance and selection of some fruit characters of apple. 1. Inheritance of low and high acidity. Euphytica 27:753–760CrossRefGoogle Scholar
  31. Visser T, Schaap AA, Devries DP (1968) Acidity and sweetness in apple and pear. Euphytica 17:153–167Google Scholar
  32. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  33. Wang A, Aldwinckle H, Forsline P, Main D, Fazio G, Brown S, Xu K (2011) EST contig-based SSR linkage maps for Malus × domestica cv ‘Royal Gala’ and an apple scab resistant accession of M. sieversii, the progenitor species of domestic apple. Mol Breed. doi: 10.1007/s11032-011-9554-1
  34. Xu K, Xu X, Ronald PC, Mackill DJ (2000) A high-resolution linkage map in the vicinity of the rice submergence tolerance locus Sub1. Mol Gen Genet 263:681–689PubMedCrossRefGoogle Scholar
  35. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708PubMedCrossRefGoogle Scholar
  36. Yao YX, Li M, Liu Z, Hao YJ, Zhai H (2007) A novel gene, screened by cDNA-AFLP approach, contributes to lowering the acidity of fruit in apple. Plant Physiol Biochem 45:139–145PubMedCrossRefGoogle Scholar
  37. Yao Y, Zhai H, Zhao L, Yi K, Liu Z, Song Y (2008) Analysis of the apple fruit acid/low-acid trait by SSR markers. Front Agric China 2:463–466CrossRefGoogle Scholar
  38. Yao YX, Li M, Liu Z, You CX, Wang DM, Zhai H, Hao YJ (2009) Molecular cloning of three malic acid related genes MdPEPC, MdVHA-A, MdcyME and their expression analysis in apple fruits. Sci Hort 122:404–408CrossRefGoogle Scholar
  39. You F, Huo N, Gu Y, Luo M-c, Ma Y, Hane D, Lazo G, Dvorak J, Anderson O (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinform 9:253CrossRefGoogle Scholar
  40. Zhang YZ, Li PM, Cheng LL (2010) Developmental changes of carbohydrates, organic acids, amino acids, and phenolic compounds in ‘Honeycrisp’ apple flesh. Food Chem 123:1013–1018CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Horticulture, New York State Agricultural Experiment StationCornell UniversityGenevaUSA

Personalised recommendations