A Multidisciplinary Approach Providing New Insight into Fruit Flesh Browning Physiology in Apple (Malus x domestica Borkh.)

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Di Guardo, Mario ^a   Tadiello, Alice ^a   Farneti, Brian ^b   Lorenz, Giorgia ^a   Masuero, Domenico ^a   Vrhovsek, Urska ^a   Costa, Guglielmo ^b   Velasco, Riccardo ^a   Costa, Fabrizio ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CATECHOL OXIDASE; MOLECULAR MARKER; PHENYLALANINE AMMONIA LYASE; POLYPHENOL;

APPLE; ARTICLE; CELL METABOLISM; ENZYME ACTIVITY; GENE ACTIVATION; GENE DUPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCATION; GENE SEQUENCE; GENETIC LINKAGE; GENETIC REGULATION; GLYCATION; MD PAL GENE; MD PPO GENE; PLANT PHYSIOLOGY; PPO GENE; RNA ISOLATION; SINGLE NUCLEOTIDE POLYMORPHISM;

CATECHOL OXIDASE; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MALUS; PHENYLALANINE AMMONIA-LYASE; QUANTITATIVE TRAIT LOCI;

EID: 84885750244     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078004     Document Type: Article

References (68)

1. Giovannoni JJ, (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52: 725-749. doi:10.1146/annurev.arplant.52.1.725. PubMed: 11337414.
2. Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C, (2003) Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol Biol 52: 511-526. doi:10.1023/A:1024886500979. PubMed: 12956523.
3. Newcomb RD, Crowhurst RN, Gleave AP, Rikkerink EHA, Allan AC, et al. (2006) Analyses of Expressed Sequence Tags from Apple. Plant Physiol 141: 147-166. doi:10.1104/pp.105.076208. PubMed: 16531485.
4. Park S, Sugimoto N, Larson MD, Beaudry R, van Nocker S, (2006) Identification of Genes with Potential Roles in Apple Fruit Development and Biochemistry through Large-Scale Statistical Analysis of Expressed Sequence Tags. Plant Physiol 141: 811-824. doi:10.1104/pp.106.080994. PubMed: 16825339.
5. Costa F, Alba R, Schouten H, Soglio V, Gianfranceschi L, et al. (2010) Use of homologous and heterologous gene expression profiling tools to characterize transcription dynamics during apple fruit maturation and ripening. BMC Plant Biol 10: 299. PubMed: 20973957.
6. Ohlsson T, (1994) Minimal processing - preservation methods of the future - an overview. Trends Food Sci Technol 5: 341-344. doi:10.1016/0924-2244(94)90210-0.
7. Gunes G, Watkins CB, Hotchkiss JH, (2001) Physiological responses of fresh-cut apple slices under high CO2 and low O2 partial pressures. Postharvest Biol Technol 22: 197-204. doi:10.1016/S0925-5214(01)00083-7.
8. Coseteng MY, Lee CY, (1987) Changes in apple polyphenoloxidase and polyphenol concentrations in relation to degree of browning. J Food Sci 52(4):: 985--989. doi:10.1111/j.1365-2621.1987.tb14257.x.
9. Murata M, Tsurutani M, Tomita M, Homma S, Kaneko K, (1995) Relationship between Apple Ripening and Browning: Changes in Polyphenol Content and Polyphenol Oxidase. J Agric Foods Chemestry 43(5).
10. Amiot MJ, Tacchini M, Aubert S, Nicolas J, (1992) Phenolic compounds and browning susceptibility of various apple cultivars at maturity. J Food Sci 57(4):: 958-962. doi:10.1111/j.1365-2621.1992.tb14333.x.
11. Demeke T, Morris CF, (2002) Molecular characterization of wheat polyphenol oxidase (PPO). Theor Appl Genet 104: 813-818. doi:10.1007/s00122-001-0847-3. PubMed: 12582641.
12. Boss PK, Gardner RC, Janssen B-J, Ross GS, (1995) An apple polypgenol oxidase cDNA is up-regulated in wounded tissues. Plant Mol Biol 27: 429-433. doi:10.1007/BF00020197. PubMed: 7888632.
13. Martinez MV, Whitaker JR, (1995) The biochemistry and control of enzymatic browning. Trends Food Sci Technol 6: 195-200. doi:10.1016/S0924-2244(00)89054-8.
14. Murata M, Nishimura M, Murai N, Haruta M, Homma S, et al. (2001) A transgenic apple callus showing reduced polyphenol oxidase activity and lower browning potential. Biosci Biotechnol Biochemestry 65(2):: 383-388. doi:10.1271/bbb.65.383.
15. Gorny JR, Hess-Pierce B, Cifuentes RA, Kader AA, (2002) Quality changes in fresh-cut pear slices as affected by controlled atmospheres and chemical preservatives. Postharvest Biol Technol 24: 271-278. doi:10.1016/S0925-5214(01)00139-9.
16. Nicolas JJ, Richard-Forget FG, Goupy PM, Amiot MJ, Aubert SY, (1994) Enzymatic browning reactions in apple and apple products. Crit Rev Food Sci Nutr 34: 109-157. doi:10.1080/10408399409527653. PubMed: 8011143.
17. Chow Y-N, Louarme L, Bonazzi C, Nicolas J, Billaud C, (2011) Apple polyphenoloxidase inactivation during heating in the presence of ascorbic acid and chlorogenic acid. Foods Chemestry 129: 761-767.
18. Serpen A, Gökmen V, (2007) Reversible degradation kinetics of ascorbic acid under reducing and oxidizing condition. Food Chem 104: 721-725. doi:10.1016/j.foodchem.2006.11.073.
19. Buta JG, Moline HE, Spaulding DW, Wang CY, (1999) Extending Storage Life of Fresh-Cut Apples Using Natural Products and Their Derivatives. J Agric Food Chem 1: 1-6. PubMed: 10563838.
20. Davey MW, Kenis K, Keulemans J, (2006) Genetic control of fruit vitamin C contents. Plant Physiol 142: 343-351. doi:10.1104/pp.106.083279. PubMed: 16844833.
21. Kenis K, Keulemans J, Davey MK, (2008) Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes 4: 647-661. doi:10.1007/s11295-008-0140-6.
22. Cova V, Perini D, Soglio V, Komjanc M, van de Weg WE, et al. (2012) Exploiting expressed sequence tag databases for mapping markers associated with fruit development and fruit quality in apple. Mol Breeding 29: 699-715. doi:10.1007/s11032-011-9584-8.
23. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, et al. (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42(10):: 833-839. doi:10.1038/ng.654. PubMed: 20802477.
24. Voorrips RE, (2002) MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered 93: 77-78. doi:10.1093/jhered/93.1.77. PubMed: 12011185.
25. Longhi S, Moretto M, Viola R, Velasco R, Costa F, (2012) Comprehensive QTL mapping survey dissects the complex fruit texture physiology in apple (Malus x domestica Borkh.). J Exp Bot 63(3):: 1107-1121. doi:10.1093/jxb/err326. PubMed: 22121200.
26. Van Ooijen JW, (2006) JoinMap® 4, Software for the Calculation of Genetic Linkage Maps in Experimental Populations. Wageningen, Netherlands: Kyazma, B.V.
27. Van Ooijen JW, (2009) MAPQTL® 6, Software for the mapping of quantitative trait loci in experimental populations of diploid species. Wageningen, Netherlands: Kyazma, B.V.
28. Muller PY, Janovjak H, Miserez AR, Dobbie Z, (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. BioTechniques 32: 1372-1379. PubMed: 12074169.
29. Theodoridis G, Gika H, Franceschi P, Caputi L, Arapitsas P, et al. (2012) LC-MS based global metabolite profiling of grapes: solvent extraction protocol optimization. Metabolomics 8: 175--185. doi:10.1007/s11306-011-0389-x.
30. Vrhovsek U, Masuero D, Gasperotti M, Franceschi P, Caputi L, et al. (2012) A Versatile Targeted Metabolomics Method for the Rapid Quantification of Multiple Classes of Phenolics in Fruits and Beverages. J Agric Food Chem 60: 8831--8840. doi:10.1021/jf2051569. PubMed: 22468648.
31. Newman SM, Eannetta NT, Yu H, Prince JP, de Vicente MC, et al. (1993) Organization of the tomato polyphenol oxidase gene family. Plant Mol Biol 21: 1035-1051. doi:10.1007/BF00023601. PubMed: 8098228.
32. Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, et al. (2002) Development and characterisation of 140 new microsatellites in apple (Malus x domestica Borkh.). Mol Breeding 10: 217-241. doi:10.1023/A:1020525906332.
33. Liebhard R, Koller B, Gianfranceschi L, Gessler C, (2003) Creating a saturated reference map for the apple (Malus x domestica Borkh.) genome. Theor Appl Genet 106: 1497-1508. PubMed: 12677403.
34. Yamamoto T, Kimura T, Saito T, Kotobuki K, Matsuta N, et al. (2004) Genetic linkage maps of Japanese and European pears aligned to the apple consensus map. Acta Hort 663: 51-56.
35. Folta KM, Gardiner SE, (2009) Genetics and genomics of rosaceae. Springer Verlag, ISBN 978-0-387-77490-9. doi:10.1007/978-0-387-77491-6.
36. Tran TL, Taylor JS, Constabel CP, (2012) The polyphenol oxidase gene family in land plants: Lineage-specific duplication and expansion. BMC Genomics 13: 395. doi:10.1186/1471-2164-13-395. PubMed: 22897796.
37. Thygesen PW, Dry IB, Robinson SP, (1995) Polyphenol oxidase in potato. A multigene family that exhibits differential expression patterns. Plant Physiol 109: 525-531. doi:10.1104/pp.109.2.525. PubMed: 7480344.
38. Van der Hoeven R, Ronning C, Giovannoni J, Martin G, Tanksley S, (2002) Deduction about the number, organization and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell 14: 1441-1456. doi:10.1105/tpc.010478. PubMed: 12119366.
39. Jorde LB, (1995) Linkage disequilibrium as a gene-mapping tool. Am J Hum Genet 56: 11-14. PubMed: 7825565.
40. Jorde LB, (2000) Linkage disequilibrium and the search for complex disease genes. Genome Res 10: 1435-1444. doi:10.1101/gr.144500. PubMed: 11042143.
41. Rafalski A, (2002) Application of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5: 94-100. doi:10.1016/S1369-5266(02)00240-6. PubMed: 11856602.
42. Krawczak M, Ball EV, Fenton I, Stenson PD, Abeysinghe S, et al. (2000) Human gene mutation database-A biomedical information and research resource. Hum Mutat 15: 45-51. doi:10.1002/(SICI)1098-1004(200001)15:1. PubMed: 10612821.
43. Schlötterer C, (2004) The evolution of molecular markers - just a matter of fashion? Nat Rev Genet, 5: 63-69. PubMed: 14666112.
44. Fridman E, Pleban T, Zamir D, (2000) A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc Natl Acad Sci USA 97(9):: 4718-4723. doi:10.1073/pnas.97.9.4718. PubMed: 10781077.
45. Gupta PK, Roy JK, Prasad M, (2001) Single nucleotide polymorphisms: A new paradigm for molecular marker technology and DNA polymorphism detection with emphasis on their use in plants. Curr Sci 80(4):: 524-535.
46. Wilson LM, Whitt SR, Ibanez AM, Rocheford TR, Goodman MM, et al. (2004) Dissection of Maize Kernel Composition and Starch Production by Candidate Gene Association. The Plant Cell, doi/10.1105/tpc. p. 104.025700.
47. Lu Y, Yan J, Guimarães CT, Taba S, Hao Z, et al. (2009) Molecular characterization of global maize breeding germplasm based on genome-wide single nucleotide polymorphisms. Theor Apple Genet 120: 93-115. doi:10.1007/s00122-009-1162-7. PubMed: 19823800.
48. Costa F, Peace CP, Stella S, Serra S, Musacchi S, et al. (2010) QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malusxdomestica Borkh.). J Exp Bot 61(11):: 3029-3039. doi:10.1093/jxb/erq130. PubMed: 20462945.
49. Emanuelli F, Battilana J, Costantini L, Le Cunff, et al Boursiquot JM,. (2010) A candidate gene association study on muscat flavor in grapevine (Vitis vinifera. p. pp. L.). BMC Plant Biology 10, 241.
50. Dunemann F, Ulrich D, Malysheva-Otto L, Weber WE, Longhi S, et al. (2012) Functional allelic diversity of the apple alcohol acyl-transferase gene MdAAT1 associated with fruit ester volatile contents in apple cultivars. Mol Breeding 29: 609-625. doi:10.1007/s11032-011-9577-7.
51. Longhi S, Hamblin MT, Trainotti L, Peace CP, Velasco R, et al. (2013) A candidate gene based approach validates Md-PG1 as the main responsible for a QTL impacting fruit texture in apple (Malus x domestica Borkh.). BMC Plant Biol 13: 37. doi:10.1186/1471-2229-13-37. PubMed: 23496960.
52. Micheletti D, Troggio M, Zharkikh A, Costa F, Malnoy M, et al. (2011) Genetic diversity of the genus Malus and implications for linkage mapping with SNPs. Tree Genet Genomes 7: 857-868. doi:10.1007/s11295-011-0380-8.
53. Chagné D, Carlisle CM, Blond C, Volz RK, Whitworth CJ, et al. (2007) Mapping a candidate gene (MdMYB10)for red flesh and foliage colour in apple. BMC Genomics 8: 212. doi:10.1186/1471-2164-8-212. PubMed: 17608951.
54. Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, et al. (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49: 414-427. doi:10.1111/j.1365-313X.2006.02964.x. PubMed: 17181777.
55. Chagné D, Krieger C, Rassam M, Sullivan M, Fraser J, et al. (2012) QTL and candidate gene mapping for polyphenolic composition in apple fruit. BMC Plant Biol 12: 12. doi:10.1186/1471-2229-12-12. PubMed: 22269060.
56. Kumar S, Chagné D, Bink MCAM, Volz RK, Whitworth C, et al. (2012) Genomic selection for fruit quality traits in apple (Malus x domestica Borkh.). PLOS_ONE 7(5):: 1-10.
57. Mellidou I, Chagné D, Laing WA, Keulemans J, Davey MW, (2012) Allelic variation in paralogs of GDP-L-Galactose phosphoryòase is a major determinant of vitamin C concentration in apple fruit. Plant Physiol 160: 1613-1629. doi:10.1104/pp.112.203786. PubMed: 23001142.
58. Franck C, Baetens M, Lammertyn J, Verboven P, Davey MW, et al. (2003) Ascorbic acid concentration in cv. Conference pears during fruit development and postharvest storage. Journal of Agricultural Food Chemestry 51: 4757-4763.
59. Ogundiwin EA, Peace CP, Gradziel TM, Parfitt DE, Bliss FA, et al. (2009) A fruit quality gene map of Prunus. BMC Genomics 10: 587. doi:10.1186/1471-2164-10-587. PubMed: 19995417.
60. Treutter D, (2001) Biosynthesis of phenolic compounds and its regulation in apple. Plant Growth Regul 34: 71-89. doi:10.1023/A:1013378702940.
61. Pannala AS, Chan TS, O'Brien PJ, Rice-Evans CA, (2001) Flavonoid B-ring chemistry and antioxidant activity: fast reaction kinetics. Biochem Biophys Res Commun 282: 1161-1168. doi:10.1006/bbrc.2001.4705. PubMed: 11302737.
62. Regev-Shoshani G, Shoseyov O, Bilkis I, Kerem Z, (2003) Glycosylation of resveratrol protects it from enzymic oxidation. Biochem J 374: 157-163. doi:10.1042/BJ20030141. PubMed: 12697026.
63. Spanos GA, Wrolstad RE, Heatherbell DA, (1990) Influence of processing and storage on the phenolic composition of apple juice. J, Agric Food Chem 38: 1572-1579. doi:10.1021/jf00097a031.
64. MacDonald MJ, D'Cunha GB, (2007) A modern view of phenylalanine ammonia lyase. Biochemestry Cell Biol 85(3):: 273-282. doi:10.1139/O07-018.
65. Bagal UR, Leebens-Mack JH, Lorenz WW, Dean JFD, (2012) The phenylalanine ammonia lyase (PAL) gene family shows a gymnosperm-specific lineage. BMC Genomics 13: 51. doi:10.1186/1471-2164-13-51. PubMed: 22296850.
66. Choi Y-j, Tomás-Barberán, Saltveit ME, (2002) Wound-induced phenolic accumulation and browning in lettuce (Lactuca sativa L.) leaf tissue is reduced by exposure to n-alcohols. Postharvest Biol Technol 37: 47-55.
67. Constabel CP, Bergey DR, Ryan CA, (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92: 407-411. doi:10.1073/pnas.92.2.407. PubMed: 7831300.
68. Thipyapong P, Steffens JC, (1997) Tomato Polyphenol Oxidase (Differential Response of the Polyphenol Oxidase F Promoter to Injuries and Wound Signals). Plant Physiol 1158(2):: 409-418.