Analysis of natural variation of the potato tuber proteome reveals novel candidate genes for tuber bruising

Journal of Proteome Research

Volumn 11, Issue 2, 2012, Pages 703-716

  Urbany, Claude ^a   Colby, Thomas ^a   Stich, Benjamin ^a   Schmidt, Lysann ^a   Schmidt, Jürgen ^a   Gebhardt, Christiane ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

association genetics; bruising; candidate genes; class III lipase; enzymatic discoloration; natural variation; potato; proteomics

Indexed keywords

ADENOSINE DIPHOSPHATE GLUCOSE; ANNEXIN; APROTININ; ARACHIDONATE 5 LIPOXYGENASE; ASPARTIC ACID; CATECHOL OXIDASE; ISOPROTEIN; PATATIN ISOFORM; PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR; STARCH; STARCH PHOSPHORYLASE; TRIACYLGLYCEROL LIPASE; TRYPSIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; CULTIVAR; DNA POLYMORPHISM; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; GERMPLASM; MECHANICS; NONHUMAN; PHENOTYPE; PLANT GENETICS; PLANT PARAMETERS; PLANT TISSUE; POTATO; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE TRAIT LOCUS; TISSUE INJURY; TUBER BRUISING;

AGRICULTURE; CASE-CONTROL STUDIES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FOOD; PLANT PROTEINS; PLANT TUBERS; PROTEOME; PROTEOMICS; SOLANUM TUBEROSUM;

SOLANUM TUBEROSUM;

EID: 84855206976     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2006186     Document Type: Article

References (67)

1. Wheeler, R. M.; Tibbitts, T. W. Growth and tuberization of potato (Solanum tuberosum L.) under continuous light Plant Physiol. 1986, 80 (3) 801-804
2. Adams, J. B.; Brown, H. M. Discoloration in raw and processed fruits and vegetables Crit. Rev. Food Sci. Nutr. 2007, 47 (3) 319-333
3. Esquerre, C.; Gowen, A. A.; O'Donnell, C. P.; Downey, G. Initial studies on the quantitation of bruise damage and freshness in mushrooms using visible-near-infrared spectroscopy J. Agric. Food Chem. 2009, 57 (5) 1903-1907
4. Friedman, M. Nutritional consequences of food processing Forum Nutr. 2003, 56, 350-352
5. Matheis, G. Enzymatic browning of foods Z. Lebensm.-Unters.-Forsch. A 1983, 176 (6) 454-462
6. Ravi, V.; Aked, J. Review on tropical root and tuber crops. II. Physiological disorders in freshly stored roots and tubers Crit. Rev. Food Sci. Nutr. 1996, 36 (7) 711-731
7. Murphy, J. P.; Kong, F.; Pinto, D. M.; Wang-Pruski, G. Relative quantitative proteomic analysis reveals wound response proteins correlated with after-cooking darkening Proteomics 2010, 10 (23) 4258-4269
8. Friedman, M. Chemistry, Biochemistry, and Dietary Role of Potato Polyphenols. A Review J. Agric. Food Chem. 1997, 45 (5) 1523-1540
9. Prieto, H.; Utz, D.; Castro, A.; Aguirre, C.; Gonzalez-Aguero, M.; Valdes, H.; Cifuentes, N.; Defilippi, B. G.; Zamora, P.; Zuniga, G.; Campos-Vargas, R. Browning in Annona cherimola fruit: role of polyphenol oxidase and characterization of a coding sequence of the enzyme J. Agric. Food Chem. 2007, 55 (22) 9208-9218
10. Schmitz, G. E.; Sullivan, M. L.; Hatfield, R. D. Three polyphenol oxidases from red clover (Trifolium pratense) differ in enzymatic activities and activation properties J. Agric. Food Chem. 2008, 56 (1) 272-280
11. Segovia-Bravo, K. A.; Jaren-Galan, M.; Garcia-Garcia, P.; Garrido-Fernandez, A. Characterization of polyphenol oxidase from the Manzanilla cultivar (Olea europaea pomiformis) and prevention of browning reactions in bruised olive fruits J. Agric. Food Chem. 2007, 55 (16) 6515-6520
12. Stevens, L. H.; Davelaar, E. Biochemical Potential of Potato Tubers To Synthesize Blackspot Pigments in Relation to Their Actual Blackspot Susceptibility J. Agric. Food Chem. 1997, 45 (11) 4221-4226
13. McGarry, A.; Hole, C. C.; Drew, R. L. K.; Parsons, N. Internal damage in potato tubers: a critical review Postharvest Biol. Technol. 1996, 8 (4) 239-258
14. Luo, Z. W.; Hackett, C. A.; Bradshaw, J. E.; McNicol, J. W.; Milbourne, D. Construction of a genetic linkage map in tetraploid species using molecular markers Genetics 2001, 157 (3) 1369-1385
15. Osborn, T. C.; Alexander, D. C.; Fobes, J. F. Identification of restriction fragment length polymorphisms linked to genes controlling soluble solids content in tomato fruit Theor. Appl. Genet. 1987, 73 (3) 350-356
16. Salvi, S.; Tuberosa, R. To clone or not to clone plant QTLs: present and future challenges Trends Plant Sci. 2005, 10 (6) 297-304
17. Pflieger, S.; Lefebvre, V.; Causse, M. The candidate gene approach in plant genetics: a review Mol. Breeding 2001, 7 (4) 275-291
18. Canovas, F. M.; Dumas-Gaudot, E.; Recorbet, G.; Jorrin, J.; Mock, H. P.; Rossignol, M. Plant proteome analysis Proteomics 2004, 4 (2) 285-298
19. Hoehenwarter, W.; Larhlimi, A.; Hummel, J.; Egelhofer, V.; Selbig, J.; van Dongen, J. T.; Wienkoop, S.; Weckwerth, W. MAPA distinguishes genotype-specific variability of highly similar regulatory protein isoforms in potato tuber J. Proteome Res. 2011, 10 (7) 2979-2991
20. Aghaei, K.; Ehsanpour, A. A.; Komatsu, S. Proteome analysis of potato under salt stress J. Proteome Res. 2008, 7 (11) 4858-4868
21. Agrawal, L.; Chakraborty, S.; Jaiswal, D. K.; Gupta, S.; Datta, A.; Chakraborty, N. Comparative proteomics of tuber induction, development and maturation reveal the complexity of tuberization process in potato (Solanum tuberosum L.) J. Proteome Res. 2008, 7 (9) 3803-3817
22. Badri, M. A.; Rivard, D.; Coenen, K.; Vaillancourt, L. P.; Goulet, C.; Michaud, D.; SELDI-TOF, A MS procedure for the detection, quantitation, and preliminary characterization of low-molecular-weight recombinant proteins expressed in transgenic plants Proteomics 2009, 9 (2) 233-241
23. Barel, G.; Ginzberg, I. Potato skin proteome is enriched with plant defence components J. Exp. Bot. 2008, 59 (12) 3347-3357
24. Chaves, I.; Pinheiro, C.; Paiva, J. A.; Planchon, S.; Sergeant, K.; Renaut, J.; Graca, J. A.; Costa, G.; Coelho, A. V.; Ricardo, C. P. Proteomic evaluation of wound-healing processes in potato (Solanum tuberosum L.) tuber tissue Proteomics 2009, 9 (17) 4154-4175
25. Delaplace, P.; van der Wal, F.; Dierick, J. F.; Cordewener, J. H.; Fauconnier, M. L.; du Jardin, P.; America, A. H. Potato tuber proteomics: comparison of two complementary extraction methods designed for 2-DE of acidic proteins Proteomics 2006, 6 (24) 6494-6497
26. Hoehenwarter, W.; van Dongen, J. T.; Wienkoop, S.; Steinfath, M.; Hummel, J.; Erban, A.; Sulpice, R.; Regierer, B.; Kopka, J.; Geigenberger, P.; Weckwerth, W. A rapid approach for phenotype-screening and database independent detection of cSNP/protein polymorphism using mass accuracy precursor alignment Proteomics 2008, 8 (20) 4214-4225
27. Lehesranta, S. J.; Davies, H. V.; Shepherd, L. V.; Koistinen, K. M.; Massat, N.; Nunan, N.; McNicol, J. W.; Karenlampi, S. O. Proteomic analysis of the potato tuber life cycle Proteomics 2006, 6 (22) 6042-6052
28. Lehesranta, S. J.; Koistinen, K. M.; Massat, N.; Davies, H. V.; Shepherd, L. V.; McNicol, J. W.; Cakmak, I.; Cooper, J.; Luck, L.; Karenlampi, S. O.; Leifert, C. Effects of agricultural production systems and their components on protein profiles of potato tubers Proteomics 2007, 7 (4) 597-604
29. Lehesranta, S. J.; Davies, H. V.; Shepherd, L. V.; Nunan, N.; McNicol, J. W.; Auriola, S.; Koistinen, K. M.; Suomalainen, S.; Kokko, H. I.; Karenlampi, S. O. Comparison of tuber proteomes of potato varieties, landraces, and genetically modified lines Plant Physiol. 2005, 138 (3) 1690-1699
30. Bradshaw, J.; Bryan, G.; Ramsay, G. Genetic resources (including wild and cultivated Solanum species) and progress in their utilisation in potato breeding Potato Res. 2006, 49 (1) 49-65
31. Love, S. L. Founding clones, major contributing ancestors, and exotic progenitors of prominent north American potato cultivars Am. J. Potato Res. 1999, 76, 263-272
32. Gonzalez-Martinez, S. C.; Wheeler, N. C.; Ersoz, E.; Nelson, C. D.; Neale, D. B. Association genetics in Pinus taeda L. I. Wood property traits Genetics 2007, 175 (1) 399-409
33. Li, L.; Paulo, M. J.; Strahwald, J.; Lubeck, J.; Hofferbert, H. R.; Tacke, E.; Junghans, H.; Wunder, J.; Draffehn, A.; van Eeuwijk, F.; Gebhardt, C. Natural DNA variation at candidate loci is associated with potato chip color, tuber starch content, yield and starch yield Theor. Appl. Genet. 2008, 116, 1167-1181
34. Li, L.; Strahwald, J.; Hofferbert, H. R.; Lubeck, J.; Tacke, E.; Junghans, H.; Wunder, J.; Gebhardt, C. DNA variation at the invertase locus invGE/GF is associated with tuber quality traits in populations of potato breeding clones Genetics 2005, 170 (2) 813-821
35. Pajerowska-Mukhtar, K.; Stich, B.; Achenbach, U.; Ballvora, A.; Lübeck, J.; Strahwald, J.; Tacke, E.; Hofferbert, H.-R.; Ilarionova, E.; Bellin, D.; Walkemeier, B.; Basekow, R.; Kersten, B.; Gebhardt, C. Single nucleotide polymorphisms in the Allene Oxide Synthase 2 gene are associated with field resistance to late blight in populations of tetraploid potato cultivars Genetics 2009, 181 (3) 1115-1127
36. Simko, I.; Haynes, K. G.; Jones, R. W. Mining data from potato pedigrees: tracking the origin of susceptibility and resistance to Verticillium dahliae in North American cultivars through molecular marker analysis Theor. Appl. Genet. 2004, 108 (2) 225-230
37. Ross, H. Potato breeding-problems and perspectives; Paul Parey: Berlin and Hamburg, 1986; p 132.
38. Malosetti, M.; van der Linden, C. G.; Vosman, B.; van Eeuwijk, F. A.; Mixed-Model, A Approach to association mapping using pedigree information with an illustration of resistance to phytophthora infestans in potato Genetics 2007, 175 (2) 879-889
39. Gebhardt, C.; Ballvora, A.; Walkemeier, B.; Oberhagemann, P.; Schüler, K. Assessing genetic potential in germplasm collections of crop plants by marker-trait association: a case study for potatoes with quantitative variation of resistance to late blight and maturity type Mol. Breed. 2004, 13 (1) 93-102
40. Urbany, C.; Stich, B.; Schmidt, L.; Simon, L.; Berding, H.; Junghans, H.; Niehoff, K. H.; Braun, A.; Tacke, E.; Hofferbert, H. R.; Lubeck, J.; Strahwald, J.; Gebhardt, C. Association genetics in Solanum tuberosum provides new insights into potato tuber bruising and enzymatic tissue discoloration BMC Genomics 2011, 12, 7
41. Scheele, C. v.; Svensson, G.; Rasmussen, J. Die Bestimmung des Stärkegehaltes und der Trockensubstanz der Kartoffel mit Hilfe des spezifischen Gewichts Landw. VersStn. 1937, 127, 67-96
42. Hughes, J. C.; Grant, A.; Prescott, E. H. A.; Pennington, D. E.; Worts, W. H. A portable pendulum for testing dynamic tissue failure susceptibility of potatoes J. Agric. Eng. Res. 1985, 32 (3) 269-277
43. Gobom, J.; Schuerenberg, M.; Mueller, M.; Theiss, D.; Lehrach, H.; Nordhoff, E. Alpha-cyano-4-hydroxycinnamic acid affinity sample preparation. A protocol for MALDI-MS peptide analysis in proteomics Anal. Chem. 2001, 73 (3) 434-438
44. Suckau, D.; Resemann, A.; Schuerenberg, M.; Hufnagel, P.; Franzen, J.; Holle, A. A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics Anal. Bioanal. Chem. 2003, 376 (7) 952-965
45. Xu, X.; Pan, S.; Cheng, S.; Zhang, B.; Mu, D.; Ni, P.; Zhang, G.; Yang, S.; Li, R.; Wang, J.; Orjeda, G.; Guzman, F.; Torres, M.; Lozano, R.; Ponce, O.; Martinez, D.; De la Cruz, G.; Chakrabarti, S. K.; Patil, V. U.; Skryabin, K. G.; Kuznetsov, B. B.; Ravin, N. V.; Kolganova, T. V.; Beletsky, A. V.; Mardanov, A. V.; Di Genova, A.; Bolser, D. M.; Martin, D. M.; Li, G.; Yang, Y.; Kuang, H.; Hu, Q.; Xiong, X.; Bishop, G. J.; Sagredo, B.; Mejia, N.; Zagorski, W.; Gromadka, R.; Gawor, J.; Szczesny, P.; Huang, S.; Zhang, Z.; Liang, C.; He, J.; Li, Y.; He, Y.; Xu, J.; Zhang, Y.; Xie, B.; Du, Y.; Qu, D.; Bonierbale, M.; Ghislain, M.; Herrera Mdel, R.; Giuliano, G.; Pietrella, M.; Perrotta, G.; Facella, P.; O'Brien, K.; Feingold, S. E.; Barreiro, L. E.; Massa, G. A.; Diambra, L.; Whitty, B. R.; Vaillancourt, B.; Lin, H.; Massa, A. N.; Geoffroy, M.; Lundback, S.; DellaPenna, D.; Buell, C. R.; Sharma, S. K.; Marshall, D. F.; Waugh, R.; Bryan, G. J.; Destefanis, M.; Nagy, I.; Milbourne, D.; Thomson, S. J.; Fiers, M.; Jacobs, J. M.; Nielsen, K. L.; Sonderkaer, M.; Iovene, M.; Torres, G. A.; Jiang, J.; Veilleux, R. E.; Bachem, C. W.; de Boer, J.; Borm, T.; Kloosterman, B.; van Eck, H.; Datema, E.; Hekkert, B. L.; Goverse, A.; van Ham, R. C.; Visser, R. G. Genome sequence and analysis of the tuber crop potato Nature 2011, 475 (7355) 189-195
46. Smith, A. M.; Denyer, K.; Martin, C. The synthesis of the starch granule Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48 (1) 67-87
47. Bauw, G.; Nielsen, H. V.; Emmersen, J.; Nielsen, K. L.; Jorgensen, M.; Welinder, K. G. Patatins, Kunitz protease inhibitors and other major proteins in tuber of potato cv. Kuras FEBS J. 2006, 273 (15) 3569-3584
48. Welinder, K. G.; Jorgensen, M. Covalent structures of potato tuber lipases (patatins) and implications for vacuolar import J. Biol. Chem. 2009, 284 (15) 9764-9769
49. Jorgensen, M.; Bauw, G.; Welinder, K. G. Molecular properties and activities of tuber proteins from starch potato cv. Kuras J. Agric. Food Chem. 2006, 54 (25) 9389-9397
50. Odeny, D. A.; Stich, B.; Gebhardt, C. Physical organization of mixed protease inhibitor gene clusters, coordinated expression and association with resistance to late blight at the StKI locus on potato chromosome III. Plant Cell Environ. 2010, in press.
51. Wang, F.; Bai, M.-Y.; Deng, Z.; Oses-Prieto, J. A.; Burlingame, A. L.; Lu, T.; Chong, K.; Wang, Z.-Y. Proteomic study identifies proteins involved in brassinosteroid regulation of rice growth J. Integr. Plant Biol. 2010, 52 (12) 1075-1085
52. Garge, N.; Pan, H.; Rowland, M. D.; Cargile, B. J.; Zhang, X.; Cooley, P. C.; Page, G. P.; Bunger, M. K. Identification of quantitative trait loci underlying proteome variation in human lymphoblastoid cells Mol. Cell. Proteomics 2010, 9 (7) 1383-1399
53. Stylianou, I. M.; Affourtit, J. P.; Shockley, K. R.; Wilpan, R. Y.; Abdi, F. A.; Bhardwaj, S.; Rollins, J.; Churchill, G. A.; Paigen, B. Applying gene expression, proteomics and single-nucleotide polymorphism analysis for complex trait gene identification Genetics 2008, 178 (3) 1795-1805
54. Zhao, Y.; Basu, U.; Dodson, M.; Basarb, J.; Guan, L. Proteome differences associated with fat accumulation in bovine subcutaneous adipose tissues Proteome Sci. 2010, 8 (1) 14
55. Skvortsov, S.; Schäfer, G.; Stasyk, T.; Fuchsberger, C.; Bonn, G. K.; Bartsch, G.; Klocker, H.; Huber, L. A. Proteomics profiling of microdissected low- and high-grade prostate tumors identifies lamin A as a discriminatory biomarker J. Proteome Res. 2010, 10 (1) 259-268
56. Kumar, D. M.; Thota, B.; Shinde, S. V.; Prasanna, K. V.; Hegde, A. S.; Arivazhagan, A.; Chandramouli, B. A.; Santosh, V.; Somasundaram, K. Proteomic identification of haptoglobin α2 as a glioblastoma serum biomarker: implications in cancer cell migration and tumor growth J. Proteome Res. 2010, 9 (11) 5557-5567
57. Amon, L. M.; Law, W.; Fitzgibbon, M. P.; Gross, J. A.; O'Briant, K.; Peterson, A.; Drescher, C.; Martin, D. B.; McIntosh, M. Integrative proteomic analysis of serum and peritoneal fluids helps identify proteins that are up-regulated in serum of women with ovarian cancer PLoS ONE 2010, 5 (6) e11137
58. Turra, D.; Bellin, D.; Lorito, M.; Gebhardt, C. Genotype-dependent expression of specific members of potato protease inhibitor gene families in different tissues and in response to wounding and nematode infection J. Plant Physiol. 2009, 166 (7) 762-774
59. Glaczinski, H.; Heibges, A.; Salamini, F.; Gebhardt, C. Members of the Kunitz-type protease inhibitor gene family of potato inhibit soluble tuber invertase in vitro Potato Res. 2002, 45 (2) 163-176
60. Hirschberg, H. J. H. B.; Simons, J.-W. F. A.; Dekker, N.; Egmond, M. R. Cloning, expression, purification and characterization of patatin, a novel phospholipase A Eur. J. Biochem. 2001, 268 (19) 5037-5044
61. Rydel, T. J.; Williams, J. M.; Krieger, E.; Moshiri, F.; Stallings, W. C.; Brown, S. M.; Pershing, J. C.; Purcell, J. P.; Alibhai, M. F. The crystal structure, mutagenesis, and activity studies reveal that patatin is a lipid acyl hydrolase with a Ser-Asp catalytic dyad Biochemistry 2003, 42 (22) 6696-6708
62. Stupar, R. M.; Beaubien, K. A.; Jin, W.; Song, J.; Lee, M.-K.; Wu, C.; Zhang, H.-B.; Han, B.; Jiang, J. Structural diversity and differential transcription of the patatin multicopy gene family during potato tuber development Genetics 2006, 172 (2) 1263-1275
63. Rommens, C. M.; Ye, J.; Richael, C.; Swords, K. Improving potato storage and processing characteristics through all-native DNA transformation J. Agric. Food Chem. 2006, 54 (26) 9882-9887
64. Hunt, M. D.; Eannetta, N. T.; Yu, H.; Newman, S. M.; Steffens, J. C. cDNA cloning and expression of potato polyphenol oxidase Plant Mol. Biol. 1993, 21 (1) 59-68
65. Thygesen, P. W.; Dry, I. B.; Robinson, S. P. Polyphenol oxidase in potato. A multigene family that exhibits differential expression patterns Plant Physiol. 1995, 109 (2) 525-531
66. Seo, Y. S.; Kim, E. Y.; Mang, H. G.; Kim, W. T. Heterologous expression, and biochemical and cellular characterization of CaPLA1 encoding a hot pepper phospholipase A1 homolog Plant J. 2008, 53 (6) 895-908
67. Calvert, C. M.; Gant, S. J.; Bowles, D. J. Tomato annexins p34 and p35 bind to F-actin and display nucleotide phosphodiesterase activity inhibited by phospholipid binding Plant Cell 1996, 8 (2) 333-342