Identification and impact of stable prognostic biochemical markers for cold-induced sweetening resistance on selection efficiency in potato (Solanum tuberosum L.) breeding programs

Autoři: Sanjay K. Gupta aff001;  James Crants aff001
Působiště autorů: University of Minnesota, Department of Soil, Water and Climate, St. Paul, MN, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0225411


Biochemical markers for cold-induced sweetening (CIS) resistance were tested for their stability over years and their use in selection of parents for crossing to achieve high selection efficiency in potato breeding programs.

Two regulatory enzymes directly associated with reducing sugar (RS) accumulation during potato tubers cold storage were tested as a predictor for CIS resistance. These enzymes were studied in 33 potato clones from various breeding programs over four years. Clones with the presence of A-II isozymes of UDP-glucose pyrophosphorylase (UGPase) and low activity of vacuolar acid invertase (VAcInv) enzyme had increased resistance to cold-induced sweetening (CIS). Depending on the levels of these enzymes, clones were divided into class A, class B and class C. Clones categorized as class A had average RS of 0.73 mg per g FW after six months at 5.5°C storage. Class B and C had average RS of 1.15 and 3.80 mg per g FW respectively. The enzyme activity was closely associated with RS accumulation over long-term cold storage.

The biochemical markers were found to be stable over the years. Repeated-measure analysis showed 75% chance of maintaining class from one year to the next and a 25% chance of switching, No clone switched between class A and class C, even across all four years. Application of these biochemical markers can identify clones with CIS resistance early in the selection process. Biochemical markers were used to select parents for crossing and six families were established. Results showed that with both parents from class A, 95% of their offspring had desirable glucose levels and chip color, which dropped to 52% when one parent was from class A and other from class B. These results suggest that two regulatory enzymes, i.e., UGPase and VAcInv, can be used as stable prognostic biochemical markers for CIS resistance for precise parent selection resulting in progenies with significantly higher percentage of clones with acceptable processing quality.

Klíčová slova:

Enzyme inhibitors – Enzyme regulation – Glucose – Potato – Starches – Tubers – Isozymes


1. Knowles NR, Driskill EP, Knowles LO. Sweetening responses of potato tubers of different maturity to conventional and non-conventional storage temperature regimes. Postharvest Biol Technol. 2009;52: 49–61. doi: 10.1016/j.postharvbio.2008.08.015

2. Kyriacou MC, Ioannides IM, Gerasopoulos D, Siomos AS. Storage profiles and processing potential of four potato (Solanum tuberosum L.) cultivars under three storage temperature regimes. J Food Agric Environ. 2009;7: 31–37.

3. Bhaskar PB, Wu L, Busse JS, Whitty BR, Hamernik AJ, Jansky SH, et al. Suppression of the Vacuolar Invertase Gene Prevents Cold-Induced Sweetening in Potato. Plant Physiol. 2010;154: 939–948. doi: 10.1104/pp.110.162545 20736383

4. Sowokinos JR, Hayes RJ, Thill CA. Coordinated Regulation of Cold Induced Sweetening in Tetraploid Potato Families by Isozymes of UDP-Glucose Pyrophosphorylase and Vacuolar Acid Invertase. Am J Potato Res. 2018;95: 487–494.

5. Orawetz T, Malinova I, Orzechowski S, Fettke J. Reduction of the plastidial phosphorylase in potato (Solanum tuberosum L.) reveals impact on storage starch structure during growth at low temperature. Plant Physiol Biochem. 2016;100: 141–149. doi: 10.1016/j.plaphy.2016.01.013 26828405

6. Schreiber L, Nader-Nieto AC, Schönhals EM, Walkemeier B, Gebhardt C. SNPs in genes functional in starch-sugar interconversion associate with natural variation of tuber starch and sugar content of potato (Solanum tuberosum L.). G3 Genes, Genomes, Genet. 2014;4: 1797–1811. doi: 10.1534/g3.114.012377 25081979

7. Xu X, Dees D, Dechesne A, Huang XF, Visser RGF, Trindade LM. Starch phosphorylation plays an important role in starch biosynthesis. Carbohydr Polym. 2017;157: 1628–1637. doi: 10.1016/j.carbpol.2016.11.043 27987877

8. Sowokinos JR. Biochemical and molecular control of cold-induced sweetening in potatoes. Am J Potato Res. 2001;78: 221–236. doi: 10.1007/BF02883548

9. Gupta SK, Sowokinos JR. Physicochemical and kinetic properties of unique isozymes of UDP-Glc pyrophosphorylase that are associated with resistance to sweetening in cold-stored potato tubers. J Plant Physiol. 2003;160: 589–600. doi: 10.1078/0176-1617-01045 12872480

10. McKenzie MJ, Sowokinos JR, Shea IM, Gupta SK, Lindlauf RR, Anderson JAD. Investigations on the role of acid invertase and UDP-glucose pyrophosphorylase in potato clones with varying resistance to cold-induced sweetening. Amer J Potato Res. 2005;82: 231–239. doi: 10.1007/BF02853589

11. Sowokinos JR, Vigdorovich V, Abrahamsen M. Molecular cloning and sequence variation of UDP-glucose pyrophosphorylase cDNAs from potatoes sensitive and resistant to cold sweetening. J Plant Physiol. 2004;161: 947–955. doi: 10.1016/j.jplph.2004.04.006 15384406

12. Sowokinos JR. Allele and isozyme patterns of UDP-glucose pyrophosphorylase as a marker for cold-sweetening resistance in potatoes. Am J Potato Res. 2001;78: 57–64. doi: 10.1007/BF02874825

13. Ciereszko I, Johansson H, Kleczkowski LA. Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Plant Sci. 2001;72: 67–72.

14. Sowokinos JR, Lulai EC, Knoper JA. Tissue Defects in Solanum Translucent. Plant Physiol. 1995;78: 489–494.

15. Sowokinos JR, Shock CC, Stieber TD, Eldredge EP. Compositional and enzymatic changes associated with the sugar-end defect in Russet Burbank potatoes. Am J Potato Res. 2000;77: 47–56. doi: 10.1007/BF02853661

16. Koh EJ, Lee SJ, Hong SW, Lee HS. The ABA effect on the accumulation of an invertase inhibitor transcript that is driven by the CAMV35S promoter in ARABIDOPSIS. Mol Cells. 2008;26: 236–242. 18427162

17. Kingston-Smith AH, Walker RP, Pollock CJ. Invertase in leaves: Conundrum or control point? J Exp Bot. 1999;50: 735–743. doi: 10.1093/jxb/50.335.735

18. Richardson DL, Davies H V, Ross HA, Mackay GR. Invertase activity and its relation to hexose accumulation in potato tubers. J Exp Bot. 1990;41: 95–99. doi: 10.1093/jxb/41.1.95

19. Zrenner R, Schüler K, Sonnewald U. Soluble acid invertase determines the hexose-to-sucrose ratio in cold-stored potato tubers. Planta. 1996;198: 246–52. doi: 10.1007/bf00206250 8580777

20. Matsuura-Endo C, Kobayashi A, Noda T, Takigawa S, Yamauchi H, Mori M. Changes in sugar content and activity of vacuolar acid invertase during low-temperature storage of potato tubers from six Japanese cultivars. J Plant Res. 2004;117: 131–137. doi: 10.1007/s10265-003-0137-z 14986152

21. Bhaskar PB, Wu L, Busse JS, Whitty BR, Hamernik AJ, Jansky SH, et al. Suppression of the Vacuolar Invertase Gene Prevents Cold-Induced Sweetening in Potato. Plant Physiol. 2010;154: 939–948. doi: 10.1104/pp.110.162545 20736383

22. Sin’kevich MS, Sabel’nikova EP, Deryabin AN, Astakhova N V., Dubinina IM, Burakhanova EA, et al. The changes in invertase activity and the content of sugars in the course of adaptation of potato plants to hypothermia. Russ J Plant Physiol. 2008;55: 449–454. doi: 10.1134/S1021443708040031

23. Xu C, Coleman WK, Meng FR, Bonierbale M, Li XQ. Relationship between glucose accumulation and activities of acid invertase and its inhibitors in potatoes under simulated commercial conditions. Potato J. 2009;36: 35–44.

24. Dale MFB, Mackat GR. Inheritane of table and processing quality. Potato Gen. In: Bradshaw JE, Mackay GR, editors. Potato Genetics. Potato Gen. Wallingford, UK: CAB International; 1994. pp. 285–315.

25. Thill CA, Peloquin SJ. A breeding method for accelerated development of cold chipping clones in potato. Euphytica. 1995;84: 73–80. doi: 10.1007/BF01677559

26. Bradshaw J. E. and Mackay GR. Breeding strategies for clonally propagated potatoes. In: Bradshaw JE and GRM, editor. Potato Genetics. Wallingford, UK: CAB International; 1994. pp. 467–497.

27. Oberhagemann P, Chatot-Balandras C, Schafer-Pregl R, Wegener D, Palomino C, Salamini F, et al. A genetic analysis of quantitative resistance to late blight in potato: towards marker-assisted selection. Mol Breed. 1999;5: 399–415. doi: 10.1023/A:1009623212180

28. 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: 93–102. doi: 10.1023/B:MOLB.0000012878.89855.df

29. Slater AT, Cogan NOI, Forster JW. Cost analysis of the application of marker-assisted selection in potato breeding. Mol Breed. 2013;32: 299–310. doi: 10.1007/s11032-013-9871-7

30. Slater AT, Cogan NOI, Rodoni BC, Hayes BJ, Forster JW. Improving the selection efficiency in potato breeding. Acta Hortic. 2016; 237–242. doi: 10.17660/ActaHortic.2016.1127.37

31. Slater AT, Cogan NOI, Hayes BJ, Schultz L, Dale MFB, Bryan GJ, et al. Improving breeding efficiency in potato using molecular and quantitative genetics. Theor Appl Genet. 2014;127: 2279–2292. doi: 10.1007/s00122-014-2386-8 25186170

32. Milczarek D, Flis B, Przetakiewicz A. Suitability of Molecular Markers for Selection of Potatoes Resistant to Globodera spp. Am J Potato Res. 2011;88: 245–255. doi: 10.1007/s11032-013-9871-7

33. Massa AN, Manrique-Carpintero NC, Coombs J, Haynes KG, Bethke PC, Brandt TL, et al. Linkage analysis and QTL mapping in a tetraploid russet mapping population of potato. BMC Genet. 2018;19: 1–13. doi: 10.1186/s12863-017-0594-3

34. Gupta SK. Predictive Markers for Cold-Induced Sweetening Resistance in Cold Stored Potatoes (Solanum tuberosum L.). Am J Potato Res. 2017;94: 297–305. doi: 10.1007/s12230-017-9565-5

35. Pressey R. Role of invertase in the accumulation of sugars in cold-stored potatoes. Am Potato J. 1969;46: 291–297. doi: 10.1007/BF02877144

36. Lindsay H. A colorimetric estimation of reducing sugars in potatoes with 3,5 dinitrosalicylic acid. Potato Res. 1973;16: 176–179.

37. Bradford MM. A Rapid and Sensitive Method for Quantitation of Microgram Quantities of Protein Utilizing Principle of Protein-Dye Binding. Anal Biochem. 1976;72: 248–254. doi: 10.1006/abio.1976.9999 942051

38. Sowokinos JR. Allele and isozyme patterns of UDP-glucose pyrophosphorylase as a marker for cold-sweetening resistance in potatoes. Am J Potato Res. 2001;78: 57–64. doi: 10.1007/BF02874825

39. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227: 680–685. doi: 10.1038/227680a0 5432063

40. Sowokinos R, Spychalla P, Desborough SL. Pyrophosphorylases in Solanum tuberosum’ IV. Purification, Tissue Localization, and Physicochemical Properties of UDP-Glucose Pyrophosphorylase. Plant Physiol. 1993;101: 1073–1080. doi: 10.1104/pp.101.3.1073 12231759

41. Zhu X, Richael C, Chamberlain P, Busse JS, Bussan AJ, Jiang J, et al. Vacuolar invertase gene silencing in potato (Solanum tuberosum L.) improves processing quality by decreasing the frequency of sugar-end defects. PLoS One. 2014;9: e93381. doi: 10.1371/journal.pone.0093381 24695527

42. Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, et al. Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J. 2015; 1–8. doi: 10.1111/pbi.12323

43. Liu X, Zhang C, Ou Y, Lin Y, Song B, Xie C, et al. Systematic analysis of potato acid invertase genes reveals that a cold-responsive member, StvacINV1, regulates cold-induced sweetening of tubers. Mol Genet Genomics. 2011;286: 109–118. doi: 10.1007/s00438-011-0632-1 21691778

44. Liu X, Cheng S, Liu J, Ou Y, Song B, Zhang C, et al. The potato protease inhibitor gene, St-Inh, plays roles in the cold-induced sweetening of potato tubers by modulating invertase activity. Postharvest Biol Technol. 2013;86: 265–271. doi: 10.1016/j.postharvbio.2013.07.001

45. Ou Y, Song B, Liu X, Lin Y, Zhang H, Li M, et al. Profiling of StvacINV1 Expression in Relation to Acid Invertase Activity and Sugar Accumulation in Potato Cold-Stored Tubers. Potato Res. 2013;56: 157–165. doi: 10.1007/s11540-013-9237-x

46. Pressey R, Shaw R. Effect of temperature on invertase, invertase inhibitor, and sugars in potato tubers. Plant Physiol. 1966;41: 1657–1661. doi: 10.1104/pp.41.10.1657 16656454

47. Wu L, Bhaskar PB, Busse JS, Zhang R, Bethke PC, Jiang J. Developing cold-chipping potato varieties by silencing the vacuolar invertase gene. Crop Sci. 2011;51: 981–990. doi: 10.2135/cropsci2010.08.0473

48. McKenzie MJ, Chen RKY, Harris JC, Ashworth MJ, Brummell DA. Post-translational regulation of acid invertase activity by vacuolar invertase inhibitor affects resistance to cold-induced sweetening of potato tubers. Plant, Cell Environ. 2013;36: 176–185. doi: 10.1111/j.1365-3040.2012.02565.x 22734927

49. Lin Y, Liu J, Liu X, Ou Y, Li M, Zhang H, et al. Interaction proteins of invertase and invertase inhibitor in cold-stored potato tubers suggested a protein complex underlying post-translational regulation of invertase. Plant Physiol Biochem. 2013;73: 237–244. doi: 10.1016/j.plaphy.2013.09.012 24161651

50. Liu X, Shi W, Yin W, Wang J. Distinct cold responsiveness of a StInvInh2 gene promoter in transgenic potato tubers with contrasting resistance to cold-induced sweetening. Plant Physiol Biochem. 2017;111: 77–84. doi: 10.1016/j.plaphy.2016.11.021 27915175

51. Pritchard M. K. and Adam I L. R. Relationships between fry color and sugar concentration in stored Russet Burbank and Shepody potatoes. Am Potato J. 1994;71: 59–68.

52. Coleman W. IL1, Tail G. C. C., Clayton S., Howie M. and AP. A portable monitor for the rapid assesment of processing quality of stored potato tubers. Am Potato J. 1993;70: 909–923.

53. Frozen, Potato, Products, Institute. Comments submitted to Docket No. FDA-2009-N-0393: Acrylamide in Food: Request for comments and for scientific data and information. 2009.

54. Zhang H, Liu X, Liu J, Ou Y, Lin Y, Li M, et al. A novel RING finger gene, SbRFP1, increases resistance to cold-induced sweetening of potato tubers. FEBS Lett. 2013;587: 749–755. doi: 10.1016/j.febslet.2013.01.066 23395609

55. Matsuura-Endo C, Kobayashi A, Noda T, Takigawa S, Yamauchi H, Mori M. Changes in sugar content and activity of vacuolar acid invertase during low-temperature storage of potato tubers from six Japanese cultivars. J Plant Res. 2004;117: 131–137. doi: 10.1007/s10265-003-0137-z 14986152

56. Gupta SK, Sowokinos JR, Hahn IS. Regulation of UDP-glucose pyrophosphorylase isozyme UGP5 associated with cold-sweetening resistance in potatoes. J Plant Physiol. 2008;165: 679–690. doi: 10.1016/j.jplph.2007.09.001 17996328

57. Sasaki T, Tadokoro K, Suzuki S. Multiple forms of invertase of potato tuber stored at low temperature. Phytochemistry. 1971;10: 2047–2050. doi: 10.1016/S0031-9422(00)97195-4

58. Chen S, Hajirezaei MR, Zanor MI, Hornyik C, Debast S, Lacomme C, et al. RNA interference-mediated repression of sucrose-phosphatase in transgenic potato tubers (Solanum tuberosum) strongly affects the hexose-to-sucrose ratio upon cold storage with only minor effects on total soluble carbohydrate accumulation. Plant, Cell Environ. 2008;31: 165–176. doi: 10.1111/j.1365-3040.2007.01747.x 17999659

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