Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Translucent tissue defect in potato (Solanum tuberosum L.) tubers is associated with oxidative stress accompanying an accelerated aging phenotype

Abstract

Translucent tissue defect (TTD) is an undesirable postharvest disorder of potato tubers characterized by the development of random pockets of semi-transparent tissue containing high concentrations of reducing sugars. Translucent areas turn dark during frying due to the Maillard reaction. The newly released cultivar, Premier Russet, is highly resistant to low temperature sweetening, but susceptible to TTD. Symptoms appeared as early as 170 days after harvest and worsened with time in storage (4–9 °C, 95 % RH). In addition to higher concentrations of glucose, fructose and sucrose, TTD resulted in lower dry matter, higher specific activities of starch phosphorylase and glc-6-phosphate dehydrogenase, higher protease activity, loss of protein, and increased concentrations of free amino acids (esp. asparagine and glutamine). The mechanism of TTD is unknown; however, the disorder has similarities with the irreversible senescent sweetening that occurs in tubers during long-term storage, where much of the decline in quality is a consequence of progressive increases in oxidative stress with advancing age. The respiration rate of non-TTD ‘Premier Russet’ tubers was inherently higher (ca. 40 %) than that of ‘Russet Burbank’ tubers (a non-TTD cultivar). Moreover, translucent tissue from ‘Premier Russet’ tubers had a 1.9-fold higher respiration rate than the average of non-translucent tissue and tissue from non-TTD tubers. Peroxidation of membrane lipids during TTD development resulted in increased levels of malondialdehyde and likely contributed to a measurable increase in membrane permeability. Superoxide dismutase and catalase activities and the ratio of oxidized to total glutathione were substantially higher in translucent tissue. TTD tubers also contained twofold less ascorbate than non-TTD tubers. TTD appears to be a consequence of oxidative stress associated with accelerated aging of ‘Premier Russet’ tubers.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Abbreviations

6PGDH:

6-Phosphogluconate dehydrogenase

AOX:

Alternate oxidase

AsA:

Ascorbate

BC:

Brown center

CAT:

Catalase

DAH:

Days after harvest

DAP:

Days after planting

DNS:

Dinitrosalicylic acid

Fru:

Fructose

G6PDH:

Glucose-6-phosphate dehydrogenase

Glc:

Glucose

GRase:

Glutathione reductase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

IBS:

Internal brown spot

IHN:

Internal heat necrosis

INH:

Invertase inhibitor (1 and 2)

LOX:

Lipoxygenase

LTS:

Low temperature sweetening

MDA:

Malondialdehyde

NBT:

Nitro-blue tetrazolium

ROS:

Reactive oxygen species

RS:

Reducing sugars

SOD:

Superoxide dismutase

SP:

Starch phosphorylase (L and H)

TBARS:

Thiobarbituric acid-reactive substances

TCA:

Trichloroacetic acid

TEA:

Triethanolamine

TEMED:

Tetramethylethylenediamine

TTD:

Translucent tissue defect

References

  1. Al-Saikhan MS, Howard LR, Miller JC (1995) Antioxidant activity and total phenolics in different genotypes of potato (Solanum tuberosum L.). J Food Sci 60:341–344

  2. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

  3. Amrein TM, Bachmann S, Noti A, Biedermann M, Barbosa MF, Biedermann-Brem S, Grob K, Keiser A, Realini P, Escher F, Amado R (2003) Potential of acrylamide formation, sugars, and free asparagine in potatoes: a comparison of cultivars and farming systems. J Agric Food Chem 51:5556–5560

  4. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

  5. Bergmeyer HU, Bernt E (1974) Sucrose. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie-Academic Press, New York, pp 1176–1179

  6. Bergmeyer HU, Bernt E, Schmidt F, Stork H (1974) Determination with hexokinase and glucose-6-phosphate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie-Academic Press, New York, pp 1196–1201

  7. Bernt E, Bergmeyer HU (1974) d-Fructose. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie-Academic Press, New York, pp 1304–1307

  8. Bethke PC, Zhu X, Wiberley-Bradford AE, Bussan AJ, Jiang J (2013) Cold-induced sweetening, sugar ends, stem-end chip defect and acrylamide can be controlled effectively by silencing of the potato vacuolar invertase gene. In: Proceedings Wisconsin annual potato meetings. p 151

  9. Bilodeau C, Chevrier N (1998) Endogenous ascorbate level modulates ozone tolerance in Euglena gracilis calls. Plant Physiol Biochem 36:695–702

  10. Blauer JM, Knowles LO, Knowles NR (2013a) Evidence that tuber respiration is the pacemaker of physiological aging in seed potatoes (Solanum tuberosum L.). J Plant Growth Regul. doi:10.1007/s00344-013-9338-4

  11. Blauer JM, Kumar GNM, Knowles LO, Dhingra A, Knowles NR (2013b) Changes in ascorbate and associated gene expression during development and storage of potato tubers (Solanum tuberosum L.). Post Biol Tech 78:76–91

  12. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantity of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

  13. Brandt TL, Kleinkopf G, Olsen N, Love S (2003) Storage management for Umatilla Russet potatoes. Bulletin 839, University of Idaho, Moscow

  14. Brummell DA, Chen RKY, Harris JC, Zhang H, Hamiaux C, Kralicek AV, McKenzie MJ (2011) Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J Exp Bot 62:3519–3534

  15. Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Meth In Enzym 2:764–775

  16. Davies HV (1998) Physiological mechanisms associated with the development of internal necrotic disorders of potato. Am J Potato Res 75(1):37–44

  17. Dean BB, Kolattukudy PE, Davis RW (1977) Chemical composition and ultrastucture of suberin from Hollow Heart tissue in potato tubers (Solanum tuberosum L.). Plant Physiol 59:1008–1010

  18. Deplace P, Fauconnier ML, Sergeant K, Dierick JF, Oufir M, van der Wal F, America AH, Renaut J, Hausman JF, du Jardin P (2009) Potato (Solanum tuberosum L.) tuber aging induces changes in the proteome and antioxidants associated with the sprouting pattern. J Exp Bot 60:1273–1288

  19. Dhindsa RS (1982) Inhibition of protein synthesis by products of lipid peroxidation. Phytochem 21:309–313

  20. Driskill EP, Knowles LO, Knowles NR (2007) Temperature-induced changes in potato processing quality during storage are modulated by tuber maturity. Am J Potato Res 84:367–383

  21. Du Z, Bramlage WJ (1992) Modified thiobutyric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J Agric Food Chem 40:1566–1570

  22. Foyer CH, Noctor G (2011) Ascorbate and Glutathione: the Heart of the Redox Hub. Plant Physiol 155:2–18

  23. Hartley DP, Kroll DJ, Petersen DR (1997) Prooxidant-initiated lipid peroxidation in isolated rat hepatocytes: detection of 4-hydroxynonenal- and malondialdehyde-protein adducts. Chem Res Toxicol 10:895–905

  24. Hassel RL, Kelley DM, Wittmeyer EC, Wallace C, Grassbaugh EM, Elliot JY, Wenneker GL (1997) Ohio potato cultivar trials. Ohio State Univ. Horticulture Series No. 666

  25. Jankowski KM, Parkin KL, von Elbe JH (1997) Nonuniform browning or “mottling” in French fry products associated with a heterogeneous distribution of reducing sugars. J Food Process Preserv 21:33–54

  26. Jevremovic S, Petric M, Zivkovic S, Trifunovic M, Subotic A (2010) Superoxide dismutase activity and isoenzyme profiles in bulbs of snake’s head fritillary in response to cold treatment. Arch Biol Sci Belgrade 62:553–558

  27. Kleinkopf GE, Weastermann DT, Wille MJ, Kleinschmidt GD (1987) Specific gravity of Russet Burbank potato. Am Pot J 64:579–587

  28. Knowles NR, Knowles LO (1989) Correlations between electrolyte leakage and degree of saturation of polar lipids from aged potato (Solanum tuberosum L.) tuber tissue. Ann Bot 63:331–338

  29. Knowles LO, Knowles NR (2012) Toxicity and metabolism of exogenous α, β-unsaturated carbonyls in potato (Solanum tuberosum L.) tubers. J Agric Food Chem 60:11173–11181

  30. Knowles NR, Driskill EP, Knowles LO (2009) Sweetening responses of potato tubers of different maturity to conventional and non-conventional storage temperature regimes. Postharvest Biol Technol 52:49–61

  31. Konze JR, Elstner EF (1978) Ethane and ethylene formation by mitochondria as indication of aerobic lipid degradation in response to wounding of plant tissue. Biochim Biophys Acta 528:213–221

  32. Kumar GNM, Knowles NR (1993a) Age of potato seed-tubers influences protein synthesis during sprouting. Physiol Plant 89:262–270

  33. Kumar GNM, Knowles NR (1993b) Changes in lipid peroxidation and lipolytic and free-radical scavenging enzyme activities during aging and sprouting of potato (Solanum tuberosum L.) seed-tubers. Plant Physiol 102:115–124

  34. Kumar GNM, Knowles NR (1996a) Nature of enhanced respiration during sprouting of aged potato seed-tubers. Physiol Plant 97:228–236

  35. Kumar GNM, Knowles NR (1996b) Oxidative stress results in increased sinks for metabolic energy during aging and sprouting of potato seed-tubers. Plant Physiol 112:1301–1313

  36. Kumar GNM, Houtz RL, Knowles NR (1999) Age-induced protein modifications and increased proteolysis in potato seed-tubers. Plant Physiol 119:89–99

  37. Kumar GNM, Knowles LO, Fuller N, Knowles NR (2000) Alpha-1,4 glucan phosphorylase activity correlates with senescent sweetening but not low temperature-induced sweetening in potato. Plant Physiol 123(1):126 (abstract no. 596)

  38. Kumar GNM, Iyer S, Knowles NR (2007) Extraction of RNA from fresh, frozen and lyophilized tuber and root tissues. J Agric Food Chem 55:1674–1678

  39. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

  40. Leshem YY (1987) Membrane phospholipid catabolism and Ca2+ activity control of senescence. Plant Physiol 69:551–559

  41. Liu Y, Wan Q, Wu R, Wang X, Wang H, Shi C, Bi Y (2012) Role of hydrogen peroxide in regulating glucose-6-phosphate dehydrogenase activity under salt stress. Biologia Plant 56:313–320

  42. Liu J, Wang X, Hu Y, Hu W, Bi Y (2013) Glucose-6-phosphate dehydrogenase plays a pivotal role in tolerance to drought stress in soybean root. Plant Cell Rep 32:415–429

  43. Lulai EC, Sowokinos JR, Knoper JA (1986) Translucent tissue defects in Solanum tuberosum L. II. Alterations in lipolytic acyl hydrolase, lypoxygenase, and morphology of mitochondria and amyloplasts. Plant Physiol 80:424–428

  44. Manwaring JD, Csallany AS (1988) Malodialdehyde-containing proteins and their relationship to vitamin E. Lipids 23:651–654

  45. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci 96:8271–8276

  46. Michaud D, Faye L, Yelle S (1993) Electorphoretic analysis of plant cysteine and serine proteinases using gelatin-containing polyacrylamide gels and class specific proteinase inhibitors. Electrophoresis 14:94–98

  47. Michaud D, Nguyen-Quoc B, Bernier-Vadnais N, Faye L, Yelle S (1994) Cysteine proteinase forms in sprouting potato tuber. Physiol Plant 90:497–503

  48. Moller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591

  49. National Agricultural Statistics Service (USDA) (2012) Potatoes 2011 summary: September 2012. ISSN: 1949–1514

  50. Nicot N, Hausman J, Hoffman L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56:2907–2914

  51. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

  52. Novy RG, Whitworth JL, Stark JC, Love SL, Corsini DL, Pavek JJ, Vales MI, James SR, Hane DC, Shock CC, Charlton BA, Brown CR, Knowles NR, Pavek MJ, Brandt TL, Olsen N (2008) Premier Russet: a dual-purpose, potato cultivar with significant resistance to low-temperature sweetening during long-term storage. Am J Potato Res 85:198–209

  53. Pots AM, Gruppen H, van Diepenbeek R, van der Lee JJ, van Boekel MAJS, Wijngaards G, Voragen AGJ (1999) The effect of storage of whole potatoes of three cultivars on the patatin and protease inhibitor content; a study using capillary electrophoresis and MALDI-TOF mass spectrometry. J Sci Food Agric 79:1557–1564

  54. Pouvreau L, Gruppen H, van Koningsveld GA, van der Broek LAM, Voragen AGJ (2003) The most abundant protease inhibitor in potato tuber (cv. Elkana) is a serine protease inhibitor from the Kunitz family. J Agric Food Chem 51:5001–5005

  55. Racusen D (1985) Esterase specificity of patatin from two potato cultivars. Can J Bot 64:2104–2106

  56. Rahnama H, Ebrahimzadeh H (2006) Antioxidant isozymes activities in potato plants (Solanum tuberosum L.) under salt stress. J Sci Islam Rep Iran 17:225–230

  57. Rathore RS, Garg N, Garg S, Kumar A (2009) Starch phosphorylase: role in starch metabolism and biotechnological applications. Crit Rev Biotech 29:214–224

  58. Salin ML (1988) Toxic oxygen species and protective systems of the chloroplast. Physiol Plant 72:681–689

  59. Sowokinos JR(2007) Internal physiological disorders and nutritional and compositional factors that affect market quality. In: Vreugdenhil D (ed), Potato Biology and Biotechnology Advances and Perspectives. Elsevier, Amsterdam, pp 501–523

  60. Sowokinos JR, Lulai EC, Knoper JA (1985) Translucent tissue defects in Solanum tuberosum L. I. alterations in amyloplast membrane integrity, enzyme activities, sugars, and starch content. Plant Physiol 78:489–494

  61. Sowokinos JP, Shock CC, Steiber TD, Eldredge EP (2000) Compositional and enzymatic changes associated with the sugar-end defect in Russet Burbank potatoes. Am J Potato Res 77:47–56

  62. Spychalla JP, Desborough SL (1990) Superoxide dismutase, catalase, and α-tocopherol content of stored potato tubers. Plant Physiol 94:1214–1218

  63. Steup M (1990) Starch degrading enzymes. In: Lea PJ (ed) Methods in Plant Biochemistry, vol 3. Elsevier, Amsterdam, pp 103–128

  64. Steup M, Latzko E (1979) Intracellular localization of phosphorylases in spinach and pea leaves. Planta 145:69–75

  65. Sumner JB (1921) Dinitrosalicylic acid: a reagent for the estimation of sugar in normal and diabetic urine. J Biol Chem 47:5–9

  66. Tanaka K, Sano T, Ishizuka K, Kitta K, Kawamura Y (1994) Comparison of properties of leaf and root glutathione reductases from spinach. Physiol Plant 91:353–358

  67. Tiwari R, Kumar A (2012) Starch phosphorylase: biochemical and biotechnological perspectives. Bio Mol Bio Rev 7:69–83

  68. von Schaewen A, Langenkamper G, Graeve K, Wenderoth I, Scheibe R (1995) Molecular characterization of the plastidic glucose-6-phosphate dehydrogenase from potato in comparison to its cytosolic counterpart. Plant Physiol 109:1327–1335

  69. Wagner AM, Krab K (1995) The alternative respiration pathway in plants: role and regulation. Physiol Plant 95:318–325

  70. Walsh TA, Strickland JA (1993) Proteolysis of the 85-kilodalton crystalline cysteine proteinase inhibitor from potato releases functional cystatin domains. Plant Physiol 103:1227–1234

  71. Weeda SM, Kumar GNM, Knowles NR (2009) Developmentally linked changes in proteases and protease inhibitors suggest a role for potato multicystatin in regulating protein content of potato tubers. Planta 230:73–84

  72. Weeda SM, Kumar GNM, Knowles NR (2011) Protein mobilization from potato tubers during long-term storage and daughter tuber formation. Int J Plant Sci 172:459–470

  73. Yencho GC, McCord PH, Haynes KG, Sterrett SB (2008) Internal heat necrosis—a review. Am J Potato Res 85:69–76

  74. Zabrouskov V, Kumar GNM, Spychalla JP, Knowles NR (2002) Oxidative metabolism and the physiological age of seed potatoes are affected by increased α-linolenate content. Phys Plant 116:172–185

  75. Zeeman SC, Smith SM, Smith AM (2004) The breakdown of starch in leaves. New Phytol 163:247–261

  76. Zhao J, Williams CC, Last RL (1998) Induction of Arabidopsis tryptophan pathway enzymes and camalexin by amino acid starvation, oxidative stress, and abiotic elicitor. Plant Cell 10:359

  77. Zommick DH, Knowles LO, Kumar GNM, Knowles NR (2012) In-season heat stress compromises postharvest quality and low temperature sweetening resistance in potato (Solanum tuberosum L.). Am J Potato Res 90:156

Download references

Acknowledgments

Financial support from the USDA/ARS, Washington State Potato Commission, WSU Agricultural Research Center and WSU Department of Horticulture is gratefully acknowledged. We thank Dr. Sanjay Gupta, University of Minnesota, for providing the invertase activity protocol.

Author information

Correspondence to N. Richard Knowles.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Zommick, D.H., Kumar, G.N.M., Knowles, L.O. et al. Translucent tissue defect in potato (Solanum tuberosum L.) tubers is associated with oxidative stress accompanying an accelerated aging phenotype. Planta 238, 1125–1145 (2013). https://doi.org/10.1007/s00425-013-1951-8

Download citation

Keywords

  • Aging
  • Mottling
  • Oxidative metabolism
  • Physiological disorder
  • Postharvest
  • Respiration
  • Senescent sweetening
  • Storage