Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

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 via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

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

  • 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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

  • 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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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)

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

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

Authors and Affiliations

  1. Postharvest Physiology and Biochemistry Laboratory, Department of Horticulture, Washington State University, P.O. Box 646414, Pullman, WA, 99164-6414, USA

    Daniel H. Zommick, G. N. Mohan Kumar, Lisa O. Knowles & N. Richard Knowles

Authors
  1. Daniel H. Zommick
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. N. Mohan Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lisa O. Knowles
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Richard Knowles
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

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

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-1951-8

Keywords

Search

Navigation