Skip to main content
Log in

Gene expression profiles predictive of cold-induced sweetening in potato

  • Original Article
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Cold storage (2–4 °C) used in potato production to suppress diseases and sprouting during storage can result in cold-induced sweetening (CIS), where reducing sugars accumulate in tuber tissue leading to undesirable browning, production of bitter flavors, and increased levels of acrylamide with frying. Potato exhibits genetic and environmental variation in resistance to CIS. The current study profiles gene expression in post-harvest tubers before cold storage using transcriptome sequencing and identifies genes whose expression is predictive for CIS. A distance matrix for potato clones based on glucose levels after cold storage was constructed and compared to distance matrices constructed using RNA-seq gene expression data. Congruence between glucose and gene expression distance matrices was tested for each gene. Correlation between glucose and gene expression was also tested. Seventy-three genes were found that had significant p values in the congruence and correlation tests. Twelve genes from the list of 73 genes also had a high correlation between glucose and gene expression as measured by Nanostring nCounter. The gene annotations indicated functions in protein degradation, nematode resistance, auxin transport, and gibberellin response. These 12 genes were used to build models for prediction of CIS using multiple linear regression. Nine linear models were constructed that used different combinations of the 12 genes. An F-box protein, cellulose synthase, and a putative Lax auxin transporter gene were most frequently used. The findings of this study demonstrate the utility of gene expression profiles in predictive diagnostics for severity of CIS.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • AAFC (2015) Potato Market Information Review. In: Market Analysis and Information Section HaCSD, Agriculture and Agri-Food Canada (ed) Ottawa, ON

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  CAS  PubMed  Google Scholar 

  • Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor–dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexa A, Rahnenfuhrer J (2010) topGO: enrichment analysis for gene ontology. R package version 2

  • Bagnaresi P, Moschella A, Beretta O, Vitulli F, Ranalli P, Perata P (2008) Heterologous microarray experiments allow the identification of the early events associated with potato tuber cold sweetening. BMC Genomics 9:176. doi: 10.1186/1471-2164-9-176

  • Bailey K, Phillips I, Pitt D (1978) The role of buds and gibberellin in dormancy and the mobilization of reserve materials in potato tubers. Ann Bot 42:649–657

    Article  CAS  Google Scholar 

  • Bhaskar P, Wu L, Busse J, Whitty B, Hamernik A, Jansky S, Buell C, Bethke P, Jiang J (2010) Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiol 154:939–948

  • Bradshaw J, Hackett C, Pande B, Waugh R, Bryan G (2008) QTL mapping of yield, agronomic and quality traits in tetraploid potato (Solanum tuberosum subsp. tuberosum). Theor Appl Genet 116:193–211

    Article  PubMed  Google Scholar 

  • Brandt T, Woodell L, Olsen N (2012) Glucose concentrations: storing for multiple use. Potato grower. Harris Publishing, Inc Idaho Falls, ID, pp. 30–34

  • Campbell V, Legendre P, Lapointe F-J (2011) The performance of the Congruence Among Distance Matrices (CADM) test in phylogenetic analysis. BMC Evol Biol 11:1–15. doi:10.1186/1471-2148-11-64

    Article  Google Scholar 

  • Chen X, Song B, Liu J, Yang J, He T, Lin Y, Zhang H, Xie C (2012) Modulation of gene expression in cold-induced sweetening resistant potato species Solanum berthaultii exposed to low temperature. Mol Gen Genomics 287:411–421

    Article  CAS  Google Scholar 

  • Cheng H, Qin L, Lee S, Fu X, Richards D, Cao D, Luo D, Harberd N, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064

    Article  CAS  PubMed  Google Scholar 

  • Clegg M, Rappaport L (1970) Regulation of bud rest in tubers of potato, Solanum tuberosum L VI. Biochemical changes induced in excised potato buds by gibberellic acid. Plant Physiol 45:8–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Datir S, Latimer J, Thomson S, Ridgway H, Conner A, Jacobs J (2012) Allele diversity for the apoplastic invertase inhibitor gene from potato. Mol Gen Genomics 287:451–460

    Article  CAS  Google Scholar 

  • Davies H, Viola R (1988) The effect of gibberellic acid on starch breakdown in sprouting tubers of Solanum tuberosum L. Ann Bot 61:689–693

    Article  CAS  Google Scholar 

  • Driskill E, Knowles L, Knowles N (2007) Temperature-induced changes in potato processing quality during storage are modulated by tuber maturity. Am J Potato Res 84:367–383

  • Drouin G, Dover G (1990) Independent gene evolution in the potato actin gene family demonstrated by phylogenetic procedures for resolving gene conversions and the phylogeny of angiosperm actin genes. J Mol Evol 31:132–150

    Article  CAS  PubMed  Google Scholar 

  • Duffy MJ, O'Donovan N, McDermott E, Crown J (2016) Validated biomarkers: the key to precision treatment in patients with breast cancer. Breast. doi:10.1016/j.breast.2016.07.009

    PubMed  Google Scholar 

  • Fernandez-Pozo N, Menda N, Edwards J, Saha S, Tecle I, Strickler S, Bombarely A, Fisher-York T, Pujar A, Foerster H (2015) The Sol Genomics Network (SGN)—from genotype to phenotype to breeding. Nucleic Acids Res 43:D1036–D1041

    Article  PubMed  Google Scholar 

  • Fischer M, Schreiber L, Colby T, Kuckenberg M, Tacke E, Hofferbert H-R, Schmidt J, Gebhardt C (2013) Novel candidate genes influencing natural variation in potato tuber cold sweetening identified by comparative proteomics and association mapping. BMC Plant Biol 13:1–15

    Article  Google Scholar 

  • Gálvez J, Tai H, Lagüe M, Zebarth B, Strömvik M (2016) The nitrogen responsive transcriptome in potato (Solanum tuberosum L.) reveals significant gene regulatory motifs. Sci Rep 6:26090

    Article  PubMed  PubMed Central  Google Scholar 

  • Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26:317–325

    Article  CAS  PubMed  Google Scholar 

  • Harris P (1978) Water. In: Harris PM (ed) The potato crop: the scientific basis for improvement. Springer Dordrecht, pp. 245–278

  • Hartmann A, Senning M, Hedden P, Sonnewald U, Sonnewald S (2011) Reactivation of meristem activity and sprout growth in potato tubers require both cytokinin and gibberellin. Plant Physiol 155:776–796

    Article  CAS  PubMed  Google Scholar 

  • Hertog M, Tijskens L, Hak P (1997) The effects of temperature and senescence on the accumulation of reducing sugars during storage of potato (Solanum tuberosum L.) tubers: a mathematical model. Postharvest Biol Technol 10:67–79

    Article  CAS  Google Scholar 

  • Hogervorst J, Baars B-J, Schouten L, Konings E, Goldbohm R, van den Brandt P (2010) The carcinogenicity of dietary acrylamide intake: a comparative discussion of epidemiological and experimental animal research. Crit Rev Toxicol 40:485–512

    Article  CAS  PubMed  Google Scholar 

  • Joazeiro C, Weissman A (2000) RING finger proteins: mediators of ubiquitin ligase activity. Cell 102:549–552

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:1

    Article  Google Scholar 

  • Knowles N, Driskill E Jr, Knowles L (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 

  • Kolbe H, Stephan-Beckmann S (1997) Development, growth and chemical composition of the potato crop (Solanum tuberosum L.). II. Tuber and whole plant. Potato Res 40:135–153

    Article  CAS  Google Scholar 

  • Krauss A, Marschner H (1982) Influence of nitrogen nutrition, daylength and temperature on contents of gibberellic and abscisic acid and on tuberization in potato plants. Potato Res 25:13–21

    Article  CAS  Google Scholar 

  • Kumar D, Singh B, Kumar P (2004) An overview of the factors affecting sugar content of potatoes. Ann Appl Biol 145:247–256

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Cheng H, King K, Wang W, He Y, Hussain A, Lo J, Harberd N, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Paulo M-J, Strahwald J, Lübeck J, Hofferbert H-R, Tacke E, Junghans H, Wunder J, Draffehn A, van Eeuwijk F (2008) Natural DNA variation at candidate loci is associated with potato chip color, tuber starch content, yield and starch yield. Theor Appl Genet 116:1167–1181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:1007–1016

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Cheng S, Liu J, Ou Y, Song B, Zhang C, Lin Y, Li X-Q, Xie C (2013) The potato protease inhibitor gene, St-Inh, plays roles in the cold-induced sweetening of potato tubers by modulating invertase activity. Postharvest Biol Technol 86:265–271

    Article  CAS  Google Scholar 

  • Maillard L (1912) Action of amino acids on sugars. Formation of melanoidins in a methodical way. Compt Rend 154:66

    CAS  Google Scholar 

  • Martínez-García F, García-Martínez L, Bou J, Prat S (2001) The interaction of gibberellins and photoperiod in the control of potato tuberization. J Plant Growth Regul 20:377–386

    Article  PubMed  Google Scholar 

  • Mathis L, Voytas D, Zhang F, Clasen B, Haun W, Stoddard T (2014) Potatoes with reduced cold-induced sweetening Google Patents

  • McKenzie M, Sowokinos J, Shea I, Gupta S, Lindlauf R, Anderson J (2005) Investigations on the role of acid invertase and UDP-glucose pyrophosphorylase in potato clones with varying resistance to cold-induced sweetening. Am J Potato Res 82:231–239

    Article  CAS  Google Scholar 

  • McKenzie M, Chen R, Harris J, Ashworth M, Brummell D (2013) Post-translational regulation of acid invertase activity by vacuolar invertase inhibitor affects resistance to cold-induced sweetening of potato tubers. Plant Cell Environ 36:176–185

  • Menendez CM, Ritter E, Schäfer-Pregl R, Walkemeier B, Kalde A, Salamini F, Gebhardt C (2002) Cold sweetening in diploid potato: mapping quantitative trait loci and candidate genes. Genetics 162:1423–1434

  • Menzel C (1980) Tuberization in potato at high temperatures: responses to gibberellin and growth inhibitors. Ann Bot 46:259–265

    Article  CAS  Google Scholar 

  • Metzger M, Hristova V, Weissman A (2012) HECT and RING finger families of E3 ubiquitin ligases at a glance. J Cell Sci 125:531–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mottram D, Wedzicha B, Dodson A (2002) Food chemistry: acrylamide is formed in the Maillard reaction. Nature 419:448–449

    Article  CAS  PubMed  Google Scholar 

  • Nakane E, Kawakita K, Doke N, Yoshioka H (2003) Elicitation of primary and secondary metabolism during defense in the potato. J Gen Plant Pathol 69:378–384

    Article  CAS  Google Scholar 

  • NASS-USDA (2014) Potatoes 2014 Summary. In: Agriculture NASSaUSDo (ed) Washinton, DC

  • Neubauer J, Lulai E, Thompson A, Suttle J, Bolton M, Campbell L (2013) Molecular and cytological aspects of native periderm maturation in potato tubers. J Plant Physiol 170:413–423

    Article  CAS  PubMed  Google Scholar 

  • Nicot N, Hausman J-F, Hoffmann 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  CAS  PubMed  Google Scholar 

  • Parry G, Estelle M (2006) Auxin receptors: a new role for F-box proteins. Curr Opin Cell Biol 18:152–156

    Article  CAS  PubMed  Google Scholar 

  • Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195

    Article  Google Scholar 

  • Quinones V, Zanlungo S, Holuigue L, Litvak S, Jordana X (1995) The cox1 initiation codon is created by RNA editing in potato mitochondria. Plant Physiol 108:1327–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2015. www.R-project.org

  • Reeve R, Timm H, Weaver M (1973) Cell wall thickness during growth of domestic and foreign potato cultivars. Am Potato J 50:204–211

    Article  Google Scholar 

  • Rentzsch S, Podzimska D, Voegele A, Imbeck M, Müller K, Linkies A, Leubner-Metzger G (2012) Dose-and tissue-specific interaction of monoterpenes with the gibberellin-mediated release of potato tuber bud dormancy, sprout growth and induction of α-amylases and β-amylases. Planta 235:137–151

    Article  CAS  PubMed  Google Scholar 

  • Roumeliotis E, Visser R, Bachem C (2012) A crosstalk of auxin and GA during tuber development. Plant Signal Behav 7:1360–1363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shallenberger R, Smith O, Treadway R (1959) Food color changes, role of the sugars in the browning reaction in potato chips. J Agric Food Chem 7:274–277

    Article  CAS  Google Scholar 

  • Sharma V, Singh B, Raigond P, Kaushik S (2016) Role of invertase activity in processing quality of potatoes: effect of storage temperature and duration. J Environ Biol 37:239

    Article  PubMed  Google Scholar 

  • Skaar JR, Pagan JK, Pagano M (2013) Mechanisms and function of substrate recruitment by F-box proteins. Nat Rev Mol Cell Biol 14:369–381

    Article  CAS  PubMed  Google Scholar 

  • Sołtys-Kalina D, Szajko K, Sierocka I, Śliwka J, Strzelczyk-Żyta D, Wasilewicz-Flis I, Jakuczun H, Szweykowska-Kulinska Z, Marczewski W (2015) Novel candidate genes AuxRP and Hsp90 influence the chip color of potato tubers. Mol Breeding 35:1–12

    Article  Google Scholar 

  • Sowokinos JR (2001) Biochemical and molecular control of cold-induced sweetening in potatoes. Am J Potato Res 78:221–236

    Article  CAS  Google Scholar 

  • Sun T (2011) The molecular mechanism and evolution of the GA–GID1–DELLA signaling module in plants. Curr Biol 21:R338–R345

    Article  CAS  PubMed  Google Scholar 

  • Tai H, Conn G, Davidson C (2009) Arbitrary multi-gene reference for normalization of real-time PCR gene expression data. Plant Mol Biol Report 27:315–320

    Article  CAS  Google Scholar 

  • Tai H, Goyer C, Platt H, De Koeyer D, Murphy A, Uribe P, Halterman D (2013) Decreased defense gene expression in tolerance versus resistance to Verticillium dahliae in potato. Funct Integr Genomics 13:367–378

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Calderon-Villalobos L, Sharon M, Zheng C, Robinson C, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    Article  CAS  PubMed  Google Scholar 

  • Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyler L, Thomas S, Hu J, Dill A, Alonso J, Ecker J, T-p S (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vreugdenhil D, Sergeeva L (1999) Gibberellins and tuberization in potato. Pot Res 42:471–481

    Article  CAS  Google Scholar 

  • Wiberley-Bradford A, Busse J, Jiang J, Bethke P (2014) Sugar metabolism, chip color, invertase activity, and gene expression during long-term cold storage of potato (Solanum tuberosum) tubers from wild-type and vacuolar invertase silencing lines of Katahdin. BMC Res Notes 7:801

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiberley-Bradford A, Busse J, Bethke P (2016) Temperature-dependent regulation of sugar metabolism in wild-type and low-invertase transgenic chipping potatoes during and after cooling for low-temperature storage. Postharvest Biol Technol 115:60–71

    Article  CAS  Google Scholar 

  • Xu X, van Lammeren A, Vermeer E, Vreugdenhil D (1998) The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiol 117:575–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu C, Coleman W, Meng F-R, Bonierbale M, Li X-Q (2009) Relationship between glucose accumulation and activities of acid invertase and its inhibitors in potatoes under simulated commercial conditions. Pot J 36:35–44

  • Zhang H, Liu X, Liu J, Ou Y, Lin Y, Li M, Song B, Xie C (2013) A novel RING finger gene, SbRFP1, increases resistance to cold-induced sweetening of potato tubers. FEBS Lett 587:749–755

    Article  CAS  PubMed  Google Scholar 

  • Zommick D, Knowles L, Pavek M, Knowles N (2014) In-season heat stress compromises postharvest quality and low-temperature sweetening resistance in potato (Solanum tuberosum L.). Planta 239:1243–1263

    Article  CAS  PubMed  Google Scholar 

  • Zrenner R, Schuler K, Sonnewald U (1996) Soluble acid invertase determines the hexose-to-sucrose ratio in cold-stored potato tubers. Planta 198:246–252. DOI 10.1007/bf00206250

Download references

Acknowledgements

This work was supported by the Agricultural Innovation Program funding from AgricTulture and Agri-Food Canada and Sipre. The authors also acknowledge Plant & Food Research for funding. Charlotte Davidson, Lana Nolan, Katrina Monaghan, and Kathryn Wright contributed technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathan Neilson.

Electronic supplementary material

Table S1

(XLSX 15 kb)

Table S2

(XLSX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Neilson, J., Lagüe, M., Thomson, S. et al. Gene expression profiles predictive of cold-induced sweetening in potato. Funct Integr Genomics 17, 459–476 (2017). https://doi.org/10.1007/s10142-017-0549-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-017-0549-9

Keywords

Navigation