Effects of high temperature on in vitro tuberization and accumulation of stress-responsive proteins in potato

  • Danijel Pantelić
  • Ivana Č. Dragićević
  • Jelena Rudić
  • Jianming Fu
  • Ivana Momčilović
Research Report Cultivation Physiology
  • 26 Downloads

Abstract

Potato (Solanum tuberosum L.) plants are highly vulnerable to heat stress. Even moderately elevated temperatures can disturb the process of tuberization in this important crop, causing a decline in tuber initiation, a reduction in tuber bulking, and tuber disorders. In the present study, we investigated the effects of heat stress on tuberization in two potato cultivars, the heat-sensitive cultivar Désirée and the heat-tolerant cultivar Festival, using an in vitro system. A temperature of 29 °C reduced tuber initiation and tuber bulking, and stimulated shoot elongation in cv. Désirée, while this temperature treatment did not significantly alter tuberization or shoot elongation in cv. Festival. In addition, high temperature interfered with the onset of microtuber dormancy and promoted growth of tuber apical buds during the tuber bulking stage in both cultivars. Stress-responsive proteins HSP17.6-CI, HSP101, and eEF1A showed heat-induced accumulation patterns in shoots and microtubers of these two cultivars, with the exception of a decline in the abundance of eEF1A in cv. Désirée microtubers under heat stress. High levels of HSP17.6-CI in microtubers of cv. Désirée did not ameliorate the effects of heat stress on tuberization of this relatively heat-sensitive cultivar. Conversely, a higher level of eEF1A under heat stress in microtubers of the heat-tolerant cv. Festival indicated a possible function of this protein in alleviating the negative effects of high temperature on potato tuberization. This study suggested that analysis of stress-responsive proteins in potato microtubers combined with assessment of tuberization parameters in vitro may represent a useful screening procedure for selection of heat-tolerant potato genotypes.

Keywords

Heat stress Heat tolerance Solanum tuberosum HSP Eukaryotic elongation factor 1A 

Notes

Acknowledgements

This study was funded by the Ministry of Education, Science and Technological Development of the Republic of Serbia, Project Grant No. TR31049.

References

  1. Ahn YJ, Zimmerman JL (2006) Introduction of the carrot HSP17.7 into potato (Solanum tuberosum L.) enhances cellular membrane stability and tuberization in vitro. Plant Cell Environ 29:95–104CrossRefPubMedGoogle Scholar
  2. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  3. Bukovnik U, Fu J, Bennett M, Prasad PVV, Ristić Z (2009) Heat tolerance and expression of protein synthesis elongation factors, EF-Tu and EF-1α, in spring wheat. Funct Plant Biol 36:234–241CrossRefGoogle Scholar
  4. Delaplace P, Fauconnier ML, Sergeant K, Dierick JF, Oufir M, van der Wal F, America AHP, Renaut J, Hausman JF, du Jardin P (2009) Potato (Solanum tuberosum L.) tuber ageing induces changes in the proteome and antioxidants associated with the sprouting pattern. J Exp Bot 60:1273–1288CrossRefPubMedPubMedCentralGoogle Scholar
  5. Doyle SM, Genest O, Wickner S (2013) Protein rescue from aggregates by powerful molecular chaperone machines. Nat Rev Mol Cell Biol 14:617–629CrossRefPubMedGoogle Scholar
  6. Dragićević I, Konjević R, Vinterhalter B, Vinterhalter D, Nešković M (2008) The effects of IAA and tetcyclacis on tuberization in potato (Solanum tuberosum L.) shoot cultures in vitro. Plant Growth Regul 54:189–193CrossRefGoogle Scholar
  7. FAO (2015) Statistical pocketbook: World Food and Agriculture. Food and Agriculture Organization of the United Nations, Rome, Italy. http://www.fao.org/3/a-i4691e.pdf. Accessed 07 Sept 2017
  8. Friedrich KL, Giese KC, Buan NR, Vierling E (2004) Interactions between small heat shock protein subunits and substrate in small heat shock protein-substrate complexes. J Biol Chem 279:1080–1089CrossRefPubMedGoogle Scholar
  9. Gangadhar BH, Yu JW, Sajeesh K, Park SW (2014) A systematic exploration of high-temperature stress-responsive genes in potato using large-scale yeast functional screening. Mol Genet Genomics 289:185–201CrossRefPubMedGoogle Scholar
  10. Garner N, Blake J (1989) The induction and development of potato microtubers in vitro on media free of growth regulating substances. Ann Bot 63:663–674CrossRefGoogle Scholar
  11. Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94:73–82CrossRefPubMedGoogle Scholar
  12. Gopal J, Minocha JL (1998) Effectiveness of in vitro selection for agronomic characters in potato. Euphytica 103:67–74CrossRefGoogle Scholar
  13. Hancock RD, Morris WL, Ducreux LJM, Morris JA, Usman M, Verrall SR, Fuller J, Simpson CG, Zhang R, Hedley PE, Taylor MA (2014) Physiological, biochemical and molecular responses of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ 37:439–450CrossRefPubMedGoogle Scholar
  14. Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci 97:4392–4397CrossRefPubMedPubMedCentralGoogle Scholar
  15. Khan MA, Munive S, Bonierbale M (2015) Early generation in vitro assay to identify potato populations and clones tolerant to heat. Plant Cell Tiss Organ Cult 121:45–52CrossRefGoogle Scholar
  16. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  17. Lee GJ, Pokala N, Vierling E (1995) Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J Biol Chem 270:10432–10438CrossRefPubMedGoogle Scholar
  18. Lehesranta SJ, Koistinen KM, Massat N, Davies HV, Shepherd LVT, McNicol JW, Cakmak I, Cooper J, Lück L, Kärenlampi SO, Leifert C (2007) Effects of agricultural production systems and their components on protein profiles of potato tubers. Proteomics 7:597–604CrossRefPubMedGoogle Scholar
  19. Levy D, Veilleux RE (2007) Adaptation of potato to high temperatures and salinity—a review. Am J Potato Res 84:487–506CrossRefGoogle Scholar
  20. Linsmaier EM, Skoog F (1965) Organic growth factor requirement for tobacco tissue cultures. Physiol Plant 18:100–127CrossRefGoogle Scholar
  21. Lubaretz O, zur Nieden U (2002) Accumulation of plant small heat-stress proteins in storage organs. Planta 215:220–228CrossRefPubMedGoogle Scholar
  22. Malik MK, Slovin JP, Hwang CH, Zimmerman JL (1999) Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance. Plant J 20:89–99CrossRefPubMedGoogle Scholar
  23. Manrique LA (1992) Potato production in the tropics: crop requirements. J Plant Nutr 15:2679–2726CrossRefGoogle Scholar
  24. Momčilović I, Ristić Z (2007) Expression of chloroplast protein synthesis elongation factor, EF-Tu, in two lines of maize with contrasting tolerance to heat stress during early stages of plant development. J Plant Physiol 164:90–99CrossRefPubMedGoogle Scholar
  25. Momčilović I, Pantelić D, Hfidan M, Savić J, Vinterhalter D (2014) Improved procedure for detection of superoxide dismutase isoforms in potato, Solanum tuberosum L. Acta Physiol Plant 36:2059–2066CrossRefGoogle Scholar
  26. Momčilović I, Pantelić D, Zdravković-Korać S, Oljača J, Rudić J, Fu J (2016) Heat-induced accumulation of protein synthesis elongation factor 1A implies an important role in heat tolerance in potato. Planta 244:671–679CrossRefPubMedGoogle Scholar
  27. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15:473–497CrossRefGoogle Scholar
  28. Nakamoto H, Vígh L (2007) The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–306CrossRefPubMedGoogle Scholar
  29. Nowak J, Colborne D (1989) In vitro tuberization and tuber proteins as indicators of heat stress tolerance in potato. Am Potato J 66:35–45CrossRefGoogle Scholar
  30. Struik PC (2007) Responses of the potato plant to temperature. In: Vreugdenhil D, Bradshaw J, Gebhardt C, Govers F, MacKerron DKL, Taylor MA, Ross HA (eds) Potato biology and biotechnology: advances and perspectives. Elsevier, Amsterdam, pp 367–393CrossRefGoogle Scholar
  31. Vettermann C, Jäck HM, Mielenz D (2002) A colloidal silver staining-destaining method for precise assignment of immunoreactive spots in two-dimensional protein patterns. Anal Biochem 308:381–387CrossRefPubMedGoogle Scholar
  32. Vreugdenhil D, Boogaard Y, Visser RGF, de Bruijn SM (1998) Comparison of tuber and shoot formation from in vitro cultured potato explants. Plant Cell Tiss Organ Cult 53:197–204CrossRefGoogle Scholar
  33. Wang D, Luthe DS (2003) Heat sensitivity in a bentgrass variant. Failure to accumulate a chloroplast heat shock protein isoform implicated in heat tolerance. Plant Physiol 133:319–327CrossRefPubMedPubMedCentralGoogle Scholar
  34. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252CrossRefPubMedGoogle Scholar
  35. Wiltshire JJJ, Cobb AH (1996) A review of the physiology of potato tuber dormancy. Ann Appl Biol 129:553–569CrossRefGoogle Scholar
  36. Xu X, van Lammeren AAM, Vermeer E, Vreugdenhil D (1998a) The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Phys 117:575–584CrossRefGoogle Scholar
  37. Xu X, Vreugdenhil D, van Lammeren AAM (1998b) Cell division and cell enlargement during potato tuber formation. J Exp Bot 49:573–582CrossRefGoogle Scholar

Copyright information

© Korean Society for Horticultural Science and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Danijel Pantelić
    • 1
  • Ivana Č. Dragićević
    • 2
  • Jelena Rudić
    • 2
    • 4
  • Jianming Fu
    • 3
  • Ivana Momčilović
    • 1
  1. 1.Institute for Biological Research “Siniša Stanković”University of BelgradeBelgradeSerbia
  2. 2.Faculty of BiologyUniversity of BelgradeBelgradeSerbia
  3. 3.Department of AgronomyKansas State UniversityManhattanUSA
  4. 4.Institute for Biological Research “Siniša Stanković”University of BelgradeBelgradeSerbia

Personalised recommendations