, Volume 249, Issue 5, pp 1379–1390 | Cite as

Comparative physiological and metabolomic analyses reveal natural variations of tulip in response to storage temperatures

  • Yanping Wang
  • Huimin Zhao
  • Yaping Wang
  • Siyuan Yu
  • Yuchao Zheng
  • Wen’en Wang
  • Zhulong ChanEmail author
Original Article


Main conclusion

Three tulip cultivars were screened out with successful bloom after a short-term cold treatment, and the differential responses to postharvest cold treatment were analyzed between two contrasting tulip cultivars.

Tulip is one of the most important ornamental bulbous plants in the world. A precious precooling treatment during bulb postharvest is required for optimal floral stalk elongation and flower development in tulip. In this study, the naturally growing and flowering variations of tulip to storage temperatures were analyzed after long-term cold (LTC) and short-term cold (STC) treatments. Three cultivars were screened out with successful blooming after STC, which included ‘Dow Jones’ (DJ), ‘Van Eijk’ (VE) and ‘World’s Favourite’ (WF) (5 °C for 2 weeks). Comparative analysis revealed that DJ cultivar maintained normal and intact reproductive organs under STC condition, while the ‘Orange Emperor’ (OE) cultivar, which failed blooming after STC treatment, showed gradually destroyed reproductive organs under STC condition. In addition, the DJ cultivar accumulated lower ROS levels and higher antioxidant enzyme activities, as well as significantly higher contents of total primary metabolites than OE to maintain normal shoot growth and floral organ development under STC condition. The relative expression levels of genes involved in vernalization and/or flower time regulation in DJ were significantly higher than those in OE after STC treatment. This study provides new insights into understanding the underlying mechanism of natural variation of tulip cultivars during postharvest storage treatment.


Cold response Floral stalk elongation Flowering Metabolic profiling Natural variation Storage temperature 



Tulip cv. Dow Jones


Flowering Locus K homology domain


Long-term cold treatment


Tulip vc. Orange Emperor


Short-term cold treatment









This research was supported by Huazhong Agricultural University Scientific and Technological Self-innovation Foundation (Program nos. 2016QD026 and 2016RC010) and Project 2662018PY069 supported by the Fundamental Research Funds for the Central Universities. We thank Professor Jihong Liu (Huazhong Agricultural University) for kindly sharing qRT-PCR instrument. We appreciate the editor and reviewers for their comments and suggestions.

Compliance with ethical standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary material

425_2018_3072_MOESM1_ESM.docx (5.5 mb)
Supplementary material 1 (DOCX 5607 kb)


  1. Alexandre CM, Hennig L (2008) FLC or not FLC: the other side of vernalization. J Exp Bot 59: 1127–1135CrossRefGoogle Scholar
  2. Aung LH (1979) Temperature regulation of growth and endogenous abscisic acid-like content of Tulipa gesneriana L. Plant Physiol 63:1111–1116CrossRefGoogle Scholar
  3. Aung LH, Hertogh De (1968) Gibberellin-like substances in non-cold and cold treated tulip bulbs (Tulipa sp.). In: Wightman F, Setterfield G (eds) Biochemistry and physiology of plant growth substances. The Runge Press, Ottawa, pp 943–956Google Scholar
  4. Aung LH, Herogh De, Staby G (1969) Temperature regulation of endogenous gibberellin activity and development of Tulipa gesneriana L. Plant Physiol 44:403–406CrossRefGoogle Scholar
  5. Balk PA, de Boer AD (1999) Rapid stalk elongation in tulip (Tulipa gesneriana L. cv. Apeldoorn) and the combined action of cold-induced invertase and the water-channel protein gammaTIP. Planta 209:346–354CrossRefGoogle Scholar
  6. 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 72:248–254CrossRefGoogle Scholar
  7. Chan Z (2012) Expression profiling of ABA pathway transcripts indicates crosstalk between abiotic and biotic stress responses in Arabidopsis. Genomics 100:110–115CrossRefGoogle Scholar
  8. Danyluk J, Kane NA, Breton G, Limin AE, Fowler DB, Sarhan F (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol 132: 1849–1860CrossRefGoogle Scholar
  9. Davies JN, Kempton RJ (1975) Carbohydrate changes in tulip bulbs during dry storage and forcing. Acta Horticult 47:353–363CrossRefGoogle Scholar
  10. De Hertogh AA, Le Nard M (1993) Tulipa. In: De Hertogh A, Le Nard M (eds) The physiology of flower bulbs: a comprehensive treatise of the physiology and utilization of ornamental flowering bulbous and tuberous plants. Elsevier, Amsterdam, pp 638–639Google Scholar
  11. Ferreira DA, Martins MCM, Cheavegatti-Gianotto A, Carneiro M, Amadeu RR, Wolf LD, Hoffmann HP, de Abreu LGF, Caldana C (2018) Metabolite profiles of Sugarcane Culm reveal the relationship among metabolism and axillary bud outgrowth in genetically related Sugarcane commercial cultivars. Front Plant Sci 9: 857CrossRefGoogle Scholar
  12. de Hoon MJL, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454CrossRefGoogle Scholar
  13. Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184CrossRefGoogle Scholar
  14. Ehlert C, Maurel C, Tardieu F, Simonneau T (2009) Aquaporin-mediated reduction in maize root hydraulic conductivity impacts cell turgor and leaf elongation even without changing transpiration. Plant Physiol 150:1093–1104CrossRefGoogle Scholar
  15. Eisenbarth DA, Weig AR (2005) Dynamics of aquaporins and water relations during hypocotyl elongation in Ricinus communis L. seedlings. J Exp Bot 56:1831–1842CrossRefGoogle Scholar
  16. Hobson GE (1979) Response of tulip scale mitochondria to temperature in relation to cold treatment of the bulbs. J Exp Bot 30:327–331CrossRefGoogle Scholar
  17. Hobson GE, Davies JN (1977) Mitochondrial activity and carbohydrate levels in tulip bulbs in relation to cold treatment. J Exp Bot 28:559–568CrossRefGoogle Scholar
  18. Hu L, Li H, Pang H, Fu J (2012) Responses of antioxidant gene, protein and enzymes to salinity stress in two genotypes of perennial ryegrass (Lilium perenne) differing in salt tolerance. J Plant Physiol 169:149–156CrossRefGoogle Scholar
  19. Kawata J (1975) Optimum temperature and duration of low temperature treatment for forcing tulips. Acta Hortic 47:201–208CrossRefGoogle Scholar
  20. Khuankaew T, Ruamrungsri S, Ito S, Sato T, Ohtake N, Sueyoshi K, Ohyama T (2010) Assimilation and translocation of nitrogen and carbon in Curcuma alismatifolia Gagnep. Plant Biol (Stuttg) 12:414–423CrossRefGoogle Scholar
  21. Kim D-H, Sung S (2017) The binding specificity of the PHD-finger domain of VIN3 moderates vernalization response. Plant Physiol 173:1258–1268CrossRefGoogle Scholar
  22. Kim D-H, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299CrossRefGoogle Scholar
  23. Koyama K, Hatano H, Nakamura J, Takumi S (2012) Characterization of three VERNALIZATION INSENSITIVE3-like (VIL) homologs in wild wheat, Aegilops tauschii Coss. Hereditas 149:62–71CrossRefGoogle Scholar
  24. Lambrechts H, Rook F, Kolloffel C (1994) Carbohydrate status of tulip bulbs during cold-induced flower stalk elongation and flowering. Plant Physiol 104:515–520CrossRefGoogle Scholar
  25. Le Moigne MA, Guérin V, Furet PM, Billard V, Lebrec A, Spíchal L, Roman H, Citerne S, Morvan-Bertrand A, Limami A, Vian A, Lothier J (2018) Asparagine and sugars are both required to sustain secondary axis elongation after bud outgrowth in Rosa hybrida. J Plant Physiol 222:17–27CrossRefGoogle Scholar
  26. Leeggangers HA, Moreno-Pachon N, Gude H, Immink RG (2013) Transfer of knowledge about flowering and vegetative propagation from model species to bulbous plants. Int J Dev Biol 57:611–620CrossRefGoogle Scholar
  27. Leeggangers HA, Nijveen H, Bigas JN, Hilhorst HW, Immink RG (2017) Molecular regulation of temperature-dependent floral induction in Tulipa gesneriana. Plant Physiol 173:1904–1919CrossRefGoogle Scholar
  28. Lehmann S, Funck D, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids 39:949–962CrossRefGoogle Scholar
  29. Lim M-H, Kim J, Kim Y-S, Chuang K-S, Seo Y-H, Lee I, Kim J, Hong CB, Kim H-J, Park C-M (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16:731–740CrossRefGoogle Scholar
  30. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protocol 1:387–396CrossRefGoogle Scholar
  31. Mattioli R, Biancucci M, Lonoce C, Costantino P, Trovato M (2012) Proline is required for male gametophyte development in Arabidopsis. BMC Plant Biol 12:236CrossRefGoogle Scholar
  32. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  33. Mittler R, Vanderauwera S, Suzuki N, Miller G, Togetti V, Vandepoele K, Gollery M, Shulaev V, Breusegem FV (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309CrossRefGoogle Scholar
  34. Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46:292–299CrossRefGoogle Scholar
  35. Moreno-Pachon NM, Leeggangers HA, Nijveen H, Severing E, Hilhorst H, Immink RG (2016) Elucidating and mining the Tulipa and Lilium transcriptomes. Plant Mol Biol 92:249–261CrossRefGoogle Scholar
  36. Ohyama T, Ikarashi T, Baba A (1988) Effect of cold storage treatment for forcing bulbs on the C and N metabolism of tulip plants. Soil Sci Plant Nutr 34:519–533CrossRefGoogle Scholar
  37. Okubo H, Uemoto S (1985) Changes in endogenous gibberellin and auxin activities during first internode elongation in tulip flower stalk. Plant Cell Physiol 26:709–719CrossRefGoogle Scholar
  38. Ranwala AP, Miller WB (2008) Gibberellin-mediated changes in carbohydrate metabolism during flower stalk elongation in tulips. Plant Growth Regul 55:241–248CrossRefGoogle Scholar
  39. Ream TS, Woods DP, Amasino RM (2013) The molecular basis of vernalization in different plant groups. Cold Spring Harbor Laboratory Press, Volume LXXVII, pp 105–115Google Scholar
  40. Rietveld PL, Wilkinson C, Franssen HM, Balk PA, van der Plas LHW, Weisbeek PJ, de Boer AD (2000) Low temperature sensing in tulip (Tulipa gesneriana L.) is mediated through an increased response to auxin. J Exp Bot 51:587–594CrossRefGoogle Scholar
  41. Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, New YorkGoogle Scholar
  42. Shi H, Wang Y, Cheng Zm Ye T, Chan Z (2012) Analysis of natural variation in bermudagrass (Cynodon dactylon) reveals physiological responses underlying drought tolerance. PLoS ONE 7(12):e53422CrossRefGoogle Scholar
  43. Soga K, Wakabayashi K, Hoson T, Kamisaka S (2000) Flower stalk segments of Arabidopsis thaliana ecotype Columbia lack the capacity to grow in response to exogenously applied auxin. Plant Cell Physiol 41:1327–1333CrossRefGoogle Scholar
  44. Steward FC, Barber JT, Bleichert EF, Roca WM (1971) The behavior of shoot apical of Tulipa in relation to floral induction. Dev Biol 25:310–315CrossRefGoogle Scholar
  45. Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164CrossRefGoogle Scholar
  46. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97CrossRefGoogle Scholar
  47. Van der Toorn A, Zemah H, Van As H, Bendel P, Kamenetsky R (2000) Developmental changes and water status in tulip bulbs during storage: visualization by NMR imaging. J Exp Bot 51:1277–1287CrossRefGoogle Scholar
  48. Van Kilsdonk MG, Nicolay K, Franssen JM, Kolloffel C (2002) Bud abortion in tulip bulbs studied by magnetic resonance imaging. J Exp Bot 53:1603–1611CrossRefGoogle Scholar
  49. Wang Y, Li L, Ye T, Lu Y, Chen X, Wu Y (2013) The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J Exp Bot 64:675–684CrossRefGoogle Scholar
  50. Xu R-Y, Niimi Y, Kojima K (2007) Exogenous GA3 overcomes bud deterioration in tulip (Tulipa gesneriana L.) bulbs during dry storage by promoting endogenous IAA activity in the internodes. Plant Growth Regul 52:1–8CrossRefGoogle Scholar
  51. Xu R-Y, Niimi Y, Yuuki O, Kojima K (2008) Changes in diffusible indole-3-acetic acid from various parts of tulip plant during rapid elongation of the flower stalk. Plant Growth Regul 54:81–88CrossRefGoogle Scholar
  52. Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor downregulated by vernalization. Science 303:1640–1644CrossRefGoogle Scholar
  53. Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Horticultural Plant Biology, Ministry of Education, Key Laboratory of Urban Agriculture in Central China, Ministry of Agriculture, College of Horticulture and Forestry SciencesHuazhong Agricultural UniversityWuhanChina

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