Skip to main content
Log in

Seasonal dimorphism and winter chilling stress in Thymus sibthorpii

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

Seasonal dimorphism (summer/winter) has been so far studied only in a few plants and has been focused on summer drought stress. However, Thymus sibthorpii in the study area appears to be affected by winter chilling stress and not by summer drought stress. Thus, the winter leaves were thicker and more compact compared to the summer leaves and they had more stomata and peltate hairs, more sclerenchymatous fibers, vacuoles with phenolics, and chloroplasts than the summer leaves. In addition, their chloroplasts possessed large grana and starch grains. In the summer leaves, cell vacuoles in mesophyll did not contain phenolics, and chloroplasts were devoid of starch grains and had large plastoglobuli. Physiological measurements revealed higher net photosynthetic rate and chlorophyll content in the winter leaves than in the summer leaves. Proline and soluble sugar content along with antioxidative enzyme (superoxide dismutase, peroxidase, ascorbate peroxidase, glutathione reductase) activities were increased in the winter leaves.

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.

Similar content being viewed by others

Abbreviations

APX:

ascorbate peroxidase

Chl:

chlorophyll

E:

transpiration rate

GR:

glutathione reductase

gs :

stomatal conductance

LM:

light microscopy

PN:

net photosynthetic rate

POD:

peroxidase

SEM:

scanning electron microscopy

SOD:

superoxide dismutase

TEM:

transmission electron microscopy

References

  • Aronne, G., De Micco, V.: Seasonal dimorphism in the Mediterranean Cistus incanus L. subsp. incanus. — Ann. Bot. 87: 789–794, 2001.

    Article  Google Scholar 

  • Bafeel, S.O., Ibrahim, M.M.: Antioxidants and accumulation of a-tocopherol induce chilling tolerance in Medicago sativa. — Int. J. Agr. Biol. 10: 593–598, 2008.

    CAS  Google Scholar 

  • Beauchamp, C.H., Fridovich, I.: Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. — Analyt. Biochem. 44: 276–287, 1971.

    Article  CAS  PubMed  Google Scholar 

  • Beck, E.H., Fettig, S., Knake, C., Hartig, K., Bhattarai, T.: Specific and unspecific responses of plants to cold and drought stress. — J. Biosci. 32: 501–510, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Christodoulakis, N.S.: An anatomical study of seasonal dimorphism in the leaves of Phlomis fruticosa. — Ann. Bot. 63: 389–394, 1989.

    Google Scholar 

  • Christodoulakis, N.S., Bazos, J.: Leaf anatomy of three seasonally dimorphic subshrubs. — Acta ecol. 11: 291–296, 1990.

    Google Scholar 

  • Christodoulakis, N.S., Fasseas, C.: Seasonal dimorphism of Phlomis fruticosa under controlled environmental conditions. — Acta ecol. 12: 323–330, 1991.

    Google Scholar 

  • Christodoulakis, N.S., Tsimbani, H., Fasseas, C.: Leaf structural peculiarities in Sarcopoterium spinosum, a seasonally dimorphic subshrub. — Ann. Bot. 65: 291–296, 1990.

    Google Scholar 

  • Crifó, T., Puglisi, I., Petrone, G., Recupero, G.R., Lo Piero, A.R.: Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. — Gene 476: 1–9, 2011.

    Article  PubMed  Google Scholar 

  • Diamantopoulos, J., Margaris, N.S.: The transition of Euphorbia acanthothamnos from the winter to the summer form. — Flora 171: 315–328, 1981.

    Google Scholar 

  • Gratani, L., Bombelli, A.: Leaf anatomy, inclination, and gas exchange relationship in evergreen sclerophyllous and drought semideciduous shrub species. — Photosynthetica 37: 573–585, 1999.

    Article  Google Scholar 

  • Gratani, L., Bombelli, A.: Correlation between leaf age and other leaf traits in three Mediterranean maquis shrub species: Quercus ilex, Phillyrea latifolia and Cistus incanus. — Environm. exp. Bot. 43: 141–153, 2000.

    Article  Google Scholar 

  • Halliwell, B., Foyer, G.: Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. — Planta 139: 9–17, 1978.

    Article  CAS  PubMed  Google Scholar 

  • Hare, P.D., Cress, W.A.: Metabolic implications of stressinduced proline accumulation in plants. — Plant Growth Reg. 21: 79–102, 1997.

    Article  CAS  Google Scholar 

  • Huang, M., Guo, Z.: Responses of antioxidative system to chilling stress in two rice cultivars differing in sensitivity. — Biol. Plant. 49: 81–84, 2005.

    Article  CAS  Google Scholar 

  • Imahori, Y., Takemura, M., Bai, J.: Chilling-induced oxidative stress and antioxidant responses in mume (Prunus mume) fruit during low temperature storage. — Postharvest Biol. Technol. 49: 54–60, 2008.

    Article  CAS  Google Scholar 

  • Karabourniotis, G.: Light-guiding function of foliar sclereid in the evergreen sclerophyll Phillyrea latifolia: a quantitative approach. — J. exp. Bot. 49: 739–746, 1998.

    CAS  Google Scholar 

  • Khan, A.A., McNeilly, T., Collins, C.: Accumulation of amino acids, proline, and carbohydrates in response to aluminum and manganese stress in maize. — J. Plant Nutr. 23: 1303–1314, 2000.

    Article  CAS  Google Scholar 

  • Kumar, S., Malik, J., Thakur, P., Kaistha, S., Sharma, D., Upadhyaya, H.D., Berger, J.D., Nayyar, H.: Growth and metabolic responses of contrasting chickpea (Cicer arietinum) genotypes to chilling stress at reproductive phase. — Acta Physiol. Plant. 33: 779–787, 2011.

    Article  CAS  Google Scholar 

  • Kyparissis, A., Manetas, Y.: Seasonal leaf dimorphism in a semi-deciduous Mediterranean shrub: ecophysiological comparisons between winter and summer leaves. — Acta ecol. 14: 23–32, 1993.

    Google Scholar 

  • Lepistö, A., Rintamäki, E.: Coordination of plastid and light signaling pathways upon development of Arabidopsis leaves under various photoperiods. — Mol. Plant 5: 799–816, 2012.

    Article  PubMed  Google Scholar 

  • Letchamo, W., Xu, H.L., Gosselin, A.: Photosynthetic potential of Thymus vulgaris selections under two light regimes and three soil water levels. — Sci. Hort. 62: 89–101, 1995.

    Article  Google Scholar 

  • Margaris, N.S., Papadogianni, P.: [Effect of daylength on leaf anatomy of Euphorbia acanthothamnos and its ecological significance.] — Beitr. Biol. Pflanz. 51: 353–358, 1975. [In German]

    Google Scholar 

  • Marin, M., Koko, V., Duletic-Lausevic, S., Marin, P.D.: Micromorphology of trichomes of Thymus malyi (Lamiaceae). — J. Microscop. 232: 406–409, 2008.

    Article  CAS  Google Scholar 

  • Michelet, L., Krieger-Liszkay, A.: Reactive oxygen intermediates produced by photosynthetic electron transport are enhanced in short-day grown plants. — Biochim. biophys. Acta Bioenerg. 1817: 1306–1313, 2012.

    Article  CAS  Google Scholar 

  • Mittler, R., Vanderauwera, S., Gollery, M., Breusegem, F.V.: Reactive oxygen gene network of plants. — Trends Plant Sci. 9: 490–498, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Mohammadian, M.A., Mobrami, Z., Sajedi, R.H.: Bioactive compounds and antioxidant capacities in the flavedo tissue of two citrus cultivars under low temperature. — Braz. J. Plant Physiol. 23: 203–208, 2011.

    CAS  Google Scholar 

  • Nakano, Y., Asada, K.: Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate depleted medium and reactivation by monodehydroascorbate radical. — Plant Cell Physiol. 28: 131–140, 1987.

    CAS  Google Scholar 

  • Ngo, T.T., Lenhoff, H.M.: A sensitive and versatile chromogenic assay for peroxidase and peroxidase-coupled reactions. — Anal. Biochem. 105: 389–397, 1980.

    Article  CAS  PubMed  Google Scholar 

  • Patakas, A., Noitsakis, B.: Leaf age effects on solute accumulation in water-stressed grapevines. — J. Plant Physiol. 158: 63–69, 2001.

    Article  CAS  Google Scholar 

  • Plumer, D.T.: Practical Biochemistry. — McGraw-Hill, New York 1987.

    Google Scholar 

  • Pongprasert, N., Sekozawa, Y., Sugaya, S., Gemma, H.: The role and mode of action of UV-C hormesis in reducing cellular oxidative stress and the consequential chilling injury of banana fruit peel. — Int. Food Res. J. 18: 741–749, 2011.

    CAS  Google Scholar 

  • Queval, G., Issakidis-Bourguet, E., Hoeberichts, F.A., Vandorpe, M., Gakiere, B., Vanacker, H., Miginiac-Maslow, M., Van Breusegem, F., Noctor, G.: Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. — Plant J. 52: 640–657, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Satil, F., Kaya, A., Bicakli, A., Özatli, S., Tümen, G.: Comparative morphological, anatomical and palynological studies on Thymus migricus Klokov & Des.-Shost and T. fedtschenkoi Ronniger var. handelii (Ronniger) Jalas grown in East Anatolia. — Pak. J. Bot. 37: 531–549, 2005.

    Google Scholar 

  • Steer, M.V.: Understanding Cell Structure. — Cambridge University Press, Cambridge 1981.

    Google Scholar 

  • Wintermans, J.F., Mots, A.: Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. — Biochim. biophys. Acta 109: 448–453, 1965.

    Article  CAS  PubMed  Google Scholar 

  • Yadav, S.K.: Cold stress tolerance mechanisms in plants. A review. — Agron. Sustain. Dev. 30: 515–527, 2010.

    Article  CAS  Google Scholar 

  • Zhang, Y.H., Chen, L.J., He, J.L., Qian, L.S., Wu, L.Q., Wang, R.F.: Characteristics of chlorophyll fluorescence and antioxidative system in super-hybrid rice and its parental cultivars under chilling stress. — Biol. Plant. 54: 164–168, 2010.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. M. Bosabalidis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lianopoulou, V., Patakas, A. & Bosabalidis, A.M. Seasonal dimorphism and winter chilling stress in Thymus sibthorpii . Biol Plant 58, 139–146 (2014). https://doi.org/10.1007/s10535-013-0371-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-013-0371-8

Additional key words

Navigation