Skip to main content
Log in

Selective trans-Cinnamic Acid Uptake Impairs [Ca2+]cyt Homeostasis and Growth in Cucumis sativus L.

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

To obtain insight into interspecies interactions mediated by allelochemicals, the response of cucumber (Cucumis sativus L. cv Jinyan No.4) and figleaf gourd (Cucurbita ficifolia Bouché) seedlings to trans-cinnamic acid (CA) (1) was investigated. While trans-CA is an autotoxin in cucumber root exudates, figleaf gourd is resistant to it. Cucumber, however, had a high rate of trans-CA uptake by the roots, leading to reduced root growth. The trans-CA treatment also resulted in an intracellular release of Ca2+ from the vacuole to the cytoplasm, and, thus, an increased [Ca2+]cyt level accompanied by gradual loss of cell viability in cucumber roots. Taken together, these results suggest that [Ca2+]cyt homeostatic disturbance is one of the primary triggers for trans-CA phytotoxicity in cucumber.

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

Similar content being viewed by others

References

  • Anil, V.S.and Rao, K.S. 2001. Calcium-mediated signal transduction in plants: A perspective on the role of Ca2+ and CDPKs during early plant development. J. Plant Physiol. 158, 1237–1256.

    Article  CAS  Google Scholar 

  • Baerson, S.R., Sanchez-Moreiras, A., Pedrol-Bonjoch, N., Schulz, M., Kagan, I.A., Agarwal, A.K., Reigosa, M.J., and Duke, S.O. 2005. Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one. J. Biol. Chem. 280, 21867–21881.

    Article  CAS  PubMed  Google Scholar 

  • Bais, H.P., Vepachedu, R., Gilroy, S., Callaway, R.M., and Vivanco, J.M. 2003. Allelopathy and exotic plant invasion: From molecules and genes to species interactions. Science 301, 1377–1380.

    Article  CAS  PubMed  Google Scholar 

  • Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., and Vivanco, J.M. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233–266.

    Article  CAS  PubMed  Google Scholar 

  • Bartels, D. and Sunkar, R. 2005. Drought and salt tolerance in plants. Crit. Rev. Plant Sci. 24, 23–58.

    Article  CAS  Google Scholar 

  • Blum, U. 2005. Relationships between phenolic acid concentrations, transpiration, water utilization, leaf area expansion, and uptake of phenolic acids: nutrient culture studies. J. Chem. Ecol. 31, 1907–1932.

    Article  CAS  PubMed  Google Scholar 

  • Canals, R.M., Emeterio, L.S., and Peralta, J. 2005. Autotoxicity in Lolium rigidum: analyzing the role of chemically mediated interactions in annual plant populations. J. Theor. Biol. 235, 402–407.

    Article  CAS  PubMed  Google Scholar 

  • Chon, S.U., Kim, Y.M., and Lee, J.C. 2003. Herbicidal potential and quantification of causative allelochemicals from several Compositae weeds. Weed Res. 43,444–450.

    Article  CAS  Google Scholar 

  • Ding, J., Sun, Y., Xiao, C.L., Shi, K., Zhou, Y.H., and Yu, J.Q. 2007. Physiological basis of different allelopathic reactions of cucumber and figleaf gourd plants to cinnamic acid. J. Exp. Bot. 58, 3765–3773.

    Article  CAS  PubMed  Google Scholar 

  • EINSET, J., and CONNOLLY, E.L. 2009. Glycine betaine enhances extracellular processes blocking ROS signaling during stress. Plant Signal Behav. 4, 197–199.

    Article  CAS  PubMed  Google Scholar 

  • Fujita K.I. and Kubo, I. 2003. Synergism of polygodial and trans-cinnamic acid on inhibition of root elongation in lettuce seedling growth bioassays. J. Chem. Ecol. 29, 2253–2262.

    Article  CAS  PubMed  Google Scholar 

  • Funk, C. and Brodelius, P.E. 1990. Phenylpropanoid metabolism in suspension cultures of Vanilla planifolia Andr. III. Conversion of 4-methoxycinnamic acids into 4-hydroxybenzoic acids. Plant Physiol. 94, 102–108.

    Article  CAS  PubMed  Google Scholar 

  • Golisz, A., Sugano, M., and Fujii, Y. 2008. Microarray expression profiling of Arabidopsis thaliana L. in response to allelochemicals identified in buckwheat. J. Exp. Bot. 59:3099–3109

    Article  CAS  PubMed  Google Scholar 

  • Hetherington, A.M. and Brownlee, C. 2004. The generation of Ca2+ signals in plants. Annu. Rev. Plant Biol. 55, 401–427.

    Article  CAS  PubMed  Google Scholar 

  • Hierro, J.L. and Callaway, R.M., 2003. Allelopathy and exotic plant invasion. Plant Soil 256, 29–39.

    Article  CAS  Google Scholar 

  • Hiradate, S., Morita, S., Furubayashi, A., Fujii, Y., and Harada, J. 2005. Plant growth inhibition by cis-cinnamoyl glucosides and cis-cinnamic acid. J. Chem. Ecol. 31, 591–601.

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa, S. and Wagatsuma, T. 1998. Plasma membrane permeability of root-tip cells following temporary exposure to Al ions is a rapid measure of Al tolerance among plant species. Plant Cell Physiol. 39, 516–525.

    CAS  Google Scholar 

  • Knight, H. 2000. Calcium signaling during abiotic stress in plants. Inr. Rev. Cytol. 195, 269–324.

    Article  CAS  Google Scholar 

  • Knight, H., Trewavas, A.J., and Knight, M.R. 1997. Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 12, 1067–1078.

    Article  CAS  PubMed  Google Scholar 

  • Lecourieux, D., Raneva, R., and Pugin, A. 2006. Calcium in plant defence-signalling pathways. New Phytol. 171, 249–269.

    Article  CAS  PubMed  Google Scholar 

  • LI, A., WANG, X., LESEBERG, C.H., JIA, J., and MAO, L. 2008. Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivum L.). Plant Signal Behav. 3, 654–656.

    PubMed  Google Scholar 

  • Mahajan, S. and Tuteja, N. 2005. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139–158.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mori, I.C. and Schroeder, J.I. 2004. Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol. 135, 702–708.

    Article  CAS  PubMed  Google Scholar 

  • Orcutt, D.M. and Nilsen, E.T. 2000. The Physiology of Plants Under Stress-soil and Biotic Factors, pp.684. Wiley, J., New York.

  • Pandey, S., Tiwari, S.B., and Upadhyaya, K.C. 2000. Calcium signaling: linking environmental signals to cellular functions. Crit. Rev. Plant Sci. 19, 291–318.

    Article  CAS  Google Scholar 

  • Qin, Y., Yang, J., and Zhao, J. 2005. Calcium changes and the response to methyl jasmonate in rice lodicules during anthesis. Protoplasma 225, 103–122.

    Article  CAS  PubMed  Google Scholar 

  • Rice, E.L. 1984. Allelopathy. 2nd ed. pp. 8–73. Academic Press, New York.

  • Schulz, M. and Friebe, A. 1999. Detoxification of allelochemicals in higher plants and enzymes involved, pp. 383–400, in Inderjit, K.M.M. (ed.). Principles and Practices in Chemical Ecology, Dakshini CRC-Press LLC, Boca Raton, Fl., USA.

    Google Scholar 

  • Schulz, M., Schnabl, H., Manthe, B., Schweihofen, B., and Casser, I. 1993. Uptake and detoxication of salicyclic acid by Vicia faba and Fagopyrum esculentum. Phytochemistry 33, 291–294.

    Article  CAS  Google Scholar 

  • Singh, H.P., Batish, D.R. and Kohli, R.K. 1999. Autotoxicity: Concept, organisms, and ecological significance. Crit. Rev. Plant Sci. 18, 757–772.

    Article  CAS  Google Scholar 

  • Weir, T.L., Bais, H.P., and Vivanco, J.M. 2003. Intraspecific and interspecific interactions mediated by a phytotoxin, (-)-catechin, secreted by the roots of Centaurea maculosa (spotted knapweed). J. Chem. Ecol. 29, 2397–2412.

    Article  CAS  PubMed  Google Scholar 

  • Wong, W.S., Guo, D., Wang, X.L., Yin, Z.Q., Xia, B., and Li, N. 2005. Study of cis-cinnamic acid in Arabidopsis thaliana. Plant Physil. Biochem. 43, 929–937.

    Article  CAS  Google Scholar 

  • Wu, H.W., Haig, T., Partley, J., Lemerle, D., and An, M. 2000. Distribution and exudation of allelochemicals in wheat Triticum aestivum. J. Chem. Ecol. 26, 2141–2154.

    Article  CAS  Google Scholar 

  • Xiong, L.M., Schumaker, K.S., and Zhu, J.K. 2002. Cell signaling during cold, drought and salt stress. Plant Cell 14, S165–S183.

    Article  CAS  PubMed  Google Scholar 

  • Ye, S.F., Yu, J.Q., Peng, Y.H., Zheng, J.H., and Zou, L.Y. 2004. Incidence of Fusarium wilt in Cucumis sativus L. is promoted by cinnamic acid, an autotoxin in root exudates. Plant Soil 263, 143–150.

    Article  CAS  Google Scholar 

  • Ye, S.F., Zhou, Y.H., Sun, Y., Zou, L.Y., and Yu, J.Q. 2006. Cinnamic acid causes oxidative stress in cucumber roots, and promotes incidence of Fusarium wilt. Environ. Exp. Bot. 56, 255–262.

    Article  CAS  Google Scholar 

  • Yin, Z.Q., Wong, W.S., Ye, W.C., and Li, N. 2003. Biologically active cis-cinnamic acid occurs naturally in Brassica parachinensis. Chinese Sci. Bulletin 48,555–558.

    Article  CAS  Google Scholar 

  • Young, C.C. 1984. Autointoxication in root exudates of Asparagus officinalis L. Plant Soil 82, 247–253.

    Article  Google Scholar 

  • Yu, J.Q. and Matsui, Y. 1994. Phytotoxic substances in the root exudates of Cucumis sativus L. J. Chem. Ecol. 20, 21–31.

    Article  CAS  Google Scholar 

  • Yu, J.Q. and Matsui, Y. 1997. Effects of root exudates of cucumber (Cucumis sativus) and allelochemicals on uptake by cucumber seedlings. J. Chem. Ecol. 23, 817–827.

    Article  CAS  Google Scholar 

  • Yu, J.Q., Shou, S.Y., Qian, Y.R., and Hu, W.H. 2000. Autotoxic potential in cucurbit crops. Plant Soil 223, 147–151.

    Article  CAS  Google Scholar 

  • Yu, J.Q., Ye, S.F., Zhang, M.F., and Hu, W.H. 2003. Effects of root exudates, aqueous root extracts of cucumber (Cucumis sativus L.) and allelochemicals on photosynthesis and antioxidant enzymes in cucumber. Biochem. Syst. Ecol. 31, 129–139.

    Article  CAS  Google Scholar 

  • Zhang, W.H. and Rengel, Z. 1999. Aluminium induces an increase in cytoplasmic calcium in intact wheat root apical cells. Aust. J. Plant Physiol. 26, 401–409.

    Article  CAS  Google Scholar 

  • Zhang, W.H., Rengel, Z., and Kuo, J. 1998. Determination of intracellular Ca2+ in intact wheat root cells: loading of acetoxymethyl ester of Fluo-3 under low temperature. Plant J. 15, 147–151.

    Article  Google Scholar 

  • Zhu, J.K. 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247–273.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful for the assistance of Dr. Hong J and Dr. Chen J in confocal and transmission electron microscopy. We also thank Dr. Margot P and Dr. Ye H for critical reading of the manuscript. This work was supported by the National Basic Research Program of China (2009CB119000) and National Key Technology R&D Program of China (2008BADA6B02).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jingquan Yu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yu, J., Sun, Y., Zhang, Y. et al. Selective trans-Cinnamic Acid Uptake Impairs [Ca2+]cyt Homeostasis and Growth in Cucumis sativus L.. J Chem Ecol 35, 1471–1477 (2009). https://doi.org/10.1007/s10886-009-9726-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-009-9726-1

Keywords

Navigation