Journal of Chemical Ecology

, Volume 35, Issue 12, pp 1471–1477 | Cite as

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

  • Jingquan Yu
  • Yao Sun
  • Yun Zhang
  • Ju Ding
  • Xiaojian Xia
  • Chunlan Xiao
  • Kai Shi
  • Yanhong Zhou
Article

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.

Keywords

Allelopathy Cucumis sativus Cucurbitaceae Cucurbit Cucumber Signalling Autotoxicity Cinnamic acid Detoxification 

Notes

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).

References

  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefPubMedGoogle Scholar
  5. Bartels, D. and Sunkar, R. 2005. Drought and salt tolerance in plants. Crit. Rev. Plant Sci. 24, 23–58.CrossRefGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. EINSET, J., and CONNOLLY, E.L. 2009. Glycine betaine enhances extracellular processes blocking ROS signaling during stress. Plant Signal Behav. 4, 197–199.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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 CrossRefPubMedGoogle Scholar
  14. Hetherington, A.M. and Brownlee, C. 2004. The generation of Ca2+ signals in plants. Annu. Rev. Plant Biol. 55, 401–427.CrossRefPubMedGoogle Scholar
  15. Hierro, J.L. and Callaway, R.M., 2003. Allelopathy and exotic plant invasion. Plant Soil 256, 29–39.CrossRefGoogle Scholar
  16. 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.CrossRefPubMedGoogle Scholar
  17. 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.Google Scholar
  18. Knight, H. 2000. Calcium signaling during abiotic stress in plants. Inr. Rev. Cytol. 195, 269–324.CrossRefGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. Lecourieux, D., Raneva, R., and Pugin, A. 2006. Calcium in plant defence-signalling pathways. New Phytol. 171, 249–269.CrossRefPubMedGoogle Scholar
  21. 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.PubMedGoogle Scholar
  22. Mahajan, S. and Tuteja, N. 2005. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139–158.CrossRefPubMedGoogle Scholar
  23. Mittler, R., Vanderauwere, S., Gollery, M., and Breusegem, F.V. 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. Orcutt, D.M. and Nilsen, E.T. 2000. The Physiology of Plants Under Stress-soil and Biotic Factors, pp.684. Wiley, J., New York.Google Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. Rice, E.L. 1984. Allelopathy. 2nd ed. pp. 8–73. Academic Press, New York.Google Scholar
  29. 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
  30. 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.CrossRefGoogle Scholar
  31. Singh, H.P., Batish, D.R. and Kohli, R.K. 1999. Autotoxicity: Concept, organisms, and ecological significance. Crit. Rev. Plant Sci. 18, 757–772.CrossRefGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. Xiong, L.M., Schumaker, K.S., and Zhu, J.K. 2002. Cell signaling during cold, drought and salt stress. Plant Cell 14, S165–S183.CrossRefPubMedGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. Young, C.C. 1984. Autointoxication in root exudates of Asparagus officinalis L. Plant Soil 82, 247–253.CrossRefGoogle Scholar
  40. Yu, J.Q. and Matsui, Y. 1994. Phytotoxic substances in the root exudates of Cucumis sativus L. J. Chem. Ecol. 20, 21–31.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. Yu, J.Q., Shou, S.Y., Qian, Y.R., and Hu, W.H. 2000. Autotoxic potential in cucurbit crops. Plant Soil 223, 147–151.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Zhu, J.K. 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247–273.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Jingquan Yu
    • 1
    • 2
  • Yao Sun
    • 1
  • Yun Zhang
    • 1
  • Ju Ding
    • 1
  • Xiaojian Xia
    • 1
  • Chunlan Xiao
    • 1
  • Kai Shi
    • 1
  • Yanhong Zhou
    • 1
  1. 1.Department of HorticultureHuajiachi Campus, Zhejiang UniversityHangzhouPeople’s Republic of China
  2. 2.Key Laboratory of Horticultural Plants Growth, Development and BiotechnologyAgricultural Ministry of ChinaHangzhouPeople’s Republic of China

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