Abstract
The systematic or long-distance signal transmission plays crucial roles in animal lives. Compared with animals, however, much less is known about the roles of long-distance signal communication in plant lives. Using the model plant Commelina communis L., we have probed the root to shoot communication mediated by heat-shock signals. The results showed that a heat shock of 5 min at 40°C in partial roots, i.e. half or even 1/4 root system, could lead to a significant decrease in stomatal conductance. The regulation capability depends on both heat shock temperature and the amount of root system, i.e. with higher temperature and more roots stressed, the leaf conductance would decrease more significantly. Interestingly, the stomatal regulation by heat shock signal is in a manner of oscillation: when stomata conductance decreased to the lowest level within about 30 min, it would increase rapidly and sometimes even exceed the initial level, and after several cycles the stomata conductance would be finally stabilized at a lower level. Feeding xylem sap collected from heat-shocked plants could lead to a decrease in stomata conductance, suggesting that the heat shock-initiated signal is basically a positive signal. Further studies showed that heat shock was not able to affect ABA content in xylem sap, and also, not able to lead to a decrease in leaf water status, which suggested that the stomatal regulation was neither mediated by ABA nor by a hydraulic signal. Heat shock could lead to an increase in xylem sap H2O2 content, and moreover, the removal of H2O2 by catalase could partially recover the stomatal inhibition by xylem sap collected from heat-shocked plants, suggesting that H2O2 might be able to act as one of the root signals to control the stomatal movement. Due to the fact that heat-shock and drought are usually two concomitant stresses, the stomatal regulation by heat-shock signal should be of significance for plant response to stresses. The observation for the stomatal regulation in an oscillation manner by presently identified new signals should contribute to further understanding of the mystery for the pant systematic signaling in response to stresses.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Xiong, L., Schumaker, K. S., Zhu, J. K., Cell signaling during cold, drought, and salt stress, Plant Cell, 2002, S165-S183.
Neill, S. J., Burnett, E. C., Regulation of gene expression during water deficit stress, J. Plant Growth Regul., 1999, 29: 23–33.
Jia, W. S., He, F. L., Zhang, D. P., Cell biological mechanism for triggering of ABA accumulation under water stress in Vicia faba leaves, Science in China, Ser. C, 2001, 44: 421–428
Ingram, J., Bartes, D., The molecular basis of dehydration tolerance in plants, Annu. Rev. Plant Mol. Plant Physiol., 1996, 47: 377–403.
Liu, X., Shi, W. L., Zhang, S. Q. et al., Nitric oxide involved in signal transduction of Jasmonic acid-induced stomatal closure of Vicia faba L., Chinese Science Bulletin, 2005, 50(6): 520–525.
Shi, W. L., Jia, W. S., Liu, X. et al., Protein tyrosine phosphatases involved in signaling of the ABA-induced H2O2 generation in guard cells of Vicia faba L., Chinese Science Bulletin, 2004, 49(17): 1841–1846.
Wang, H. B., Zhang, S. Q., Wang, X. C. et al., Involvement of Ca2+/CaM in the signal transduction of acetylcholine regulating stomatal movement, Chinese Science Bulletin, 2003, 48(4): 351–354.
Davies, W. J., Zhang, J., Root signals and the regulation of growth and development of plants in drying soil, Annu. Rev. Plant Physiol. Mol. Biol., 1991, 43: 55–75.
Sobeih, W. Y., Dodd, I. C., Bacon, M. A. et al., Long-distance signals regulating stomatal conductance and leaf growth in tomato (Lycopersicon esculentum) plants subjected to partial root-zone drying, 2004, J. Exp. Bot., 55: 2353–2363.
Jackson, M. B., Long-distance signalling from roots to shoots assessed: The flooding story, J. Exp. Bot., 2002, 53: 175–181.
Liang, J., Zhang, J., Xylem-carried ABA in plant response to soil drying, Current Topics in Plant Biology, 1999, 1: 89–96.
Wang, H. B., Zhang, S. Q., Wang, X. C. et al., Role of acetylcholine on plant root-shoot signal transduction, Chinese Science Bulletin, 2003, 48(6): 570–573.
Wilkinson, S., Davies, W. J., Xylem Sap pH Increase: A drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast, Plant Physiol., 1997, 113: 559–573.
Bahrun, A., Jensen, C. R., Asch, F. et al., Drought-induced changes in xylem pH, ionic composition, and ABA concentration act as early signals in field-grown maize (Zea mays L.), J. Exp. Bot., 2002, 53: 251–263.
Bacon, M. A., Wilkinson, S., Davies, W. J., pH-regulated leaf cell expansion in droughted plants is abscisic acid dependent, Plant Physiol., 1998, 118: 1507–1515.
Munns, R., A leaf elongation bioassay detects an unknown growth inhibitor in xylem sap from wheat and barley, Australian J. Plant Physiol., 1992, 19: 127–135.
Quarrie, S. A., Whitford, P. N., Appleford, N. E. J. et al., A monoclonal antibody to (s)-abscisic acid: Its characterization and use in a radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves, Planta, 1998, 173: 330–339.
Bellincampi, D., Dipierro, N., Salvi, G. et al., Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxine-regulated rolB gene expression in tobacco leaf explants, Plant Physiol., 2000, 122: 1379–1385.
Seong, H. L., Singh, A. P., Chung, G. C., Rapid accumulation of hydrogen peroxide in cucumber roots due to exposure to low temperature appears to mediate decreases in water transport, J. Exp. Bot., 2004, 55: 1733–1741.
Ranathunge, K., Kotula, L., Steudle, E. et al., Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores, J. Exp. Bot., 2004, 55: 433–447.
Fennell, A., Markhart, A., Rapid acclimation of root hydraulic conductivity to low temperature, J. Exp. Bot., 1998, 49: 879–884.
Malone, M., Stankovic, B., Surface potentials and hydraulic signals in wheat leaves following localized wounding by heat, Plant Cell Environ., 1991, 14: 431–436.
Zhang, X., Zhang, L., Dong, F. et al., Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba, Plant Physiol., 2001, 126: 1438–1448.
Zhong, C., Gallie, D. R., The ascorbic acid redox state controls guard cell signaling and stomatal movement, Plant Cell, 2004, 16: 1143–1162.
Xiaoping, S., Xigui, S., Junmin, H., Role and relationship of nitric oxide and hydrogen peroxide in light/dark regulated stomatal movement in Vica faba, Acta Botanica Sinica, 2004, 46: 1292–1300.
Zhenming, P., Yoshiyuki, M., Gregor, B. et al., Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cell, Nature, 2000, 406: 731–734.
Rosa, A. V., Maria, C. D. P., Daniela, V. et al., Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat Shock-induced programmed cell death in tobacco bright-yellow 2 cells, Plant Physiol., 2004, 134: 1100–1112.
James, F. D., Humberto, L. D., Christine, H. F. et al., Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings, Plant Physiol., 1998, 116: 1351–1357.
Foyer, C. H., Lopez-Delgado, H., Dat, J. F., Hydrogen peroxide and glutathione associated mechanisms of acclimatory stress tolerance and signaling, Physiol. Plant, 1997, 100: 241–254.
Sharp, R. E., LeNoble, M. E., ABA, ethylene and the control of shoot and root growth under water stress, J. Exp. Bot., 2002, 53: 33–37.
Jonathan, P. C., Hydraulic and chemical signalling in the control of stomatal conductance and transpiration, J. Exp. Bot., 2002, 53: 195–200.
Paszewski, A., Zawadxki, T., Action potential in Lupinus angusti-folius L. shoots, J. Exp. Bot., 1976, 27: 959–863.
Roblin, G., Analysis of the variation potential induced by wounding in plants, Plant Cell Physiol., 1985, 26: 455–476.
Roblin, G., Bonnemain, J. L., Propagation in vicia faba stem of potention variation induced by wounding, Plant Cell Physiol., 1985, 26: 1273–1282.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yang, S., Huang, C., Wu, Z. et al. Stomatal movement in response to long distance-communicated signals initiated by heat shock in partial roots of Commelina communis L.. SCI CHINA SER C 49, 18–25 (2006). https://doi.org/10.1007/s11427-005-0117-8
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11427-005-0117-8