Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L.

The hypothesis that electric and hydraulic long-distance signals modify photosynthesis and stomatal aperture upon re-irrigation in intact drought-stressed plants was examined. Maize plants (Zea mays L.) were exposed to drought conditions by decreasing the soil water content to 40-50% of field capacity. The decrease in water content resulted in a decline in stomatal conductance to 50-60% of the level in well-watered plants. Re-irrigation of the plants initiated both hydraulic and electric signals, followed by a two-phase response of the net CO2 uptake rate and stomatal conductance of leaves. The transitional first phase (phase 1) is characterized by a rapid decrease in both levels. In the second phase (phase 2), both parameters gradually increase to levels above those of drought-stressed plants. Elimination of either the hydraulic signal by compensatory pressure application to the root system, or of the electric signal by cooling of the leaf blade gave evidence that the two signals (1) propagated independently from each other and (2) triggered the two-phase response in leaf gas exchange. The results provided evidence that the hydraulic signal initiated a hydropassive decrease in stomatal aperture and for the involvement of electric signals in the regulation of photosynthesis of drought-stressed plants.

[1]  J. Passioura,et al.  Root signals control leaf expansion in wheat seedlings growing in drying soil , 1988 .

[2]  H. Kaiser,et al.  Rapid hydropassive opening and subsequent active stomatal closure follow heat-induced electrical signals in Mimosa pudica. , 2006, Journal of experimental botany.

[3]  P. Minchin,et al.  Electrical signalling and systemic proteinase inhibitor induction in the wounded plant , 1992, Nature.

[4]  H. Dziubińska,et al.  The effect of excitation on the rate of respiration in the liverwort Conocephalum conicum , 1989 .

[5]  Rainer Matyssek,et al.  Characteristics of Electrical Signals in Poplar and Responses in Photosynthesis1 , 2005, Plant Physiology.

[6]  E. Steudle,et al.  Direct measurement of xylem pressure in leaves of intact maize plants. A test of the cohesion-tension theory taking hydraulic architecture into consideration , 1999, Plant physiology.

[7]  J. Kucera,et al.  Rapid response of large, drought-stressed beech trees to irrigation. , 1993, Tree physiology.

[8]  E. Steudle,et al.  Water transport in the midrib tissue of maize leaves : direct measurement of the propagation of changes in cell turgor across a plant tissue. , 1985, Plant physiology.

[9]  K. Raschke.  Leaf Hydraulic System: Rapid Epidermal and Stomatal Responses to Changes in Water Supply , 1970, Science.

[10]  E. Schulze.  7 – The Regulation of Plant Transpiration: Interactions of Feedforward, Feedback, and Futile Cycles , 1994 .

[11]  H. Felle,et al.  The apoplastic pH of the substomatal cavity of Vicia faba leaves and its regulation responding to different stress factors. , 2002, Journal of experimental botany.

[12]  K. Raschke.  Stomatal Responses to Pressure Changes and Interruptions in the Water Supply of Detached Leaves of Zea mays L. , 1970, Plant physiology.

[13]  W. J. Davies,et al.  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 , 1997, Plant physiology.

[14]  F. Baluška,et al.  What is apical and what is basal in plant root development? , 2005, Trends in plant science.

[15]  R. Munns,et al.  Water relations and leaf expansion: importance of time scale. , 2000, Journal of experimental botany.

[16]  Rainer Matyssek,et al.  Impairment of gas exchange and structure in birch leaves (Betula pendula) caused by low ozone concentrations , 1991, Trees.

[17]  U. Zimmermann,et al.  Simultaneous recording of xylem pressure and trans‐root potential in roots of intact glycophytes using a novel xylem pressure probe technique , 1998 .

[18]  R. Munns,et al.  Soil water status affects the stomatal conductance of fully turgid wheat and sunflower leaves , 1986 .

[19]  Jianhua Zhang,et al.  Changes in the concentration of ABA in xylem sap as a function of changing soil water status can account for changes in leaf conductance and growth , 1990 .

[20]  B. Aloni,et al.  Water relations and hydraulic control of stomatal behaviour in bell pepper plant in partial soil drying , 2001 .

[21]  Frantisek Baluska,et al.  Plant synapses: actin-based domains for cell-to-cell communication. , 2005, Trends in plant science.

[22]  I. R. Cowan.  Stomatal Behaviour and Environment , 1978 .

[23]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[24]  Rainer Matyssek,et al.  Transient knockout of photosynthesis mediated by electrical signals. , 2004, The New phytologist.

[25]  E. Schulze,et al.  A portable steady-state porometer for measuring the carbon dioxide and water vapour exchanges of leaves under natural conditions , 2004, Oecologia.

[26]  M. Hajirezaei,et al.  The Biochemical Response of Electrical Signaling in the Reproductive System of Hibiscus Plants , 1995, Plant physiology.

[27]  Bratislav Stankovic,et al.  Surface potentials and hydraulic signals in wheat leaves following localized wounding by heat , 1991 .

[28]  J. Boyer,et al.  Root pressurization affects growth-induced water potentials and growth in dehydrated maize leaves. , 2003, Journal of experimental botany.

[29]  J. Fromm,et al.  Electrical signaling and gas exchange in maize plants of drying soil , 1998 .

[30]  Jörg Fromm,et al.  Characteristics of Action Potentials in Willow (Salix viminalis L.) , 1993 .

[31]  William J. Davies,et al.  Root Signals and the Regulation of Growth and Development of Plants in Drying Soil , 1991 .

[32]  D. Cosgrove.  Rapid, bilateral changes in growth rate and curvature during gravitropism of cucumber hypocotyls: implications for mechanism of growth control. , 1990, Plant, cell & environment.

[33]  J. Boyer,et al.  Growth-induced water potentials may mobilize internal water for growth , 1991 .

[34]  Barbara G. Pickard,et al.  Action potentials in higher plants , 1973, The Botanical Review.

[35]  Jörg Fromm,et al.  Electric Signals Released from Roots of Willow (Salix viminalis L.) Change Transpiration and Photosynthesis , 1993 .