A non-invasive plant-based probe for continuous monitoring of water stress in real time: a new tool for irrigation scheduling and deeper insight into drought and salinity stress physiology

Zimmermann, Ulrich; Bitter, Rebecca; Marchiori, Paulo Eduardo Ribeiro; Rüger, Simon; Ehrenberger, Wilhelm; Sukhorukov, Vladimir L.; Schüttler, Annika; Ribeiro, Rafael Vasconcelos

Abstract

The non-invasive, magnetic leaf patch clamp pressure probe (also termed ZIM-probe) allows for the first time to measure continuously turgor pressure changes of plant leaves over long periods of time with high precision and in real time. The probe has become an important tool in plant physiology, molecular biology and ecology, but also in agriculture because the probe is very robust and user-friendly. Growers receive the information about the water status of their plants by wireless telemetry, mobile network and internet on an as-needed basis and can thus adjust very precisely both the timing of irrigation and the quantity of water to apply. Effects of air and leaf temperature, relative humidity, illumination and wind on turgor pressure can be monitored very sensitively both under indoor and outdoor conditions. Even the effects of blue and red light as well as of oscillations of stomata aperture on turgor pressure can be monitored by the probe with high sensitivity. Similarly, water deficit due to increase of the osmotic pressure in the nutrition solutions resulted in significant changes of the probe signals. Multiple probe readings open up new possibilities to resolve (together with other techniques) the mechanisms of short- and long-distance water transport, particularly how plants can cope with water shortage. The applications of the magnetic probe are numerous and one can expect highly interesting developments in plant water relations in the nearest future.

drought; leaf patch clamp pressure probe; osmotic pressure; salinity; water relations; ZIM-probe

Ache P, Bauer H, Kollist H, Al-Rasheid KA, Lautner S, Hartung W, Hedrich R (2010) Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements. Plant Journal 62:1072-1082.
Balling A, Zimmermann U (1990) Comparative measurements of the xylem pressure of Nicotiana plants by means of the pressure bomb and pressure probe. Planta 182:325-338.
Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127-1142.
Bramley H, Ehrenberger W, Zimmermann U, Palta JA, Rüger S, Siddique KHM (2013) Non-invasive pressure probes magnetically clamped to leaves to monitor the water status of wheat. Plant and Soil 369:257-268.
Búrquez A (1987) Leaf thickness and water deficit in plants: a tool for field studies. Journal of Experimental Botany 38:109-114.
Davies E (2006) Electrical signals in plants: facts and hypotheses. In: Volkov A (ed), Plant electrophysiology, theory and methods, pp.407-422. Germany, Springer, Berlin Heidelberg.
Ehrenberger W, Rüger S, Rodriguez-Dominguez CM, Díaz-Espejo A, Fernández JE, Moreno J, Zimmermann D, Sukhorukov L, Zimmermann U (2012) Leaf patch clamp pressure probe measurements on olive leaves in a nearly turgorless state. Plant Biology 14:666-674.
Farquhar GD, Cowan IR (1974) Oscillations in stomatal conductance. Plant Physiology 54:769-772.
Feller U (2006) Stomatal opening at elevated temperature: an underestimated regulatory mechanism? General and Applied Plant Physiology. Special issue:19-31.
Fernández JE, Palomo MJ, Díaz-Espejo A, Clothier BE, Green SR, Gíron IF, Moreno F (2001) Heat-pulse measurements of sap flow in olives for automating irrigation: tests, root flow and diagnostics of water stress. Agricultural and Water Management 51:99-123.
Fernández JE, Durán PJ, Palomo MJ, Díaz-Espejo A, Charmorro V, Gíron IF (2006) Calibration of sap flow measurements by the compensation heat-pulse method in olive, plum and orange trees: relations with xylem anatomy. Tree Physiology 26:719-728.
Fernández JE, Rüger S, Rodriguez-Dominguez CM, Martín-Palomo MJ, Torres-Ruiz JM, Cuevas MV, Ehrenberger W, Diaz-Espejo A, Perez-Martin A, Zimmermann U (2010) Turgor pressure-related measurements with the LPCP probe. An alternative to the use of the Scholander chamber? In: X Simposium hispano-portugués de relaciones hídricas en las plantas. Cartagena, Spain, pp. 6-8.
Fromm J (2006) Long-distance electrical signaling and physiological functions in higher plants. In: Volkov A (ed), Plant electrophysiology, theory and methods, pp. 269-285, Germany, Springer, Berlin Heidelberg.
Geitmann A (2006) Experimental approaches used to quantify physical parameters at cellular and subcellular levels. American Journal of Botany 93:1380-1390.
Green S, Clothier B, Jardine B (2003) Theory and practical application of heat pulse to measure sap flow. Agronomy Journal 95:1371-1379.
Gurovich LA, Hermosilla P (2009) Electric signalling in fruit trees in response to water applications and light-darkness conditions. Journal of Plant Physiology 166:290-300.
Jones HG (2007) Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance. Journal of Experimental Botany 58:119-130.
Lintilhac PM, Wei C, Tanguay JJ, Outwater JO (2000) Ball tonometry: a rapid, non-destructive method for measuring cell turgor pressure in thin-walled plant cells. Journal of Plant Growth Regulation 19:90-97.
Malone M (1993) Hydraulic signals. Philosophical Transactions of the Royal Society. Biological Sciences B 341:33-39.
McBurney T (1992) The relationship between leaf thickness and plant water potential. Journal of Experimental Botany 43:327-335.
Nadler A, Raveh E, Yermiyahu A, Green SR (2003) Evaluation of TDR use to monitor water content in stem of lemon trees and soil and their responses to water stress. Soil Science Society of America Journal 67:437-448.
Nadler A, Raveh E, Yermiyahu A, Green SR (2006) Stress induced water content variations in mango stem by time domain reflectometry. Soil Science Society of America Journal 70:510-520.
Raschke K (1975) Stomatal action. Annual Review of Plant Physiology 26:309-340.
Ribeiro RV, Machado EC, Santos MG (2005) Leaf temperature in sweet orange plants under field conditions: influence of meteorological elements. Revista Brasileira de Agrometeorologia 13:353-368.
Ritchie GA, Hinckley TM (1975) The pressure chamber as an instrument for ecological research. Advances in Ecology Research 9:165-254.
Rodriguez-Dominguez CM, Ehrenberger W, Sann C, Rüger S, Sukhorukov V, Martín-Palomo MJ, Diaz-Espejo A, Cuevas MV, Torres-Ruiz JM, Perez-Martin A, Zimmermann U, Fernández JE (2012) Concomitant measurements of stem sap flow and leaf turgor pressure in olive trees using the leaf patch clamp pressure probe. Agricultural Water Management 114:50-58.
Rüger S (2008) Leaf Patch Clamp Pressure Messungen an Arabidopsis thaliana Master Thesis. Julius-Maxilimians University of Würzburg.
Rüger S, Ehrenberger W, Arend M, Geßner P, Zimmermann G, Zimmermann D, Bentrup F-W, Nadler A, Raveh E, Sukhorukov VL, Zimmermann U (2010a) Comparative monitoring of temporal and spatial changes in tree water status using the non-invasive leaf patch clamp pressure probe and the pressure bomb. Agricultural Water Management 98:283-290.
Rüger S, Netzer Y, Westhoff M, Zimmermann D, Reuss R, Ovadiya S, Gessner P, Zimmermann G, Schwartz A, Zimmermann U (2010b) Remote monitoring of leaf turgor pressure of grapevines subjected to different irrigation treatments using the leaf patch clamp pressure probe. Australian Journal of Grape and Wine Research 16:405-412.
Schwartz A, Zeiger E (1984) Metabolic energy for stomatal opening. Roles of photophosphorylation and oxidative phosphorylation. Planta 161:129-136.
Scholander P, Hammel H, Bradstreet ED, Hemmingsen E (1965) Sap pressure in vascular plants. Science 148:339-346.
Wegner LH, Zimmermann U (1998) Simultaneous recording of xylem pressure and trans-root potential in roots of intact glycophytes using a novel xylem pressure probe technique. Plant, Cell and Environment 21:849-865.
Westhoff M, Schneider H, Zimmermann D, Mimietz S, Stinzing A, Wegner LH, Kaiser W, Krohne G, Shirley S, Jakob P, Bamberg E, Bentrup F-W, Zimmermann U (2008) The mechanisms of refilling of xylem conduits and bleeding of tall birch during spring. Plant Biology 10:604-623.
Westhoff M, Reuss R, Zimmermann D, Netzer Y, Gessner A, Gessner P, Zimmermann G, Wegner LH, Bamberg E, Schwartz A, Zimmermann U (2009a) A non-invasive probe for online-monitoring of turgor pressure changes under field conditions. Plant Biology 11:701-712.
Westhoff M, Zimmermann D, Zimmermann G, Gessner P, Wegner LH, Bentrup F-W, Zimmermann U (2009b) Distribution and function of epistomatal mucilage plugs. Protoplasma 235:101-105.
Zimmermann U, Räde H, Steudle E (1969) Kontinuierliche druckmessung in pflanzenzellen. Naturwissenschaften 56:634-634.
Zimmermann U, Schneider H, Wegner LH, Wagner H-J, Szimtenings M, Haase A, Bentrup F-W (2002) What are the driving forces for water lifting in the xylem conduit? Physiologia Plantarum 114:327-335.
Zimmermann U, Schneider H, Wegner LH, Haase A (2004) Water ascent in tall trees: does evolution of land plants rely on a highly metastable state? New Phytologist 162:575-615.
Zimmermann D, Westhoff M, Zimmermann G, Gessner P, Gessner A, Wegner LH, Rokitta M, Ache P, Schneider H, Vásquez JA, Kruck W, Shirley S, Jakob P, Hedrich R, Bentrup FW, Bamberg E, Zimmermann U (2007) Foliar water supply of tall trees: evidence for mucilage-facilitated moisture uptake from the atmosphere and the impact on pressure bomb measurements. Protoplasma 232:11-34.
Zimmermann D, Reuss R, Westhoff M, Gessner P, Bauer W, Bamberg E, Bentrup F-W, Zimmermann U (2008) A novel, non-invasive, online-monitoring, versatile and easy plant-based probe for measuring leaf water status. Journal of Experimental Botany 59:3157-3167.
Zimmermann U, Rüger S, Shapira O, Westhoff M, Wegner LH, Reuss R, Gessner P, Zimmermann G, Israeli Y, Zhou A, Schwartz A, Bamberg E, Zimmermann D (2010) Effects of environmental parameters and irrigation on the turgor pressure of banana plants measured using the non-invasive, online monitoring leaf patch clamp pressure probe. Plant Biology 12:424-436.
Zimmermann U, Bitter R, Schüttler A, Ehrenberger W, Rüger S, Bramley H, Siddique K, Arend M, Bader MKF (2013) Advanced plant-based, internet-sensor technology gives new insights into hydraulic plant functioning. Acta Horticulturae 991:313-320.

Publication Dates

Publication in this collection
23 June 2015
Date of issue
2013

History

Received
18 Apr 2013
Accepted
30 Apr 2013

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Ache P, Bauer H, Kollist H, Al-Rasheid KA, Lautner S, Hartung W, Hedrich R (2010) Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements. Plant Journal 62:1072-1082.

[2] Balling A, Zimmermann U (1990) Comparative measurements of the xylem pressure of Nicotiana plants by means of the pressure bomb and pressure probe. Planta 182:325-338.

[3] Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127-1142.

[4] Bramley H, Ehrenberger W, Zimmermann U, Palta JA, Rüger S, Siddique KHM (2013) Non-invasive pressure probes magnetically clamped to leaves to monitor the water status of wheat. Plant and Soil 369:257-268.

[5] Búrquez A (1987) Leaf thickness and water deficit in plants: a tool for field studies. Journal of Experimental Botany 38:109-114.

[6] Davies E (2006) Electrical signals in plants: facts and hypotheses. In: Volkov A (ed), Plant electrophysiology, theory and methods, pp.407-422. Germany, Springer, Berlin Heidelberg.

[7] Ehrenberger W, Rüger S, Rodriguez-Dominguez CM, Díaz-Espejo A, Fernández JE, Moreno J, Zimmermann D, Sukhorukov L, Zimmermann U (2012) Leaf patch clamp pressure probe measurements on olive leaves in a nearly turgorless state. Plant Biology 14:666-674.

[8] Farquhar GD, Cowan IR (1974) Oscillations in stomatal conductance. Plant Physiology 54:769-772.

[9] Feller U (2006) Stomatal opening at elevated temperature: an underestimated regulatory mechanism? General and Applied Plant Physiology. Special issue:19-31.

[10] Fernández JE, Palomo MJ, Díaz-Espejo A, Clothier BE, Green SR, Gíron IF, Moreno F (2001) Heat-pulse measurements of sap flow in olives for automating irrigation: tests, root flow and diagnostics of water stress. Agricultural and Water Management 51:99-123.

[11] Fernández JE, Durán PJ, Palomo MJ, Díaz-Espejo A, Charmorro V, Gíron IF (2006) Calibration of sap flow measurements by the compensation heat-pulse method in olive, plum and orange trees: relations with xylem anatomy. Tree Physiology 26:719-728.

[12] Fernández JE, Rüger S, Rodriguez-Dominguez CM, Martín-Palomo MJ, Torres-Ruiz JM, Cuevas MV, Ehrenberger W, Diaz-Espejo A, Perez-Martin A, Zimmermann U (2010) Turgor pressure-related measurements with the LPCP probe. An alternative to the use of the Scholander chamber? In: X Simposium hispano-portugués de relaciones hídricas en las plantas. Cartagena, Spain, pp. 6-8.

[13] Fromm J (2006) Long-distance electrical signaling and physiological functions in higher plants. In: Volkov A (ed), Plant electrophysiology, theory and methods, pp. 269-285, Germany, Springer, Berlin Heidelberg.

[14] Geitmann A (2006) Experimental approaches used to quantify physical parameters at cellular and subcellular levels. American Journal of Botany 93:1380-1390.

[15] Green S, Clothier B, Jardine B (2003) Theory and practical application of heat pulse to measure sap flow. Agronomy Journal 95:1371-1379.

[16] Gurovich LA, Hermosilla P (2009) Electric signalling in fruit trees in response to water applications and light-darkness conditions. Journal of Plant Physiology 166:290-300.

[17] Jones HG (2007) Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance. Journal of Experimental Botany 58:119-130.

[18] Lintilhac PM, Wei C, Tanguay JJ, Outwater JO (2000) Ball tonometry: a rapid, non-destructive method for measuring cell turgor pressure in thin-walled plant cells. Journal of Plant Growth Regulation 19:90-97.

[19] Malone M (1993) Hydraulic signals. Philosophical Transactions of the Royal Society. Biological Sciences B 341:33-39.

[20] McBurney T (1992) The relationship between leaf thickness and plant water potential. Journal of Experimental Botany 43:327-335.

[21] Nadler A, Raveh E, Yermiyahu A, Green SR (2003) Evaluation of TDR use to monitor water content in stem of lemon trees and soil and their responses to water stress. Soil Science Society of America Journal 67:437-448.

[22] Nadler A, Raveh E, Yermiyahu A, Green SR (2006) Stress induced water content variations in mango stem by time domain reflectometry. Soil Science Society of America Journal 70:510-520.

[23] Raschke K (1975) Stomatal action. Annual Review of Plant Physiology 26:309-340.

[24] Ribeiro RV, Machado EC, Santos MG (2005) Leaf temperature in sweet orange plants under field conditions: influence of meteorological elements. Revista Brasileira de Agrometeorologia 13:353-368.

[25] Ritchie GA, Hinckley TM (1975) The pressure chamber as an instrument for ecological research. Advances in Ecology Research 9:165-254.

[26] Rodriguez-Dominguez CM, Ehrenberger W, Sann C, Rüger S, Sukhorukov V, Martín-Palomo MJ, Diaz-Espejo A, Cuevas MV, Torres-Ruiz JM, Perez-Martin A, Zimmermann U, Fernández JE (2012) Concomitant measurements of stem sap flow and leaf turgor pressure in olive trees using the leaf patch clamp pressure probe. Agricultural Water Management 114:50-58.

[27] Rüger S (2008) Leaf Patch Clamp Pressure Messungen an Arabidopsis thaliana Master Thesis. Julius-Maxilimians University of Würzburg.

[28] Rüger S, Ehrenberger W, Arend M, Geßner P, Zimmermann G, Zimmermann D, Bentrup F-W, Nadler A, Raveh E, Sukhorukov VL, Zimmermann U (2010a) Comparative monitoring of temporal and spatial changes in tree water status using the non-invasive leaf patch clamp pressure probe and the pressure bomb. Agricultural Water Management 98:283-290.

[29] Rüger S, Netzer Y, Westhoff M, Zimmermann D, Reuss R, Ovadiya S, Gessner P, Zimmermann G, Schwartz A, Zimmermann U (2010b) Remote monitoring of leaf turgor pressure of grapevines subjected to different irrigation treatments using the leaf patch clamp pressure probe. Australian Journal of Grape and Wine Research 16:405-412.

[30] Schwartz A, Zeiger E (1984) Metabolic energy for stomatal opening. Roles of photophosphorylation and oxidative phosphorylation. Planta 161:129-136.

[31] Scholander P, Hammel H, Bradstreet ED, Hemmingsen E (1965) Sap pressure in vascular plants. Science 148:339-346.

[32] Wegner LH, Zimmermann U (1998) Simultaneous recording of xylem pressure and trans-root potential in roots of intact glycophytes using a novel xylem pressure probe technique. Plant, Cell and Environment 21:849-865.

[33] Westhoff M, Schneider H, Zimmermann D, Mimietz S, Stinzing A, Wegner LH, Kaiser W, Krohne G, Shirley S, Jakob P, Bamberg E, Bentrup F-W, Zimmermann U (2008) The mechanisms of refilling of xylem conduits and bleeding of tall birch during spring. Plant Biology 10:604-623.

[34] Westhoff M, Reuss R, Zimmermann D, Netzer Y, Gessner A, Gessner P, Zimmermann G, Wegner LH, Bamberg E, Schwartz A, Zimmermann U (2009a) A non-invasive probe for online-monitoring of turgor pressure changes under field conditions. Plant Biology 11:701-712.

[35] Westhoff M, Zimmermann D, Zimmermann G, Gessner P, Wegner LH, Bentrup F-W, Zimmermann U (2009b) Distribution and function of epistomatal mucilage plugs. Protoplasma 235:101-105.

[36] Zimmermann U, Räde H, Steudle E (1969) Kontinuierliche druckmessung in pflanzenzellen. Naturwissenschaften 56:634-634.

[37] Zimmermann U, Schneider H, Wegner LH, Wagner H-J, Szimtenings M, Haase A, Bentrup F-W (2002) What are the driving forces for water lifting in the xylem conduit? Physiologia Plantarum 114:327-335.

[38] Zimmermann U, Schneider H, Wegner LH, Haase A (2004) Water ascent in tall trees: does evolution of land plants rely on a highly metastable state? New Phytologist 162:575-615.

[39] Zimmermann D, Westhoff M, Zimmermann G, Gessner P, Gessner A, Wegner LH, Rokitta M, Ache P, Schneider H, Vásquez JA, Kruck W, Shirley S, Jakob P, Hedrich R, Bentrup FW, Bamberg E, Zimmermann U (2007) Foliar water supply of tall trees: evidence for mucilage-facilitated moisture uptake from the atmosphere and the impact on pressure bomb measurements. Protoplasma 232:11-34.

[40] Zimmermann D, Reuss R, Westhoff M, Gessner P, Bauer W, Bamberg E, Bentrup F-W, Zimmermann U (2008) A novel, non-invasive, online-monitoring, versatile and easy plant-based probe for measuring leaf water status. Journal of Experimental Botany 59:3157-3167.

[41] Zimmermann U, Rüger S, Shapira O, Westhoff M, Wegner LH, Reuss R, Gessner P, Zimmermann G, Israeli Y, Zhou A, Schwartz A, Bamberg E, Zimmermann D (2010) Effects of environmental parameters and irrigation on the turgor pressure of banana plants measured using the non-invasive, online monitoring leaf patch clamp pressure probe. Plant Biology 12:424-436.

[42] Zimmermann U, Bitter R, Schüttler A, Ehrenberger W, Rüger S, Bramley H, Siddique K, Arend M, Bader MKF (2013) Advanced plant-based, internet-sensor technology gives new insights into hydraulic plant functioning. Acta Horticulturae 991:313-320.

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Brasil

A non-invasive plant-based probe for continuous monitoring of water stress in real time: a new tool for irrigation scheduling and deeper insight into drought and salinity stress physiology

Abstract

Publication Dates

History