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Activation of the root xylem proton pump by hydraulic signals from leaves under suppressed transpiration

Abstract

Long term field observations have revealed that the inhibition of transpiration by heavy rainfall promotes immediate positive shift in the trans-root electric potential (TRP), indicating activation of the xylem proton pump in the tree root system presumably participating in acropetal water transport. This phenomenon is indicative of signal transmission from the aerial part to the root system via change in the xylem hydraulic pressure. To test this hypothesis, we constructed a new device that enables the simultaneous recording of artificially applied xylem hydraulic pressure and the change in the TRP of tree saplings. With the application of artificial pressure to the xylem vessels (20–62 kPa), TRP shifted towards positive potential by 20–80 mV, which indicates the activation of the proton pump in the root xylem. The reaction was observed in 11 tree species, six deciduous and five evergreen, although only during the resting phase of the xylem proton pump (May to October) when the transpiration rates were high. Contrastingly the application of tension (negative pressure) produced no reaction. Simultaneous determination of the two components of the TRP, i.e. Vps (electric membrane potential difference across root surface cell membrane) and Vpx (electric membrane potential difference between root symplast and xylem vessel), are performed using the intra-cellular micro-electrode technique throughout the four seasons. Application of excess xylem hydraulic pressure had no significant effect on Vps, while it brought about hyper-polarisation of Vpx except during the winter season, most significantly during summer when transpiration is vigorous and the xylem pump is in a resting state. Such effect of excess xylem pressure was, however, not observed under anoxia.

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Abbreviations

TRP :

Trans-root electric potential (Vps − Vpx, = Vxs)

ERG:

Electro-radicogram (chronological recording of TRP)

Vps :

Electric potential difference between the symplast and the bulk water phase surrounding the root

Vpx :

Electric potential difference between the symplast and the xylem apoplast

References

  • Blum A (2011) Plant water relations, plant stress and plant production. Plant breeding for water-limited environments. Springer, Berlin, pp 28–32

    Chapter  Google Scholar 

  • Chazen O, Neumann PM (1994) Hydraulic signals from the roots and rapid cell wall hardening in growing maize (Zea mays L.) leaves are primary responses to polyethylene glycol-induced water deficits. Plant Physiol 104:1385–1392

    CAS  Article  Google Scholar 

  • Christmann A, Weller EW, Steudle E, Gril E (2007) A hydraulic signal in root-to-shoot signaling of water shortage. Plant J 52:167–174

    CAS  Article  Google Scholar 

  • Cochard H, Bodet C, Ameglio T, Cruiziat P (2000) Cryo-scanning electron microscopy observations of vessel content during transpiration in walnut petioles. Facts or Artifacts? Plant Physiol 124:1191–1202

    CAS  Article  Google Scholar 

  • De Boer AH, Katou K, Mizuno A, Kojima H, Okamoto H (1985) The role of electrogenic xylem pumps in K+ absorption from the xylem ofVigna unguiculata: the effects of auxin and fusicoccin. Plant Cell Environ 8:579–586

    Article  Google Scholar 

  • Dodd IC, Puériolas J, Huber K, Pérez-Pérez JG, Wright HR, Blackwell MS (2015) The importance of soil drying and re-wetting in crop phytohormonal and nutritional responses to deficit irrigation. J Exp Bot 66:2239–2252

    CAS  Article  Google Scholar 

  • Fromm J (2006) Long distance electrical signaling and physiological functions in higher plants. In: Volkov AG (ed) Plant electrophysiol: theory and method. Springer, Berlin, pp 269–285

    Chapter  Google Scholar 

  • Gao J, van Kleeff PJM, Oecking C, Li KW, Erban A, Kopka J, Hincha DK, De Boer AH (2014) Light modulated activity of root alkaline/neutral invertase involves the interaction with 14-3-3 proteins. Plant J 80:785–796

    CAS  Article  Google Scholar 

  • Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483–505

    CAS  Article  Google Scholar 

  • Malone M (1993) Hydraulic signals. Trans R Soc B 341:33–39

    Article  Google Scholar 

  • Masaki N, Okamoto H (2007) Correlation between the seasonal changes in electrogenic activity across root xylem/symplast interface, sap flow rate and xylem pressure in field trees (Diospyros kaki). Trees 21:443–442

    Article  Google Scholar 

  • Masaki N, Okamoto H (2009) Demonstration of the root surface electrogenic ion pump activity revealed from the seasonal inversion in the phase relation between electro-radicogram and the diurnal oscillation of air temperature in a field tree (Diospyros kaki). Trees 23:473–478

    Article  Google Scholar 

  • Mizuno A, Kojima H, Katou K, Okamoto H (1985) The electrogenic ion pumping from parenchyma symplast into xylem-direct demonstration by xylem perfusion. Plant Cell Environ 8:525–529

    Article  Google Scholar 

  • Nobel PS (1974) Introduction to biophysical plant physiology. W.H. Freeman and Co., San Francisco

    Google Scholar 

  • Okamoto H (2010) Studies on the physiological root activity of a persimmon tree for 15 years. Root Res 19:103–115

    Google Scholar 

  • Okamoto H, Katou K (1988) Demonstration of respiration-dependent water uptake and turgor generation in Vigna hypocotyl. Plant Cell Physiol 29:509–515

    CAS  Google Scholar 

  • Okamoto H, Masaki N (1999) Long term measurement of the trans-root electric potential in a persimmon tree in the field. J Plant Res 112:123–130

    Article  Google Scholar 

  • Okamoto H, Masaki N (2013) A new method to explore the effects of change in xylem pressure on the root function. Root Res 22:75–80

    Article  Google Scholar 

  • Okamoto H, Ichino K, Katou K (1978) Radial electrogenic activity in the stem of Vigna sesquipedalis: involvement of spatially separate pumps. Plant Cell Environ 1:279–284

    Article  Google Scholar 

  • Okamoto H, Mizno A, Katou K, Ono Y, Matsumura Y, Kojima H (1984) A new method in growth electro-physiology: pressurized intra-organ perfusion. Plant Cell Environ 7:139–147

    Article  Google Scholar 

  • Okamoto H, Liu Q, Nakahori K, Katou K (1989) A pressure jump method as a new tool in growth physiology for monitoring physiological extensibility and effective turgor. Plant Cell Physiol 30:979–985

    Google Scholar 

  • Shimmen T (2003) Studies on mechanoperception in the Characeae: transduction of pressure signals into electrical signals. Plant Cell Physiol 44:1215–1224

    CAS  Article  Google Scholar 

  • Smith H (1982) Light piping in plant tissues. Nature 298:423–424

    Article  Google Scholar 

  • Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788

    CAS  Google Scholar 

  • Sukhov V, Sherstneva O, Surova L, Katicheva L, Vodeneev V (2014) Proton cellular influx as a possible mechanism of variation potential influence on photosynthesis in pea. Plant Cell Environ 37:2532–2541

    CAS  Article  Google Scholar 

  • Taura T, Iwaikawa Y, Furumoto M, Katou K (1988) A model for radial water transport across plant roots. Protoplasma 144:170–179

    Article  Google Scholar 

  • Volkov AG, Brown CL (2006) Electrochemistry of plant life. In: Volkov AG (ed) Plant electrophysiology, theory and methods. Springer, Berlin, pp 437–459

    Chapter  Google Scholar 

  • Volkov AG, Collins DJ, Mwesigwa J (2006) Plant electrophysiology: pentachlorophenol induces fast action potentials in soybean. Plant Sci 153:185–190

    Article  Google Scholar 

  • Wegner LH (2014) Root pressure and beyond: energetically uphill water transport into xylem vessels? J Exp Bot 65:381–393

    CAS  Article  Google Scholar 

  • Zeuten T (2010) Water-transporting proteins. J Membr Biol 234:57–73

    Article  Google Scholar 

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Acknowledgements

Authors are very much obliged to Prof. Dr. Wolfram and Cornelia Ullrich in TU Darmstadt, Germany, for their critical reading and improvement of this manuscript. At the same time, authors are indebted to Prof. S. Okamura in Department of Electronic Engineering, Shizuoka University, for construction of the differential amplifier. They also express their gratitude to Professor T. Kinoshita and Dr. K. Takahashi in Nagoya University for their generous lending of a micro-electrode-puller long term. We also thank Ms. Y. Okamoto, for her help during this research as an able secretory of our laboratory.

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Correspondence to Hisashi Okamoto.

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Okamoto, H., Kitamura, S. & Masaki, N. Activation of the root xylem proton pump by hydraulic signals from leaves under suppressed transpiration. J Plant Res 135, 311–322 (2022). https://doi.org/10.1007/s10265-022-01368-x

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Keywords

  • Acropetal water transport
  • Hydraulic signal transmission
  • Pressure-sensitive xylem proton pump
  • Transpiration
  • Trans-root electric potential
  • Xylem pressure