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Ionic and pH signalling from roots to shoots of flooded tomato plants in relation to stomatal closure

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Abstract

Soil flooding damages shoot systems by inhibiting root functioning. An example is the inhibition of water uptake brought about by decreased root hydraulic conductance. The extent of any resulting foliar dehydration this causes is limited by partial stomatal closure that begins within 4 h and is maintained for several days. Root to shoot signals that promote closure in flooded tomato plants have remained elusive but may include changes in solute delivery to the shoot by transpiration. Accordingly, we examined total osmolites and selected mineral ions in samples of xylem sap flowing at rates approximating whole plant transpiration. After 2.5 h flooding,delivery of total osmolites and of PO4 3-SO4 2-Ca2+K+NO3 and H+strongly decreased while Na+ remained excluded. Several hours later, deliveries of osmolites, PO4 3-, SO4 2-, Ca2+, and Na+ rose above control values, suggesting that, after approximately 10 h, root integrity became degraded and solute uptake de-regulated. Deliveries of NO3 remained below control values. Reducing or eliminating the supply of K+ to detached leaves to test the potential of decreased K+ delivery to close stomata proved negative. Decrease in H+ delivery was associated with sap alkalisation. However, raising the pH of buffer from 6.0 or 6.5 to 7.0 did not close stomata when tested in the presence of abscisic acid (ABA) at a concentration (10 μmol m−3) typical of the transpiration stream of flooded plants. It is concluded that despite their rapidity and scale, negative messages in the form of increased pH and decreased solute delivery from roots to shoots are, themselves, unlikely initiators of stomatal closure in flooded tomato plants.

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References

  • Atkinson C J, Mansfield T A and Davies W J 1990 Does calcium in xylem sap regulate stomatal conductance? New Phytol. 116, 19–27

    Google Scholar 

  • Bahrun A, Jensen C R, Asch F and Mogensen V O (2002) 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. 53, 251–263.

    Google Scholar 

  • Birner PT and Steudel E 1993 Effects of anaerobic conditions on water and solute relations and on active transport in roots of maize (Zea mays L.) Planta 190, 474–483.

    Google Scholar 

  • Blatt M R 1985 Extracellular potassium activity in attached leaves and its relation to stomatal function J. Exp. Bot 36, 240–251.

    Google Scholar 

  • Carr D J and Reid D M 1969 The physiological significance of the biosynthesis of hormones and of their export to the shoot system. In Biochemistry and Physiology of Plant Growth Substances. Eds F. Whightman and G. Setterfield. pp. 1169–1185. Runge Press, Ottawa, Canada.

    Google Scholar 

  • De Silva D L R, Cox R C, Hetherington A M and Mansfield T A 1986 The role of abscisic acid and calcium in determining the behaviour of adaxial and abaxial stomata. New Phytol. 104, 41–45

  • Drew M C and Läuchli A 1985 Oxygen-dependent exclusion of sodium ions from shoots by roots of Zea mays (cv Pioneer 3906) in relation to salinity damage. Plant Physiol. 79, 171–176.

    Google Scholar 

  • Else M A, Davies W J, Malone M and Jackson M B 1995a A negative hydraulic message from oxygen-deficient roots of tomato plants? Influence of soil flooding on leaf water potential, leaf expansion and the synchrony of stomatal conductance and root hydraulic conductivity. Plant Physiol. 109: 1017–1024.

    Google Scholar 

  • Else M A, Coupland D, Dutton L and Jackson M B 2001 Decreased root hydraulic conductivity reduces leaf water potential, initiates stomatal closure and slows leaf expansion in flooded plants of castor oil (Ricinus communis) despite diminished delivery of ABA from roots to shoots in xylem sap. Physiol. Plant. 111, 46–54.

    Google Scholar 

  • Else M A, Davies W J, Whitford P N, Hall K C and Jackson M B 1994 Concentrations of abscisic acid and other solutes in xylem sap from root systems of tomato and castor-oil plants are distorted by wounding and variable sap flow rates. J. Exp. Bot. 45, 317–324.

    Google Scholar 

  • Else M A, Hall K C, Arnold G M, Davies W J and Jackson M B 1995b. Export of abscisic acid, 1-aminocyclopopane-1-carboxylic acid, phosphate, and nitrate from roots to shoots of flooded tomato plants. Plant Physiol. 107, 377–384.

    Google Scholar 

  • Else M A, Tiekstra A E, Croker S J, Davies W J and Jackson M B 1996. Stomatal closure in flooded tomato plants involves abscisic acid and a chemically unidentified anti-transpirant in xylem sap. Plant Physiol. 112, 239–247.

    Google Scholar 

  • Everard J D and Drew MC 1989 Water relations of sunflower (Helianthus annuus L.) shoots during exposure of the root system to oxygen deficiency. J. Exp. Bot. 40, 1255–1264.

    Google Scholar 

  • Gambrell R P, Delaune R D and Patrick W H Jr 1991 Redox processes in soils following oxygen depletion. In Plant Life Under Oxygen Deprivation. Ecology, Physiology and Biochemistry. Eds. M B Jackson, D D Davies and H Lambers. pp. 101–117. SPB Academic, The Hague, The Netherlands.

    Google Scholar 

  • Gerendás J and Schurr U 1999 Physicochemical aspects of ion relations and pH regulation in plants – a quantitative approach. J. Exp. Bot. 50, 1101–1114.

    Google Scholar 

  • Hoarau J, Barthes L, Bousser A, Deléens and Prioul J-L 1996 Effect of nitrate on water transfer across roots of nitrogen pre-starved maize seedlings. Planta 200, 405–415.

    Google Scholar 

  • Jackson M B 1979 Rapid injury to peas by soil waterlogging. J. Sci. Food Agric. 30, 143–152.

    Google Scholar 

  • Jackson M B 2002 Long-distance signalling from roots to shoots assessed: the flooding story. J. Exp. Bot. 53, 175–181.

    Google Scholar 

  • Jackson M B and Hall K C 1987 Early stomatal closure in waterlogged pea plants is mediated by abscisic acid in the absence of foliar water deficits. Plant Cell Environ. 10, 121–130.

    Google Scholar 

  • Jackson MB, DaviesWJ and Else MA 1996 Pressure-flow relationships, xylem solutes and root hydraulic conductance in flooded tomato plants. Ann. Bot. 77 17–24.

    Google Scholar 

  • Kramer P J 1940 Causes of decreased absorption of water by plants in poorly aerated media. Am. J. Bot. 27, 216–220.

    Google Scholar 

  • Marschner H 1995 Mineral Nutrition of Higher Plants. Second Edition. pp. 18–30. Academic Press, London.

    Google Scholar 

  • Miller DM 1985 Studies of root function in Zea mays III. Xylem sap composition at maximum root pressure provides evidence of active transport into the xylem and a measurement of the reflection coefficient of the root. Plant Physiol 77, 162–167.

    Google Scholar 

  • Netting A G 2000 pH, abscisic acid and the integration of metabolism in plants under stressed and non-stressed conditions: cellular responses to stress and their implication for soil water relations. J. Exp. Bot. 51, 147–158.

    Google Scholar 

  • Radin J W 1984 Stomatal responses to water stress and to abscisic acid in phosphorus-deficient plants. Plant Physiol. 76, 392–394.

    Google Scholar 

  • Radin J W, Parker L L and Guinn G 1982 Water relations of cotton plants under nitrogen deficiency V. Environmental control of abscisic acid accumulation and stomatal sensitivity to abscisic acid. Plant Physiol. 70: 1066–1070.

    Google Scholar 

  • Rubio G, Rimski-Korsakov H and Laavado R S 1998 Uptake of soil mineral phosphorus and fertilizer 32P in waterlogging-tolerant plants. In Phosphorus in Plant Biology: Regulatory Roles in Molecular, Cellular, Orgasmic and Ecosystem Processes. Eds. J P Lynch and J. Deikman. pp. 338–340. American Society of Plant Physiologists, Rockville, MD, USA.

    Google Scholar 

  • Scheurwater I, Cornelissen C, Dictus F, Welschen R and Lambers H 1998 Why do fast-and slow-growing grass species differ so little in their rate of root respiration, considering the large differences in rate of growth and ion uptake? Plant Cell Environ. 21, 995–1005.

    Google Scholar 

  • Schurr U and Schulze E-D 1995 The concentration of xylem sap constituents in root exudates, and in sap from intact, transpiring castor bean plants (Ricinus communis L.). Plant Cell Environ 18: 409–420.

    Google Scholar 

  • Takei K, Sakakibara H, Taniguchi M and Sugiyama T 2001 Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol. 42: 85–93.

    Google Scholar 

  • Trought M C T and Drew M C 1981 Alleviation of injury of young wheat plants in anaerobic solution cultures in relation to the supply of nitrate and other inorganic nutrients. J. Exp. Bot. 32: 509–522.

    Google Scholar 

  • Vartapetian B B and Jackson M B 1997 Plant adaptations to anaerobiosis stress. Ann. Bot. 79 (Suppl. A), 3–20.

    Google Scholar 

  • Wilkinson S 1999 PH as a stress signal. Plant Growth Regul. 29, 87–99.

    Google Scholar 

  • Wilkinson S and Davies W J 2002 ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ. 25, 195–210.

    Google Scholar 

  • Wilkinson S, Corlett J A, Oger L and Davies W J 1998 Effects of xylem sap pH on transpiration from wild-type and flacca mutant tomato leaves: A vital role for abscisic acid in preventing excessive water loss even from well-watered plants. Plant Physiol. 117, 703–709.

    Google Scholar 

  • Wilmer C and Fricker M 1996 Stomata. Second Edition. Chapman and Hall, London, UK.

    Google Scholar 

  • Zhang J and Davies WJ 1986 Chemical and hydraulic influences on the stomata of flooded plants. J. Exp. Bot. 37, 1479–1491.

    Google Scholar 

  • Zhang J and Davies W J 1989 Sequential response of whole plant water relations to prolonged soil drying and the involvement of xylem sap abscisic acid in the regulation of stomatal behaviour of sunflower plants. New Phytol 113, 167–174.

    Google Scholar 

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Correspondence to Michael B. Jackson.

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Jackson, M.B., Saker, L.R., Crisp, C.M. et al. Ionic and pH signalling from roots to shoots of flooded tomato plants in relation to stomatal closure. Plant and Soil 253, 103–113 (2003). https://doi.org/10.1023/A:1024588532535

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