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Cucurbita Ficifolia) Seedlings Exposed to Low Root Temperatures Seong Hee Leea, Janusz J

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Cucurbita Ficifolia) Seedlings Exposed to Low Root Temperatures Seong Hee Leea, Janusz J Physiologia Plantarum 133: 354–362. 2008 Copyright ª Physiologia Plantarum 2008, ISSN 0031-9317 Light-induced transpiration alters cell water relations in figleaf gourd (Cucurbita ficifolia) seedlings exposed to low root temperatures Seong Hee Leea, Janusz J. Zwiazeka and Gap Chae Chungb,* aDepartment of Renewable Resources, 4-42 Earth Sciences Building, University of Alberta, Alberta, Canada T6G 2E3 bDivision of Plant Biotechnology, Agricultural Plant Stress Research Center, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 500-757, Korea Correspondence Water relation parameters including elastic modulus (e), half-times of water *Corresponding author, w exchange (T 1/2), hydraulic conductivity and turgor pressure (P) were e-mail: [email protected] measured in individual root cortical and cotyledon midrib cells in intact figleaf gourd (Cucurbita ficifolia) seedlings, using a cell pressure probe. Received 4 December 2007; revised 7 January 2008 Transpiration rates (E) of cotyledons were also measured using a steady-state porometer. The seedlings were exposed to low ambient (approximately 22 21 doi: 10.1111/j.1399-3054.2008.01082.x 10 mmol m s ) or high supplemental irradiance (approximately 300 mmol m22 s21 PPF density) at low (8°C) or warm (22°C) root temperatures. When exposed to low irradiance, all the water relation parameters of cortical cells remained similar at both root temperatures. The exposure of cotyledons to supplemental light at warm root temperatures, however, resulted in a two- to w three-fold increase in T 1/2 values accompanied with the reduced hydraulic conductivity in both root cortical (Lp) and cotyledon midrib cells (Lpc). Low root temperature (LRT) further reduced Lpc and E, whether it was measured under low or high irradiance levels. The reductions of Lp as the result of respective light and LRT treatments were prevented by the application of 1 mM ABA. Midrib cells required higher concentrations of ABA (2 mM) in order to prevent the reduction in Lpc. When the exposure of cotyledons to light was accompanied by LRT, however, ABA proved ineffective in reversing the inhibition of Lp. LRT combined with high irradiance triggered a drastic 10-fold reduction in water permeability of cortical and midrib cells and increased e and w T 1/2 values. Measurement of E indicated that the increased water demand by the transpiring plants was fulfilled by an increase in the apoplastic pathway as principal water flow route. The importance of water transport regulation by transpiration affecting the hydraulic conductivity of the roots is discussed. Introduction uptake, being detrimental to growth of cucumber plants Figleaf gourd is frequently used as a rootstock for a (Ahn et al. 1999a). Following the initial study (Ahn et al. chilling-sensitive cucumber plant in areas in which low 1999b), a series of studies showed that the hydraulic root temperatures (LRT) interrupt the process of water conductivity of cortical cells (Lp) of figleaf gourd roots Abbreviations – AQP, aquaporin; e, elastic modulus; E, transpiration rate; Lp, hydraulic conductivity of root cortical cells; Lpc, w hydraulic conductivity of cotyledon midrib cells; P, turgor pressure; LRT, low root temperature; T 1/2, half-times of pressure relaxation. 354 Physiol. Plant. 133, 2008 did not change significantly in response to LRT (8°C), with reduced AQP expression, the osmotic water per- unlike that of the chilling-sensitive cucumber root sys- meability of isolated protoplasts was reduced to 17- to tem (Lee and Chung 2005, Lee et al. 2004, Lee et al. 30-fold (Martre et al. 2002). This indicates that when the 2005a, 2005b). In those studies, we measured Lp of corti- cell-to-cell water flux constitutes a significant proportion cal cells using excised roots (Lee et al. 2005a, 2005b). For of the total root water flux in Arabidopsis plants, it can be the evaluation of Lp, half-times of water exchange of regulated by the activity of AQP or by the abundance of w individual cells (T 1/21/Lp) were used as a direct AQPs in cell membranes. measure of changes in hydraulic conductivity because In the present study, we hypothesized that the presence the cell elastic modulus (e) and turgor pressure (P) did not of transpiration may induce the alteration of cellular change significantly when temperature was reduced (Lee water relations in the cotyledon midrib and root cortex in et al. 2005b). intact, not excised, figleaf gourd plants and also modify However, it has been known that transpiration strongly cell responses to LRT. We investigated the changes in cell affects P in cortical cells, a process that cannot be ob- P and e because the elastic properties of cells, which are served with excised roots. In wheat and maize, for exam- the functions of turgor pressure, are as significant as the ple, radial P gradients along the cortical cells were not water permeability of the cell membrane (Steudle et al. found under the conditions of 100% relative humid- 1977). Because our previous study showed that ABA was ity, following excision, and in plants without mature an effective modulator of AQP gating (Lee et al. 2005a), leaves (Rygol et al. 1993). It is particularly interesting to we also tested this assumption again with intact figleaf note that the common features of each of these appear to gourd plants, in the presence of both LRT and high be a lack of transpiration flow across the root cortex. The irradiance. presence of such P gradients is a sharp contrast to the previous works on same species (Zhu and Steudle 1991), Materials and methods possibly because of the artificial conditions that are associated with the use of excised segments of root. Palta Plant material et al. (1987) also noticed that light-induced transpiration clearly influenced both individual cell P and the overall Seeds of the figleaf gourd (Cucurbita ficifolia Bouche´) dimensions of the taproot of sugar beet. The question, were germinated for 2–3 days at 25°C in the dark on then, arises as to the influence of stomatal conductance tap water-soaked filter paper. After germination, the seed- on the overall water relations in the root system. In lings were transferred to 5-l containers (eight seedlings addition, strong light intensifies the effect of LRT with the per container) with aerated 1/5 strength mineral solu- necrotic lesions and injuries appearing on the leaves tion (Cooper 1975). The containers were positioned in (Allen and Ort 2001, Jun et al. 2001), indicating that a growth chamber (12-h photoperiod, temperature: 25/ the sensitivity or tolerance of a plant to low temperature 22°C, PPF density: approximately 300 mmol m22 s21). may not be determined if excised roots are used as The figleaf gourd seedlings utilized in the experiments experimental materials. Changes in hydraulic conductiv- were 6–8 days old and possessed fully expanded ity of root and cells occurring in accordance with cotyledons. transpiration demand may provide an additional mech- anism for the modulation of water relations. Neverthe- Light and low root temperature treatments less, it remains unclear as to the manner in which root and leaf hydraulic conductivities are coordinated and linked The figleaf gourd plants were exposed to supplemental with transpiration. light (approximately 300 mmol m22 s21) or ambient light It has been proposed that at high rates of transpiration, (approximately 10 mmol m22 s21 PPF density) during the apoplast constitutes the principal water flow route in LRT treatment. LRT (8°C) treatment was applied with roots, and the hydraulic resistance of roots is low, thus a circulating water bath (Haake, Berlin, Germany). For facilitating rapid water uptake (Steudle and Peterson the cell pressure probe measurements, cold solution was 1998). This bulk flow is driven by hydrostatic gradients pumped through a heat exchanger in order to adjust the established by transpiration. In the roots, the vascular temperature to the desired values using a thermostat elements of the xylem function as ducts, which collect cooler. The solution temperature was controlled with water and transfer it rapidly to the shoots. On the contrary, a thermocouple, which was positioned proximally to the at low rates of transpiration, such as occur at night or roots. External medium was circulated to minimize under stress conditions, osmotic flow through aquaporins unstirred layers outside the root. The fixed root system (AQPs) may constitute the predominant pathway (Steudle was covered with paper towel to prevent the infiltration and Peterson 1998). In transformed Arabidopsis plants of light to root. The roots of intact figleaf gourd plants Physiol. Plant. 133, 2008 355 were punctured with a microcapillary tube at low (8°C) or illumination of the medium, the solution was positioned warm (22°C) temperatures, which were controlled by the far away from the light exposure. Thereafter, pressure w external thermostat. At the same time, the cotyledons relaxations were conducted in order to measure T 1/2 in were exposed to either supplemental light using a lamp both root and midrib cells. (MT 400 DL/BH; Eye, Iwasaki, Japan; and Connector PDc6, 400W, Switzerland) or laboratory ambient light. In Data analysis order to avoid the excessive heating of the leaf because of light, the lamp was positioned over overhead, and mea- The data were analyzed using paired and unpaired t-test surements of leaf temperatures with a porometer (LI-1600; to determine the effects of light and LRT. Results were LI-COR Inc., NE) confirmed that the additional light did considered statistically significantly different at P 0.05. not induce a significant increase in leaf temperature. Results Cell pressure probe and transpiration measurements Cell elasticity A cell pressure probe was employed to determine the The e of root cortical cells exposed to ambient and sup- w T 1/2, P and e of individual cortical cells in the primary plemental irradiance measured 5.1 Æ 0.3 and 5.8 Æ roots and midrib cells of the cotyledons in the intact 0.3 MPa (mean Æ SE,n¼ 14, paired t-test, P ¼ 0.23).
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