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Xylem tension affects growth-induced water potential and daily elongation of maize leaves

Xylem tension affects growth-induced water potential and daily elongation of maize leaves Abstract Diurnal rates of leaf elongation vary in maize (Zea mays L.) and are characterized by a decline each afternoon. The cause of the afternoon decline was investigated. When the atmospheric environment was held constant in a controlled environment, and water and nutrients were adequately supplied to the soil or the roots in solution, the decline persisted and indicated that the cause was internal. Inside the plants, xylem fluxes of water and solutes were essentially constant during the day. However, the forces moving these components changed. Tensions rose in the xylem, and gradients of growth-induced water potentials decreased in the surrounding growing tissues of the leaf. These potentials, measured with isopiestic thermocouple psychrometry, changed because the roots became less conductive to water as the day progressed. The increased tensions were reversed by applying pressure to the soil/root system, which rehydrated the leaf. Afternoon elongation immediately recovered to rapid morning rates. The rapid morning rates did not respond to soil/root pressurization. It was concluded that increased xylem tension in the afternoon diminished the gradients in growth-induced water potential and thus inhibited elongation. Because increased tensions cause a similar but larger inhibition of elongation if maize dehydrates, these hydraulics are crucial for shaping the growth-induced water potential and thus the rates of leaf elongation in maize over the entire spectrum of water availability. Potential field, potential gradient, transpiration, osmotic potential, turgor, Zea mays L Introduction Maize leaves elongate at varying rates during the day, in part, because the natural environment varies. But when the environment is held constant with an abundant supply of water and nutrients, much of the variation remains. Leaf elongation is rapid early in the day and declines as the day progresses. Because this behaviour inhibits the overall growth of the leaf and has not been explained, this study was undertaken to investigate its causes. The approach was to determine whether the causes were outside or inside the plant. External causes could result from gradients in soil water or nutrients adjacent to the root surface that develop during the day (Nye and Tinker, 1977; Milligan and Dale, 1988; Stirzaker and Passioura, 1996) or from gradual changes in soil temperature (Ben-Haj-Salah and Tardieu, 1995; Watts, 1974). Other factors such as humidity or wind speed could be important (Loomis, 1934; Christ, 1978a, b; Cutler et al., 1980; Salah and Tardieu, 1996, 1997). On the other hand, internal factors could involve diurnal patterns of uptake and delivery of water and nutrients to the leaf (Fricke et al., 1997; Fricke, 2002b) or changes in growth-induced water potentials associated with changes in diurnal transpiration rates (Westgate and Boyer, 1984, 1985; Boyer, 1985, 1988; Fricke and Flowers, 1998; Martre et al., 1999; Fricke, 2002a; Boyer and Silk, 2004). Resistances to water flow in the vascular tissues can vary diurnally (Passioura and Munns, 1984; McCully, 1999), and biochemical or hormonal signals could change between roots and shoots as the day progresses (Davies and Zhang, 1991). In the following work, each of these variables was systematically tested in order to identify causative ones. Once a candidate was identified, the variable was eliminated or reversed, and the effect on leaf elongation was used to accept or reject the candidate. Materials and methods Plant materials Maize seeds (Zea mays L. cv. B73×Mo17, Illinois Foundation Seeds, Inc., Champaign, IL) were germinated between two sheets of paper towels wetted with nutrient solution at 29 °C in the dark. The nutrient solution was 12 mol m−3 Ca(NO3)2, 8 mol m−3 KNO3, 4 mol m−3 KH2PO4, 4 mol m−3 MgSO4, 50 mmol m−3 H3BO3, 20 mmol m−3 MnSO4, 4 mmol m−3 ZnSO4, 1 mmol m−3 CuSO4, 1 mmol m−3 H2MoO4, and 250 mmol m−3 Fe-citrate (modified Hoagland's solution; Hoagland and Arnon, 1950). On the third day, the seedlings were transferred individually to Plexiglas pots of a size that fit a pressure chamber (6 cm inner diameter, 23 cm depth) with holes for drainage. Each pot was filled with a 1:1:1 (by vol.) mix of soil, peat moss, and vermiculite at pH 6.5. The pot was covered with a pressure chamber top through which the coleoptile emerged. The seedlings continued to grow in darkness until the mesocotyl passed through the opening in the top. The plant and the pot, with top, were then transferred to a controlled environment chamber (Environmental Growth Chambers, Ohio, USA) with day/night temperatures of 25/20 °C, relative humidity of 60/90%, and 14 h of photosynthetically active radiation of 700–800 μmol m−2 s−1. Nutrients were supplied two to three times a week by filling the whole pot from the bottom upward, then draining away the excess. Because the pot was covered with the pressure chamber top, the nodal roots developing above the mesocotyl were prevented from entering the soil. In some experiments, the maize plants were grown as described above except (i) the night temperature was at 25 °C for one night instead of decreasing to 20 °C, or (ii) a single plant was developed in a bigger pot (15 cm diameter and 16 cm depth) with nodal roots growing into the same soil mix, or (iii) a plant was grown in nutrient culture without the soil. For the soil-less treatment, the dark-grown seedling was transferred to a container (10.3 cm inner diameter, 26 cm depth) filled with aerated nutrient solution as above. The container was covered with a pressure chamber top through which the coleoptile and mesocotyl passed through the opening in the top. The nodal roots did not enter the nutrient solution. Leaf elongation After leaf 5 emerged around 11 d after planting, the soil/root system of the maize plant was sealed inside the pressure chamber (7.6 cm inner diameter, 26.7 cm depth, as shown in Fig. 1 of Tang and Boyer, 2003) and the total leaf elongation was continually monitored in the environment where the plants were grown (as shown in Fig. 1 of Tang and Boyer, 2003). A fine Kevlar thread was attached to the mature portion of the leaf, and elongation was detected by an optical incremental encoder (25G, Sequential Information Systems Inc., New York, USA) that recorded motion by rotating as the leaf elongated. The encoder was unaffected by temperature or supply voltage. At 2 s intervals, the data were sent to a datalogger (CR7, Campbell Scientific, Inc. Utah, USA) which stored them as a 1 min average of total accumulated counts during the minute and converted the counts to the elongation rate. The rate was downloaded to a computer for plotting. Fig. 1. Open in new tabDownload slide Elongation of maize leaf 5 when the plant was supplied with adequate water and nutrients. (A) Length of leaf. (B) Elongation rate of leaf. The open and filled bars on the X-axis represent daytime and night-time, respectively. Root pressurization (P) In certain experiments, the soil/root system was placed in the pressure chamber and was pressurized with compressed air until guttation formed along the leaf edges while leaf elongation was continuously monitored with the encoder. This system was similar to that used by Janes and Gee (1973), Nulsen et al. (1977), Passioura and Munns (1984), Saliendra et al. (1995), and Hsiao et al. (1998), but a controller (DP25-E Process Meter, Omega Engineering Inc, Stamford, Connecticut, USA) connected to a pressure transducer (PG856–250, Statham Laboratories Inc., Puerto Rico) was set to regulate the applied pressure (P) to maintain guttation (set-up shown in Fig. 1 of Tang and Boyer, 2003). Ψw profile The profile of Ψw and its components was determined from the soil to the tip of leaf 5. After excising the shoot inside the controlled environment chamber, the shoot was immediately transferred to a humidity-saturated glove box in low light. Four 2 cm samples of leaf tissue were taken along the length of leaf 5 (counted from the base of the plant), starting at the mature tip and moving toward the growing base. The basal tissues were sampled after dissecting them from the surrounding leaf bases. The samples were rapidly transferred individually into four psychrometer cups coated with petrolatum and sealed into an isopiestic thermocouple psychrometer (Isopiestics Company, Lewes, DE), a method having the advantage that the leaf epidermis had no effect on the measurements. The pot was moved to a humidity-saturated room, and the soil was sampled at a 4 cm depth inside the pot. The whole soil/root medium was carefully detached from the pot, and one mature primary root of 10 cm with attached branches was sampled after flicking away the soil and removing the root tips. The Ψw was first determined according to Boyer (1995). The leaf and root samples were then frozen and thawed in the sealed cup, and the osmotic potential (Ψs) was measured by the same technique. Turgor pressure (Ψp) was calculated from Ψw–Ψs. A profile of leaf Ψw or its components was then constructed as a function of distance above the soil surface. In some experiments, the Ψw profile was measured in shoots whose soil/root system was exposed to P in the pressure chamber. The shoots were sampled for measurement of the water potential (Ψw) and its components, as described above, while the soil/root system was still exposed to P. No root or soil was sampled because the soil/root system was enclosed in the chamber and held at P during the sampling time. Guttation and exudate Ψs The appearance of guttation fluid was determined along the length of leaf 5 and samples were collected in a microlitre syringe. In some plants, the shoot was excised above the soil and the initial 10 mm3 of exudate was sampled from the mesocotyl stump after the cut surface was rinsed and blotted dry. The Ψs was determined isopiestically on samples with a volume of 3–5 mm3 as described by Boyer (1995). Transpiration and exudation rates Transpiration rates were determined by weighing the whole apparatus (Fig. 1 in Tang and Boyer, 2003) in the controlled environment chamber where the plants were grown, while leaf 5 elongation was simultaneously monitored with the encoder. The weight was recorded every 10 s and stored in a computer. The sum of six successive measurements gave the weight min−1. Transpiration was calculated as weight change min−1, given as running averages for the previous 10 min. For plants with P applied to the soil/root system, the same process was used by applying P until guttation began to appear. While transpiration represented the water loss from the shoot, water entering the shoot from the root system was estimated from the exudation of an excised mesocotyl of a separate plant grown identically. Leaf 5 of the separate plant elongated at a rate close to the pressurized one. The soil/root system was exposed to the same P in both plants. After excision, the cut mesocotyl surface was rinsed with water and blotted dry, and the exudate was collected every minute for the first 5 min, and every 5–10 min thereafter. The volume collected over 2 h was used to calculate the exudation rate. Conductance of the soil/root system The exudate measured as above first appeared on the cut mesocotyl surface when P balanced Ψw of the soil (i.e., P= –Ψw of soil). Raising P above this balanced condition created a total potential difference that drove water out of the mesocotyl surface at a rate determined by the conductance of the soil/root system. Because the Ψw of the soil was known from measurements with the psychrometer, and P was known, the conductance of the soil/root system could be calculated according to: (1) where e was the exudation rate from the cut surface of the mesocotyl stump of the soil/root system after the shoot was removed (mm3 s−1) and k was the conductance of the soil/root system (mm3 s−1 MPa−1). Results Leaf 5 emerged from the enclosing sheaths of the older leaves 11 d after planting (Fig. 1A). The leaf elongated rapidly during the day but slowly at night (Fig. 1B). As the lamina unrolled and became increasingly exposed, elongation displayed a prominent and sudden downward spike at the beginning of the day and upward spike at the end of the day (Fig. 1B). A few min after each spike, elongation became more stable. However, during the day, the stable elongation always was more rapid in the morning than in the afternoon (Fig. 1B). At night, the reverse occurred and there often was a noticeable increase in the rate as the night progressed (Fig. 1B, days 11–17). The temperature was stable during the day and night, but cooler at night (see Fig. 3E below). If the temperature was the same during day and night, i.e. 25 °C, elongation began at night at the same rate as at the end of the day (0.65–0.75 μm s−1 at 25 °C) instead of becoming slower (0.55 μm s−1 at 20 °C) (Fig. 2). Low night-time temperature was thus responsible for the slower night-time elongation in Fig. 1. These features continued for most of the growth period ending on day 22 (Fig. 1). Fig. 2. Open in new tabDownload slide Elongation of maize leaf 5 when temperature is the same during day and night. Temperature and relative humidity are shown at the top of the figure. Data are from a single plant 16 d after planting, which was one of four replicate plants all of which gave the same result. Fig. 3. Open in new tabDownload slide Elongation of maize leaf 5 when soil conditions were varied. (A) Plant grown in a large pot of soil in which nodal roots developed or (B) grown in aerated nutrient solution. The measurements were made on leaf 5 on day 16 after planting. (C) Elongation of a mature leaf 5 on day 22 after planting. Each of the maize graphs is from a single plant among 3–5 replicate plants. (D) Elongation of a metal rod instead of a leaf. (E) Air temperature for these experiments. Availability of water and nutrients to the roots The daytime loss in elongation rate was so persistent that its origins were investigated by varying the supply of water and nutrients to the root surfaces. Figures 1 and 2 used a small pot from which nodal roots were excluded. If, instead, the plants grew in a soil volume four times that in Figs 1 and 2, nodal roots extended into the soil and 30% more root dry mass developed, but leaf 5 continued to show the same pattern of decreased elongation in the afternoon (Fig. 3A). Plants growing without soil in a nutrient culture also displayed this pattern (Fig. 3B). The effect could not be attributed to salt accumulation on or in the root because the pattern persisted when plants were grown in half-strength nutrient solution or transferred to a water-only medium for one day (data not shown, but appeared as in Fig. 3B). The pattern was not an artefact of measurement because mature leaves showed no diurnal change in dimensions (Fig. 3C). A metal rod in place of the shoot showed zero elongation (Fig. 3D) except for a slight thermal expansion/contraction during the first 2 h after the temperature changed in the controlled environment (Fig. 3E). Flux of water and nutrients to the shoot Because the elongation pattern persisted under these varied external conditions, important internal conditions were investigated. At night, guttation occurred (Fig. 4A) and transpiration was near zero (Fig. 4B). During the day, guttation ceased as transpiration became rapid. The transpiration was steady throughout the day (Fig. 4B). Fig. 4. Open in new tabDownload slide Diurnal delivery of water and solute to the maize shoot. (A) Leaf guttation shown as a percentage of the vein ends displaying a droplet on leaf 5. (B) Transpiration of the whole shoot. Data are for day 16 after planting and are representative of a single plant among five replicate plants. (C) Soil water potential (triangles), exudate osmotic potential at the leaf base (squares), and guttate osmotic potential for the leaf edge (circles). Guttate during the day was obtained by applying P to the soil/root system. Exudate was obtained similarly from the mesocotyl stump after detopping. Data are averages for three plants with standard deviations smaller than the symbols. (D) Solute flux from root to shoot calculated as the product of the transpiration rate (from B) and exudate concentration (from C). Solutes in the transpiration stream followed this flow of water. At night, the xylem solution entering the base of the shoot (measured as Exudate, Fig. 4C) had a Ψs of –0.28 MPa, which was lower than the Ψw of the soil, presumably because salts were being loaded into the xylem by the root. During the day while transpiration was rapid, the xylem solution was diluted by the entering water, and Ψs at the base of the shoot rose to –0.1 MPa, or about the level of Ψw in the soil. By the time the transpiration stream passed the base of the shoot and reached the exposed leaf blade, its Ψs was zero, determined from the guttation fluid collected at the leaf edges after the root was pressurized (Fig. 4C). This indicated that the shoot removed essentially all the solute from the transpiration stream. The solute flux to the shoot was much greater during the day than at night (Fig. 4D), but remained nearly steady throughout the day. Ψw profiles The inability of the internal water and solute fluxes to explain the downturn in daily elongation suggested that other internal factors might have varied. A central factor would be the force needed to move water and solute in the xylem, essentially the water potential (Ψw) and its components (Kramer and Boyer, 1995). These forces were measured first when leaf 5 displayed the usual slower rate of elongation at night (Fig. 5A). At this time, Ψw of the exposed blade was –0.13 to –0.15 MPa and nearly in equilibrium with Ψw of the soil (Fig. 5B, compare Ma, Mb, Mc with S). The leaf and soil were thus very hydrated. Because the mature part of the leaf was connected to the potential of the soil mostly through the xylem, the xylem in the leaf base was also hydrated and essentially the same as in the soil (X in Fig. 5B). Fig. 5. Open in new tabDownload slide Elongation (A) and water potential (Ψw) profiles (B–E) of leaf 5 at various times during the day. At the time indicated by the arrows, samples for Ψw were taken from the soil (S), mature root (R), elongating region of leaf 5 (G), and mature regions of leaf 5 (Ma, Mb, and Mc). Because solute is virtually absent in guttation fluid (see Fig. 4C), Ma, Mb, and Mc mostly reflect xylem tension. The vertical dashed line indicates Ψw in the xylem (X) in the elongation region. Growth-induced water potential is (X–G), shown by the shaded area. The leaf base between 0 and 10 cm contained the growing region, from Tang and Boyer (2002). Elongation rate was from a single plant while the Ψw profile was the average ±1 SD for three plants on day 16 after planting. Most SD were smaller than the symbols. The solid bar on the abscissa indicates the dark period. By contrast, the Ψw of the leaf base was –0.48 MPa at night (G in Fig. 5B). This region contains the elongating tissues (basal 10 cm; see Tang and Boyer, 2002). Therefore, a growth-induced Ψw (X–G) of about 0.35 MPa was present in the growing tissues outside of the xylem in the leaf base (Fig. 5B). The Ψw of the root (R) was lower than in the mature leaf perhaps because solute was being deposited in the root xylem, as pointed out above. The solutes would cause pressure to develop in the xylem. The pressure Ψpx was calculated from (2) where Ψwx was the water potential of the xylem in the leaf base (X in Fig. 5B) and Ψsx was the osmotic potential of the xylem in the leaf base (Exudate in Fig. 4C). Accordingly, the root pressure at the leaf base was 0.15 MPa = –0.14 – (–0.29). This positive root pressure probably caused guttation by the leaf at night. The day began with a downward spike in leaf elongation that recovered to a stable but rapid rate (1.3 μm s−1, Fig. 5A) about double that at night (0.65 μm s−1). The Ψw in the mature part of the leaf was more negative than that at night, reflecting tension that had increased as the day began (Ma, Mb, and Mc in Fig. 5C compare with Fig. 5B). The tension at the leaf base was calculated from Equation 2 to be –0.3 MPa (xylem Ψw of –0.4 MPa from Fig. 5C minus xylem Ψs of –0.1 MPa from Fig. 4C). Leaf elongation was thus nearing its maximum with this tension. G was –0.5 MPa, which was slightly lower than at night, but (X–G) could not be calculated because elongation was accelerating, and the calculation required stable rates for the preceding 2 h. As the day progressed, the mature part of the leaf developed Ψw of –0.5 to –0.65 MPa (Fig. 5D), which indicated that tensions were –0.4 to –0.55 MPa (Equation 2), or substantially greater than the tension seen earlier in the day. The build-up of tension was associated with a decrease in leaf elongation to 0.85 μm s−1. With this stable rate, G had fallen to –0.7 MPa while X had moved to –0.5 MPa, giving a small growth-induced Ψw between xylem and growing tissues (X–G) of about 0.2 MPa (Fig. 5D). When night returned and transpiration decreased (Fig. 4B), the potentials began to return to their earlier night-time levels (Fig. 5E). With the release of tension, there was an upward spike in elongation and the rates then settled at the slow but gradually increasing night-time rate (Fig. 5A). Thus completed the 24 h cycle of elongation and forces moving water and xylem solutes through the plant. Tests of tension mechanism These results indicated that, despite stable water and nutrient flows during the day, the xylem tensions driving the flows were becoming larger as the day progressed while leaf elongation was declining. The correlation between increasing tension and decreasing elongation suggests that the tensions may have affected elongation. If this hypothesis is correct, leaf elongation would increase if the tensions were relieved. In order to test the hypothesis, P was applied to the soil/root system to relieve the tension. Relief of tension was detected when guttation appeared at the edges of the elongating leaf. When P was applied in the morning, leaf elongation immediately spiked upward as if tension had been relieved, but the later stable rate was the same as in the absence of P (Fig. 6B compare with Fig. 6A). When P was released, the rate spiked downward as though tension had reformed, and then settled at the rate for the rest of the day. By contrast, if this treatment was applied at the end of the day, the same spikes occurred, but the settled rate was much faster than had been occurring without P (Fig. 6C compare with Fig. 6A). The afternoon inhibition of elongation was eliminated. As a control, a mature leaf displayed only small spikes when P was applied, and there was no other elongation response (Fig. 6D). Fig. 6. Open in new tabDownload slide Elongation of leaf 5 when xylem tension was relieved by applying P to the soil/root system until guttation was observed. (A) Without P. (B) With P applied and released in the early morning. (C) As in (B) but in the late afternoon. These measurements were on day 16 after planting. (D) As in (B) but for a mature leaf with P applied and released in the morning as well as the afternoon at 27 d after planting. Dashed lines in (B) and (C) show the elongation expected without P, as in (A). Each graph is for a single plant among 2–4 replicate plants. It should be noted that P required to relieve tension was larger late in the day (Fig. 6C) than early in the day (Fig. 6B), confirming that tensions became larger as the day progressed. These changes in tension were detected in the Ψw profiles. In plants showing the growth response of Fig. 6 (Fig. 7A, E), but sampled for the Ψw profile (Fig. 7B, F), the whole shoot profile shifted to a wetter status when P was applied to the soil/root system. The applied P were higher late in the day (Fig. 7E) than early in the day (Fig. 7A), and the shift was correspondingly larger late in the day (Fig. 7F) than early in the day (Fig. 7B). Because of the rapid nature of the P treatments, steady conditions were not present and (X–G) could not be determined. But the Ψs of the shoot tissues became more negative during the day as solute accumulated (Fig. 7C, G). P applied to the soil/root system had little effect on Ψs except in the basal tissues, which became less negative especially late in the day. The turgor increased in the mature tissues, which confirmed that tension had been relieved and the tissues had rehydrated (Fig. 7D, H). However, the basal growing tissues had constant turgor throughout the day and when P was applied. Fig. 7. Open in new tabDownload slide Elongation and potential profiles for leaf 5 when tension was relieved by applying P to the soil/root system. (A, E) Elongation rate early and late on day 16, respectively. Maximal rate (max) refers to the highest rate in the morning. Dashed line shows the elongation rate without P as in Fig. 6A. Elongation trace ends when shoot was removed to measure potential profiles. Profiles of water potential (B, F), osmotic potential (C, G), and turgor (D, H) before (open symbols) and after P was applied (closed symbols). Profiles after P was applied (B–D and F–H, closed symbols) were measured at the end of the traces in (A) and (E), in the same but single plants. They are compared to profiles measured in different plants at the same time but without P, presented as means ±SD (n=3). SD was sometimes too small to be seen behind the data point. See Fig. 5B for definitions of Mc, Mb, Ma, G, R, and S. If P relieved tension by forcing more water through the soil/root system, the flow should be detectable in a detopped plant. After detopping during daytime conditions, no exudation occurred from the soil/root system unless P was applied. With P applied sufficiently to cause guttation in the intact plant in the afternoon, leaf elongation became much faster (Fig. 8A) and transpiration slightly faster (Fig. 8B) in the same plant. The slight increase in transpiration was probably caused by direct evaporation when the guttation droplets appeared on the leaf edges. After detopping a separate plant elongating at a similar rate, the same P caused exudation from the soil/root system in excess of that necessary for transpiration (e in Fig. 8B). Similarly, in the early morning, the flow with P exceeded transpiration (data not shown). However, because of greater tension in the afternoon than in the morning, the P in the afternoon was about twice that in the morning, as shown in Fig. 7A and E. The exudation rate was similar for both times, indicating that the conductance of the soil/root system had decreased as the day progressed. The conductance in mid-morning was 11.03 and in late afternoon was 6.06±0.76 mm3 s−1 MPa−1 (1 SD, n=5), calculated from Equation 1. The decrease in soil/root conductance was attributable to the root because the soil remained hydrated with stable Ψw throughout the day (Fig. 4C). Fig. 8. Open in new tabDownload slide Elongation of leaf 5 (A) and transpiration and exudation (B) when P was applied to the soil/root system during the afternoon. Max in (A) shows the maximal rate in the morning. Dashed line indicates the elongation rate typical for late afternoon without P as in Fig. 6A. With P, leaf 5 guttated. Transpiration in (B) is for the plant in (A). e in (B) is for a plant like that in (A) with the same P but detopped (cross-hatched). Exudate appeared on the stump after P was applied. Data are typical for day 16 after planting, repeated four times with exudation measured twice. Discussion This study is a sequel to earlier work from this laboratory that was done with dehydrating maize (Tang and Boyer, 2002, 2003). In the present work, the maize was hydrated and leaf elongation decreased in the afternoon because xylem water came under increasing tension. Despite abundant water in the soil, the roots became less conductive to water and required greater tensions to maintain water and solute flows to the shoot. In the earlier studies of Tang and Boyer (2002, 2003), increasing tensions also inhibited leaf elongation and were caused by losses in conductance. Therefore, xylem tension was a central issue for the growth process. Its central activity in all three studies indicates that tension affects growth across the entire spectrum of soil water availability. The control by xylem tension was unequivocally demonstrated in the present work when the soil/root system was pressurized to relieve the tension. With guttation as the indicator of relief, elongation immediately responded with an initial upward spike in rate. After the spike, the leaf elongated rapidly, and the afternoon inhibition was eliminated. A similar P treatment in the early morning generated the spike but did not alter the following rate because the tensions were already small and elongation was at its maximum. The rapidity of these responses eliminates root-sourced hormonal or biochemical signals as a form of control, despite the importance of these processes over the long term (Cleland, 1971; Taiz, 1984; Passioura, 1988; Davies and Zhang, 1991). Root-sourced hydraulic signals appear to control the extensibility of cell walls in shoot growing regions (Davies and Zhang, 1991) and thus create the conditions allowing growth-induced Ψw to develop. These types of signals require considerable time to affect the shoot, as shown by Passioura (1988). Pressure was applied to the root system continually and leaf growth was compared with that in unpressurized controls as the soil dehydrated (Passioura, 1988). Differences appeared after a few days suggesting that a day or two may be required before root-sourced chemical signals change growth patterns. Munns et al. (2000b) also point out that time scales of hours or days may give different results. The importance of hydraulic signals in the short term was noted by Salah and Tardieu (1997), Hsiao et al. (1998), and Bouchabke et al. (2006) using slightly dehydrated maize. A tension mechanism may have been operating in their experiments. A tension mechanism may also explain the findings of Koch et al. (2004), who investigated mature leaf sizes at various positions in Sequoia sempervirens. Because of the great tree height, there is a standing gradient of tension caused by gravity, with leaves at the top subjected to greater tension than those at the bottom. Koch et al. (2004) report that the upper leaves were smaller than those at the bottom, in agreement with the present findings that increased xylem tension can diminish leaf growth. It should be noted that changes in turgor did not account for the afternoon inhibition of leaf elongation. Turgor in the elongating tissues did not vary during the day nor when tension was relieved in the xylem. Turgor was maintained by changes in Ψs. It appears that sufficient solute was delivered to the elongating cells to maintain their turgor throughout the day. Mechanism of tension action But why should xylem tension have such a large effect on leaf growth and so little effect on transpiration? Both processes draw on water in the xylem. Abundant water passes right through the growing leaf base and is used for rapid transpiration in the mature blade. The amount of water moving through the xylem in the leaf base is certainly sufficient for the growth of the leaf, because leaf 5 uses only 2% of this water for its growth, as shown by Tang and Boyer (2002). On the other hand, the tension at the leaf base is the initial part of a water potential field, i.e. a dynamic three-dimensional gradient that slopes radially downward into the surrounding tissues (Tang and Boyer, 2002). Each protoxylem vessel is surrounded by one of these fields (Fig. 10 in Tang and Boyer, 2002, shows the likely three-dimensional form). The downward slope moves water out of the protoxylem and into the growing cells. Because the tension in the xylem is part of this potential field, an increased tension decreases the water potential next to the xylem and inverts the initial slope of the field. The inverted shape prevents water from leaving the xylem. The effect is immediate, shown for maize leaves by Tang and Boyer (2003) and soybean stems by Nonami et al. (1997) and Passioura and Boyer (2003). The immediacy was observed in the present work by the elongation spikes followed by steady but changed elongation after pressurization. The response of the entire growing region means that a local change in the field affects growth of the whole tissue. The whole tissue responded because all the cells depended on water extraction from the xylem. Consequently, this mechanism appears to be the growth-controlling feature of this study. The presence of the field was indicated by the growth-induced water potential (X–G) in the growing tissues at the leaf base, using psychrometer measurements. The psychrometer determined the potential in the xylem (X) and average potential of the surrounding, growing tissues (G). A similar field in three dimensions was measured by Nonami and Boyer (1993) from cell measurements with a pressure probe and picolitre osmometer in the growing region of soybean hypocotyls. The measurements agreed well with the tissue level measurements with the psychrometer (Nonami and Boyer, 1993; Nonami et al., 1997). (X–G) developed because the small cells of the enlarging tissues imposed many wall/membrane barriers to flow (Tang and Boyer, 2002). Their cumulative frictional resistance prevented water from entering the growing cells rapidly. As a consequence, the yielding of the cell walls ran ahead of water entry and prevented turgor from becoming as high as it otherwise would. This effect, shown experimentally by Boyer (2001) in soybean hypocotyls, caused the low water potentials (G) necessary for (X–G) to form. As can be seen in Fig. 9 (Late Morning), (X–G) was large after several hours of rapid steady elongation in the morning, as reported in Fig. 4B of Tang and Boyer (2002). By comparison, the present study shows that (X–G) became small after several hours of steady elongation in late afternoon (Fig. 9; Late Afternoon). Therefore, the increased xylem tension diminished the potential field as the day progressed. These potentials were not generated by relaxation after excision, as was claimed (Cosgrove et al., 1984). The potentials exist in completely intact plants (Boyer, 1968; Boyer et al., 1985) including maize (Westgate and Boyer, 1984; Tang and Boyer, 2002), and excision effects are small (Westgate and Boyer, 1984; Tang and Boyer, 2002). Nor were they caused by solute in the apoplast (Cosgrove and Cleland, 1983), because solute concentrations were low (Nonami and Boyer, 1987). In the present study, the solute concentration in the guttation fluid was zero and in xylem at the leaf base was equivalent to Ψs of only –0.1 MPa. Such low apoplast concentrations contributed little to G of –0.5 to –0.7 MPa. Tensions thus dominated in the apoplast. It follows that, as the day progressed, an increase in xylem tension would diminish (X–G) as shown diagrammatically in Fig. 10 (black cells; Late Morning compared to Late Afternoon). If (X–G) became smaller, less water would be taken up from the xylem and less elongation would occur when compared to the morning rates. Fig. 9. Open in new tabDownload slide Water potential profiles during Late Morning and Late Afternoon in maize leaf 5. Elongation had been steady for 2 h before these measurements were made. Data are means for three plants from Fig. 5D (closed symbols) or individual measurements for one plant reported by Tang and Boyer (2002) (open symbols). Fig. 10. Open in new tabDownload slide Diagram of tension in the water transport pathway from soil through the root to the leaf where the path splits to enter the elongating region for growth (black cells) or the mature blade for transpiration (open cells). On the left is the position in the plant, and on the right are simplified diagrams of the tension gradient in the xylem (dashed line) and apoplast of the elongating tissues (black). Note that the water potential in the xylem in the elongating region (X) is the start of the water potential gradient in the elongating tissues (X–G). Although (X–G) is a water potential generated inside the growing cells, it is mostly tension in the apoplast. Because (X) is part of (X–G), changes in (X) between the morning and afternoon may change (X–G) as shown (Late Morning versus Late Afternoon). For a three-dimensional shape of (X–G), see Fig. 10 in Tang and Boyer (2002). Labels on the tension diagram correspond to psychrometer measurements in this study, defined in Fig. 5B. Transpiration, on the other hand, was not altered by the tension build-up. The tension was insufficient to close stomata, which would have inhibited transpiration. The vapour pressure of the evaporating water would decrease slightly with increasing tensions, but for a tension increase of 0.15 MPa from Fig. 5, the vapour pressure would decrease only 0.11%, calculated from: (3) where ΔΨw is the change in tension (MPa), R is the gas constant (L MPa mol−1 K−1), T is the temperature (K), Vw is the partial molal volume of water (L mol−1), p is the vapour pressure and subscripts w and o are the water under the new tension and the original tension, respectively. The 0.11% change in vapour pressure was detected with the thermocouple psychrometer as part of the water potential measurements but was too small to show up in the transpiration measurements. Thus, while elongation was markedly and directly affected by tension, transpiration continued essentially unchanged. Significance of elongation spikes Applying P to the soil/root system caused spikes in leaf elongation rates similar in magnitude and direction to the ones occurring on a daily basis under growth conditions. For example, at the beginning of the night upward spikes appeared that denoted relief of tension. Similarly, P applied to the soil/root system caused an upward spike as tension was relieved. The reverse occurred when day began or P was removed. The tensions develop in the xylem during the day in order for water absorption to meet the demands of transpiration. Transpiration dehydrates the leaf, leaf Ψw decreases, and tension develops in the xylem. Absorption occurs but typically lags transpiration because of the time required for leaf Ψw to decrease and develop the required tension (Kramer, 1938). The reverse occurs at night. The abruptness of the day/night transitions in the controlled environment generated the daily spikes, but gradual transitions would make the spikes less obvious. In the controlled environments, the spikes eventually dissipated as absorption stabilized, indicating that the xylem tension became steady and allowed the growth-induced potential fields to develop fully. Judging from the elongation data, the field developed in about 2 h. Similar spikes followed by rate stabilization were reported in various plants when osmotica were added or removed from root media (Cramer and Bowman, 1991; Cramer et al., 1998; Frensch and Hsiao, 1994; Munns et al., 2000a, b; Passioura and Munns, 2000). This suggests that tension-induced spikes may occur widely. Causes of increased tension during the afternoon The tension increased in the afternoon because the root system appeared to become less conductive. As a consequence, the shoot had to exert more tension to meet transpiration requirements as the day progressed. McCully (1999) reported a similar decrease in root conductance in field-grown maize because emboli developed in certain large metaxylem vessels in the nodal roots. Water flow ceased in these vessels, and leaf Ψw indicated that the shoot was exerting more tension to extract soil water in the afternoon than in the morning. This behaviour is consistent with the decreased leaf Ψw and losses in leaf growth seen in the present study late in the day. The metaxylem vessels refilled with water at night (McCully, 1999), which is consistent with the increasing leaf Ψw and recovering leaf growth seen in the present study at night. In addition to embolized root xylem (Buchard et al., 1999; McCully, 1999; Shane and McCully, 1999), emboli can develop in stems (Boyer, 1971; Tyree et al., 1986; Fuchs and Livingston, 1996; Zwieniecki and Holbrook, 1998; Holbrook et al., 2001), petioles (Canny, 1997), and leaf laminae (Neufeld et al., 1992). The tension on water in the xylem causes cavitation, enhancing embolism formation, further increasing tension, and thus risking runaway losses in vascular conductance. However, terrestrial plants appear to have redundant xylem vessels, an evolutionary result that ensures the integrity of the flow path (Dickison, 2000; Shane et al., 2000). Consequently, despite the losses in root conductance, leaf enlargement continued in the afternoon in maize, but slowly. 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This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) © 2008 The Author(s). http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Experimental Botany Oxford University Press

Xylem tension affects growth-induced water potential and daily elongation of maize leaves

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0022-0957
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10.1093/jxb/erm371
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Abstract

Abstract Diurnal rates of leaf elongation vary in maize (Zea mays L.) and are characterized by a decline each afternoon. The cause of the afternoon decline was investigated. When the atmospheric environment was held constant in a controlled environment, and water and nutrients were adequately supplied to the soil or the roots in solution, the decline persisted and indicated that the cause was internal. Inside the plants, xylem fluxes of water and solutes were essentially constant during the day. However, the forces moving these components changed. Tensions rose in the xylem, and gradients of growth-induced water potentials decreased in the surrounding growing tissues of the leaf. These potentials, measured with isopiestic thermocouple psychrometry, changed because the roots became less conductive to water as the day progressed. The increased tensions were reversed by applying pressure to the soil/root system, which rehydrated the leaf. Afternoon elongation immediately recovered to rapid morning rates. The rapid morning rates did not respond to soil/root pressurization. It was concluded that increased xylem tension in the afternoon diminished the gradients in growth-induced water potential and thus inhibited elongation. Because increased tensions cause a similar but larger inhibition of elongation if maize dehydrates, these hydraulics are crucial for shaping the growth-induced water potential and thus the rates of leaf elongation in maize over the entire spectrum of water availability. Potential field, potential gradient, transpiration, osmotic potential, turgor, Zea mays L Introduction Maize leaves elongate at varying rates during the day, in part, because the natural environment varies. But when the environment is held constant with an abundant supply of water and nutrients, much of the variation remains. Leaf elongation is rapid early in the day and declines as the day progresses. Because this behaviour inhibits the overall growth of the leaf and has not been explained, this study was undertaken to investigate its causes. The approach was to determine whether the causes were outside or inside the plant. External causes could result from gradients in soil water or nutrients adjacent to the root surface that develop during the day (Nye and Tinker, 1977; Milligan and Dale, 1988; Stirzaker and Passioura, 1996) or from gradual changes in soil temperature (Ben-Haj-Salah and Tardieu, 1995; Watts, 1974). Other factors such as humidity or wind speed could be important (Loomis, 1934; Christ, 1978a, b; Cutler et al., 1980; Salah and Tardieu, 1996, 1997). On the other hand, internal factors could involve diurnal patterns of uptake and delivery of water and nutrients to the leaf (Fricke et al., 1997; Fricke, 2002b) or changes in growth-induced water potentials associated with changes in diurnal transpiration rates (Westgate and Boyer, 1984, 1985; Boyer, 1985, 1988; Fricke and Flowers, 1998; Martre et al., 1999; Fricke, 2002a; Boyer and Silk, 2004). Resistances to water flow in the vascular tissues can vary diurnally (Passioura and Munns, 1984; McCully, 1999), and biochemical or hormonal signals could change between roots and shoots as the day progresses (Davies and Zhang, 1991). In the following work, each of these variables was systematically tested in order to identify causative ones. Once a candidate was identified, the variable was eliminated or reversed, and the effect on leaf elongation was used to accept or reject the candidate. Materials and methods Plant materials Maize seeds (Zea mays L. cv. B73×Mo17, Illinois Foundation Seeds, Inc., Champaign, IL) were germinated between two sheets of paper towels wetted with nutrient solution at 29 °C in the dark. The nutrient solution was 12 mol m−3 Ca(NO3)2, 8 mol m−3 KNO3, 4 mol m−3 KH2PO4, 4 mol m−3 MgSO4, 50 mmol m−3 H3BO3, 20 mmol m−3 MnSO4, 4 mmol m−3 ZnSO4, 1 mmol m−3 CuSO4, 1 mmol m−3 H2MoO4, and 250 mmol m−3 Fe-citrate (modified Hoagland's solution; Hoagland and Arnon, 1950). On the third day, the seedlings were transferred individually to Plexiglas pots of a size that fit a pressure chamber (6 cm inner diameter, 23 cm depth) with holes for drainage. Each pot was filled with a 1:1:1 (by vol.) mix of soil, peat moss, and vermiculite at pH 6.5. The pot was covered with a pressure chamber top through which the coleoptile emerged. The seedlings continued to grow in darkness until the mesocotyl passed through the opening in the top. The plant and the pot, with top, were then transferred to a controlled environment chamber (Environmental Growth Chambers, Ohio, USA) with day/night temperatures of 25/20 °C, relative humidity of 60/90%, and 14 h of photosynthetically active radiation of 700–800 μmol m−2 s−1. Nutrients were supplied two to three times a week by filling the whole pot from the bottom upward, then draining away the excess. Because the pot was covered with the pressure chamber top, the nodal roots developing above the mesocotyl were prevented from entering the soil. In some experiments, the maize plants were grown as described above except (i) the night temperature was at 25 °C for one night instead of decreasing to 20 °C, or (ii) a single plant was developed in a bigger pot (15 cm diameter and 16 cm depth) with nodal roots growing into the same soil mix, or (iii) a plant was grown in nutrient culture without the soil. For the soil-less treatment, the dark-grown seedling was transferred to a container (10.3 cm inner diameter, 26 cm depth) filled with aerated nutrient solution as above. The container was covered with a pressure chamber top through which the coleoptile and mesocotyl passed through the opening in the top. The nodal roots did not enter the nutrient solution. Leaf elongation After leaf 5 emerged around 11 d after planting, the soil/root system of the maize plant was sealed inside the pressure chamber (7.6 cm inner diameter, 26.7 cm depth, as shown in Fig. 1 of Tang and Boyer, 2003) and the total leaf elongation was continually monitored in the environment where the plants were grown (as shown in Fig. 1 of Tang and Boyer, 2003). A fine Kevlar thread was attached to the mature portion of the leaf, and elongation was detected by an optical incremental encoder (25G, Sequential Information Systems Inc., New York, USA) that recorded motion by rotating as the leaf elongated. The encoder was unaffected by temperature or supply voltage. At 2 s intervals, the data were sent to a datalogger (CR7, Campbell Scientific, Inc. Utah, USA) which stored them as a 1 min average of total accumulated counts during the minute and converted the counts to the elongation rate. The rate was downloaded to a computer for plotting. Fig. 1. Open in new tabDownload slide Elongation of maize leaf 5 when the plant was supplied with adequate water and nutrients. (A) Length of leaf. (B) Elongation rate of leaf. The open and filled bars on the X-axis represent daytime and night-time, respectively. Root pressurization (P) In certain experiments, the soil/root system was placed in the pressure chamber and was pressurized with compressed air until guttation formed along the leaf edges while leaf elongation was continuously monitored with the encoder. This system was similar to that used by Janes and Gee (1973), Nulsen et al. (1977), Passioura and Munns (1984), Saliendra et al. (1995), and Hsiao et al. (1998), but a controller (DP25-E Process Meter, Omega Engineering Inc, Stamford, Connecticut, USA) connected to a pressure transducer (PG856–250, Statham Laboratories Inc., Puerto Rico) was set to regulate the applied pressure (P) to maintain guttation (set-up shown in Fig. 1 of Tang and Boyer, 2003). Ψw profile The profile of Ψw and its components was determined from the soil to the tip of leaf 5. After excising the shoot inside the controlled environment chamber, the shoot was immediately transferred to a humidity-saturated glove box in low light. Four 2 cm samples of leaf tissue were taken along the length of leaf 5 (counted from the base of the plant), starting at the mature tip and moving toward the growing base. The basal tissues were sampled after dissecting them from the surrounding leaf bases. The samples were rapidly transferred individually into four psychrometer cups coated with petrolatum and sealed into an isopiestic thermocouple psychrometer (Isopiestics Company, Lewes, DE), a method having the advantage that the leaf epidermis had no effect on the measurements. The pot was moved to a humidity-saturated room, and the soil was sampled at a 4 cm depth inside the pot. The whole soil/root medium was carefully detached from the pot, and one mature primary root of 10 cm with attached branches was sampled after flicking away the soil and removing the root tips. The Ψw was first determined according to Boyer (1995). The leaf and root samples were then frozen and thawed in the sealed cup, and the osmotic potential (Ψs) was measured by the same technique. Turgor pressure (Ψp) was calculated from Ψw–Ψs. A profile of leaf Ψw or its components was then constructed as a function of distance above the soil surface. In some experiments, the Ψw profile was measured in shoots whose soil/root system was exposed to P in the pressure chamber. The shoots were sampled for measurement of the water potential (Ψw) and its components, as described above, while the soil/root system was still exposed to P. No root or soil was sampled because the soil/root system was enclosed in the chamber and held at P during the sampling time. Guttation and exudate Ψs The appearance of guttation fluid was determined along the length of leaf 5 and samples were collected in a microlitre syringe. In some plants, the shoot was excised above the soil and the initial 10 mm3 of exudate was sampled from the mesocotyl stump after the cut surface was rinsed and blotted dry. The Ψs was determined isopiestically on samples with a volume of 3–5 mm3 as described by Boyer (1995). Transpiration and exudation rates Transpiration rates were determined by weighing the whole apparatus (Fig. 1 in Tang and Boyer, 2003) in the controlled environment chamber where the plants were grown, while leaf 5 elongation was simultaneously monitored with the encoder. The weight was recorded every 10 s and stored in a computer. The sum of six successive measurements gave the weight min−1. Transpiration was calculated as weight change min−1, given as running averages for the previous 10 min. For plants with P applied to the soil/root system, the same process was used by applying P until guttation began to appear. While transpiration represented the water loss from the shoot, water entering the shoot from the root system was estimated from the exudation of an excised mesocotyl of a separate plant grown identically. Leaf 5 of the separate plant elongated at a rate close to the pressurized one. The soil/root system was exposed to the same P in both plants. After excision, the cut mesocotyl surface was rinsed with water and blotted dry, and the exudate was collected every minute for the first 5 min, and every 5–10 min thereafter. The volume collected over 2 h was used to calculate the exudation rate. Conductance of the soil/root system The exudate measured as above first appeared on the cut mesocotyl surface when P balanced Ψw of the soil (i.e., P= –Ψw of soil). Raising P above this balanced condition created a total potential difference that drove water out of the mesocotyl surface at a rate determined by the conductance of the soil/root system. Because the Ψw of the soil was known from measurements with the psychrometer, and P was known, the conductance of the soil/root system could be calculated according to: (1) where e was the exudation rate from the cut surface of the mesocotyl stump of the soil/root system after the shoot was removed (mm3 s−1) and k was the conductance of the soil/root system (mm3 s−1 MPa−1). Results Leaf 5 emerged from the enclosing sheaths of the older leaves 11 d after planting (Fig. 1A). The leaf elongated rapidly during the day but slowly at night (Fig. 1B). As the lamina unrolled and became increasingly exposed, elongation displayed a prominent and sudden downward spike at the beginning of the day and upward spike at the end of the day (Fig. 1B). A few min after each spike, elongation became more stable. However, during the day, the stable elongation always was more rapid in the morning than in the afternoon (Fig. 1B). At night, the reverse occurred and there often was a noticeable increase in the rate as the night progressed (Fig. 1B, days 11–17). The temperature was stable during the day and night, but cooler at night (see Fig. 3E below). If the temperature was the same during day and night, i.e. 25 °C, elongation began at night at the same rate as at the end of the day (0.65–0.75 μm s−1 at 25 °C) instead of becoming slower (0.55 μm s−1 at 20 °C) (Fig. 2). Low night-time temperature was thus responsible for the slower night-time elongation in Fig. 1. These features continued for most of the growth period ending on day 22 (Fig. 1). Fig. 2. Open in new tabDownload slide Elongation of maize leaf 5 when temperature is the same during day and night. Temperature and relative humidity are shown at the top of the figure. Data are from a single plant 16 d after planting, which was one of four replicate plants all of which gave the same result. Fig. 3. Open in new tabDownload slide Elongation of maize leaf 5 when soil conditions were varied. (A) Plant grown in a large pot of soil in which nodal roots developed or (B) grown in aerated nutrient solution. The measurements were made on leaf 5 on day 16 after planting. (C) Elongation of a mature leaf 5 on day 22 after planting. Each of the maize graphs is from a single plant among 3–5 replicate plants. (D) Elongation of a metal rod instead of a leaf. (E) Air temperature for these experiments. Availability of water and nutrients to the roots The daytime loss in elongation rate was so persistent that its origins were investigated by varying the supply of water and nutrients to the root surfaces. Figures 1 and 2 used a small pot from which nodal roots were excluded. If, instead, the plants grew in a soil volume four times that in Figs 1 and 2, nodal roots extended into the soil and 30% more root dry mass developed, but leaf 5 continued to show the same pattern of decreased elongation in the afternoon (Fig. 3A). Plants growing without soil in a nutrient culture also displayed this pattern (Fig. 3B). The effect could not be attributed to salt accumulation on or in the root because the pattern persisted when plants were grown in half-strength nutrient solution or transferred to a water-only medium for one day (data not shown, but appeared as in Fig. 3B). The pattern was not an artefact of measurement because mature leaves showed no diurnal change in dimensions (Fig. 3C). A metal rod in place of the shoot showed zero elongation (Fig. 3D) except for a slight thermal expansion/contraction during the first 2 h after the temperature changed in the controlled environment (Fig. 3E). Flux of water and nutrients to the shoot Because the elongation pattern persisted under these varied external conditions, important internal conditions were investigated. At night, guttation occurred (Fig. 4A) and transpiration was near zero (Fig. 4B). During the day, guttation ceased as transpiration became rapid. The transpiration was steady throughout the day (Fig. 4B). Fig. 4. Open in new tabDownload slide Diurnal delivery of water and solute to the maize shoot. (A) Leaf guttation shown as a percentage of the vein ends displaying a droplet on leaf 5. (B) Transpiration of the whole shoot. Data are for day 16 after planting and are representative of a single plant among five replicate plants. (C) Soil water potential (triangles), exudate osmotic potential at the leaf base (squares), and guttate osmotic potential for the leaf edge (circles). Guttate during the day was obtained by applying P to the soil/root system. Exudate was obtained similarly from the mesocotyl stump after detopping. Data are averages for three plants with standard deviations smaller than the symbols. (D) Solute flux from root to shoot calculated as the product of the transpiration rate (from B) and exudate concentration (from C). Solutes in the transpiration stream followed this flow of water. At night, the xylem solution entering the base of the shoot (measured as Exudate, Fig. 4C) had a Ψs of –0.28 MPa, which was lower than the Ψw of the soil, presumably because salts were being loaded into the xylem by the root. During the day while transpiration was rapid, the xylem solution was diluted by the entering water, and Ψs at the base of the shoot rose to –0.1 MPa, or about the level of Ψw in the soil. By the time the transpiration stream passed the base of the shoot and reached the exposed leaf blade, its Ψs was zero, determined from the guttation fluid collected at the leaf edges after the root was pressurized (Fig. 4C). This indicated that the shoot removed essentially all the solute from the transpiration stream. The solute flux to the shoot was much greater during the day than at night (Fig. 4D), but remained nearly steady throughout the day. Ψw profiles The inability of the internal water and solute fluxes to explain the downturn in daily elongation suggested that other internal factors might have varied. A central factor would be the force needed to move water and solute in the xylem, essentially the water potential (Ψw) and its components (Kramer and Boyer, 1995). These forces were measured first when leaf 5 displayed the usual slower rate of elongation at night (Fig. 5A). At this time, Ψw of the exposed blade was –0.13 to –0.15 MPa and nearly in equilibrium with Ψw of the soil (Fig. 5B, compare Ma, Mb, Mc with S). The leaf and soil were thus very hydrated. Because the mature part of the leaf was connected to the potential of the soil mostly through the xylem, the xylem in the leaf base was also hydrated and essentially the same as in the soil (X in Fig. 5B). Fig. 5. Open in new tabDownload slide Elongation (A) and water potential (Ψw) profiles (B–E) of leaf 5 at various times during the day. At the time indicated by the arrows, samples for Ψw were taken from the soil (S), mature root (R), elongating region of leaf 5 (G), and mature regions of leaf 5 (Ma, Mb, and Mc). Because solute is virtually absent in guttation fluid (see Fig. 4C), Ma, Mb, and Mc mostly reflect xylem tension. The vertical dashed line indicates Ψw in the xylem (X) in the elongation region. Growth-induced water potential is (X–G), shown by the shaded area. The leaf base between 0 and 10 cm contained the growing region, from Tang and Boyer (2002). Elongation rate was from a single plant while the Ψw profile was the average ±1 SD for three plants on day 16 after planting. Most SD were smaller than the symbols. The solid bar on the abscissa indicates the dark period. By contrast, the Ψw of the leaf base was –0.48 MPa at night (G in Fig. 5B). This region contains the elongating tissues (basal 10 cm; see Tang and Boyer, 2002). Therefore, a growth-induced Ψw (X–G) of about 0.35 MPa was present in the growing tissues outside of the xylem in the leaf base (Fig. 5B). The Ψw of the root (R) was lower than in the mature leaf perhaps because solute was being deposited in the root xylem, as pointed out above. The solutes would cause pressure to develop in the xylem. The pressure Ψpx was calculated from (2) where Ψwx was the water potential of the xylem in the leaf base (X in Fig. 5B) and Ψsx was the osmotic potential of the xylem in the leaf base (Exudate in Fig. 4C). Accordingly, the root pressure at the leaf base was 0.15 MPa = –0.14 – (–0.29). This positive root pressure probably caused guttation by the leaf at night. The day began with a downward spike in leaf elongation that recovered to a stable but rapid rate (1.3 μm s−1, Fig. 5A) about double that at night (0.65 μm s−1). The Ψw in the mature part of the leaf was more negative than that at night, reflecting tension that had increased as the day began (Ma, Mb, and Mc in Fig. 5C compare with Fig. 5B). The tension at the leaf base was calculated from Equation 2 to be –0.3 MPa (xylem Ψw of –0.4 MPa from Fig. 5C minus xylem Ψs of –0.1 MPa from Fig. 4C). Leaf elongation was thus nearing its maximum with this tension. G was –0.5 MPa, which was slightly lower than at night, but (X–G) could not be calculated because elongation was accelerating, and the calculation required stable rates for the preceding 2 h. As the day progressed, the mature part of the leaf developed Ψw of –0.5 to –0.65 MPa (Fig. 5D), which indicated that tensions were –0.4 to –0.55 MPa (Equation 2), or substantially greater than the tension seen earlier in the day. The build-up of tension was associated with a decrease in leaf elongation to 0.85 μm s−1. With this stable rate, G had fallen to –0.7 MPa while X had moved to –0.5 MPa, giving a small growth-induced Ψw between xylem and growing tissues (X–G) of about 0.2 MPa (Fig. 5D). When night returned and transpiration decreased (Fig. 4B), the potentials began to return to their earlier night-time levels (Fig. 5E). With the release of tension, there was an upward spike in elongation and the rates then settled at the slow but gradually increasing night-time rate (Fig. 5A). Thus completed the 24 h cycle of elongation and forces moving water and xylem solutes through the plant. Tests of tension mechanism These results indicated that, despite stable water and nutrient flows during the day, the xylem tensions driving the flows were becoming larger as the day progressed while leaf elongation was declining. The correlation between increasing tension and decreasing elongation suggests that the tensions may have affected elongation. If this hypothesis is correct, leaf elongation would increase if the tensions were relieved. In order to test the hypothesis, P was applied to the soil/root system to relieve the tension. Relief of tension was detected when guttation appeared at the edges of the elongating leaf. When P was applied in the morning, leaf elongation immediately spiked upward as if tension had been relieved, but the later stable rate was the same as in the absence of P (Fig. 6B compare with Fig. 6A). When P was released, the rate spiked downward as though tension had reformed, and then settled at the rate for the rest of the day. By contrast, if this treatment was applied at the end of the day, the same spikes occurred, but the settled rate was much faster than had been occurring without P (Fig. 6C compare with Fig. 6A). The afternoon inhibition of elongation was eliminated. As a control, a mature leaf displayed only small spikes when P was applied, and there was no other elongation response (Fig. 6D). Fig. 6. Open in new tabDownload slide Elongation of leaf 5 when xylem tension was relieved by applying P to the soil/root system until guttation was observed. (A) Without P. (B) With P applied and released in the early morning. (C) As in (B) but in the late afternoon. These measurements were on day 16 after planting. (D) As in (B) but for a mature leaf with P applied and released in the morning as well as the afternoon at 27 d after planting. Dashed lines in (B) and (C) show the elongation expected without P, as in (A). Each graph is for a single plant among 2–4 replicate plants. It should be noted that P required to relieve tension was larger late in the day (Fig. 6C) than early in the day (Fig. 6B), confirming that tensions became larger as the day progressed. These changes in tension were detected in the Ψw profiles. In plants showing the growth response of Fig. 6 (Fig. 7A, E), but sampled for the Ψw profile (Fig. 7B, F), the whole shoot profile shifted to a wetter status when P was applied to the soil/root system. The applied P were higher late in the day (Fig. 7E) than early in the day (Fig. 7A), and the shift was correspondingly larger late in the day (Fig. 7F) than early in the day (Fig. 7B). Because of the rapid nature of the P treatments, steady conditions were not present and (X–G) could not be determined. But the Ψs of the shoot tissues became more negative during the day as solute accumulated (Fig. 7C, G). P applied to the soil/root system had little effect on Ψs except in the basal tissues, which became less negative especially late in the day. The turgor increased in the mature tissues, which confirmed that tension had been relieved and the tissues had rehydrated (Fig. 7D, H). However, the basal growing tissues had constant turgor throughout the day and when P was applied. Fig. 7. Open in new tabDownload slide Elongation and potential profiles for leaf 5 when tension was relieved by applying P to the soil/root system. (A, E) Elongation rate early and late on day 16, respectively. Maximal rate (max) refers to the highest rate in the morning. Dashed line shows the elongation rate without P as in Fig. 6A. Elongation trace ends when shoot was removed to measure potential profiles. Profiles of water potential (B, F), osmotic potential (C, G), and turgor (D, H) before (open symbols) and after P was applied (closed symbols). Profiles after P was applied (B–D and F–H, closed symbols) were measured at the end of the traces in (A) and (E), in the same but single plants. They are compared to profiles measured in different plants at the same time but without P, presented as means ±SD (n=3). SD was sometimes too small to be seen behind the data point. See Fig. 5B for definitions of Mc, Mb, Ma, G, R, and S. If P relieved tension by forcing more water through the soil/root system, the flow should be detectable in a detopped plant. After detopping during daytime conditions, no exudation occurred from the soil/root system unless P was applied. With P applied sufficiently to cause guttation in the intact plant in the afternoon, leaf elongation became much faster (Fig. 8A) and transpiration slightly faster (Fig. 8B) in the same plant. The slight increase in transpiration was probably caused by direct evaporation when the guttation droplets appeared on the leaf edges. After detopping a separate plant elongating at a similar rate, the same P caused exudation from the soil/root system in excess of that necessary for transpiration (e in Fig. 8B). Similarly, in the early morning, the flow with P exceeded transpiration (data not shown). However, because of greater tension in the afternoon than in the morning, the P in the afternoon was about twice that in the morning, as shown in Fig. 7A and E. The exudation rate was similar for both times, indicating that the conductance of the soil/root system had decreased as the day progressed. The conductance in mid-morning was 11.03 and in late afternoon was 6.06±0.76 mm3 s−1 MPa−1 (1 SD, n=5), calculated from Equation 1. The decrease in soil/root conductance was attributable to the root because the soil remained hydrated with stable Ψw throughout the day (Fig. 4C). Fig. 8. Open in new tabDownload slide Elongation of leaf 5 (A) and transpiration and exudation (B) when P was applied to the soil/root system during the afternoon. Max in (A) shows the maximal rate in the morning. Dashed line indicates the elongation rate typical for late afternoon without P as in Fig. 6A. With P, leaf 5 guttated. Transpiration in (B) is for the plant in (A). e in (B) is for a plant like that in (A) with the same P but detopped (cross-hatched). Exudate appeared on the stump after P was applied. Data are typical for day 16 after planting, repeated four times with exudation measured twice. Discussion This study is a sequel to earlier work from this laboratory that was done with dehydrating maize (Tang and Boyer, 2002, 2003). In the present work, the maize was hydrated and leaf elongation decreased in the afternoon because xylem water came under increasing tension. Despite abundant water in the soil, the roots became less conductive to water and required greater tensions to maintain water and solute flows to the shoot. In the earlier studies of Tang and Boyer (2002, 2003), increasing tensions also inhibited leaf elongation and were caused by losses in conductance. Therefore, xylem tension was a central issue for the growth process. Its central activity in all three studies indicates that tension affects growth across the entire spectrum of soil water availability. The control by xylem tension was unequivocally demonstrated in the present work when the soil/root system was pressurized to relieve the tension. With guttation as the indicator of relief, elongation immediately responded with an initial upward spike in rate. After the spike, the leaf elongated rapidly, and the afternoon inhibition was eliminated. A similar P treatment in the early morning generated the spike but did not alter the following rate because the tensions were already small and elongation was at its maximum. The rapidity of these responses eliminates root-sourced hormonal or biochemical signals as a form of control, despite the importance of these processes over the long term (Cleland, 1971; Taiz, 1984; Passioura, 1988; Davies and Zhang, 1991). Root-sourced hydraulic signals appear to control the extensibility of cell walls in shoot growing regions (Davies and Zhang, 1991) and thus create the conditions allowing growth-induced Ψw to develop. These types of signals require considerable time to affect the shoot, as shown by Passioura (1988). Pressure was applied to the root system continually and leaf growth was compared with that in unpressurized controls as the soil dehydrated (Passioura, 1988). Differences appeared after a few days suggesting that a day or two may be required before root-sourced chemical signals change growth patterns. Munns et al. (2000b) also point out that time scales of hours or days may give different results. The importance of hydraulic signals in the short term was noted by Salah and Tardieu (1997), Hsiao et al. (1998), and Bouchabke et al. (2006) using slightly dehydrated maize. A tension mechanism may have been operating in their experiments. A tension mechanism may also explain the findings of Koch et al. (2004), who investigated mature leaf sizes at various positions in Sequoia sempervirens. Because of the great tree height, there is a standing gradient of tension caused by gravity, with leaves at the top subjected to greater tension than those at the bottom. Koch et al. (2004) report that the upper leaves were smaller than those at the bottom, in agreement with the present findings that increased xylem tension can diminish leaf growth. It should be noted that changes in turgor did not account for the afternoon inhibition of leaf elongation. Turgor in the elongating tissues did not vary during the day nor when tension was relieved in the xylem. Turgor was maintained by changes in Ψs. It appears that sufficient solute was delivered to the elongating cells to maintain their turgor throughout the day. Mechanism of tension action But why should xylem tension have such a large effect on leaf growth and so little effect on transpiration? Both processes draw on water in the xylem. Abundant water passes right through the growing leaf base and is used for rapid transpiration in the mature blade. The amount of water moving through the xylem in the leaf base is certainly sufficient for the growth of the leaf, because leaf 5 uses only 2% of this water for its growth, as shown by Tang and Boyer (2002). On the other hand, the tension at the leaf base is the initial part of a water potential field, i.e. a dynamic three-dimensional gradient that slopes radially downward into the surrounding tissues (Tang and Boyer, 2002). Each protoxylem vessel is surrounded by one of these fields (Fig. 10 in Tang and Boyer, 2002, shows the likely three-dimensional form). The downward slope moves water out of the protoxylem and into the growing cells. Because the tension in the xylem is part of this potential field, an increased tension decreases the water potential next to the xylem and inverts the initial slope of the field. The inverted shape prevents water from leaving the xylem. The effect is immediate, shown for maize leaves by Tang and Boyer (2003) and soybean stems by Nonami et al. (1997) and Passioura and Boyer (2003). The immediacy was observed in the present work by the elongation spikes followed by steady but changed elongation after pressurization. The response of the entire growing region means that a local change in the field affects growth of the whole tissue. The whole tissue responded because all the cells depended on water extraction from the xylem. Consequently, this mechanism appears to be the growth-controlling feature of this study. The presence of the field was indicated by the growth-induced water potential (X–G) in the growing tissues at the leaf base, using psychrometer measurements. The psychrometer determined the potential in the xylem (X) and average potential of the surrounding, growing tissues (G). A similar field in three dimensions was measured by Nonami and Boyer (1993) from cell measurements with a pressure probe and picolitre osmometer in the growing region of soybean hypocotyls. The measurements agreed well with the tissue level measurements with the psychrometer (Nonami and Boyer, 1993; Nonami et al., 1997). (X–G) developed because the small cells of the enlarging tissues imposed many wall/membrane barriers to flow (Tang and Boyer, 2002). Their cumulative frictional resistance prevented water from entering the growing cells rapidly. As a consequence, the yielding of the cell walls ran ahead of water entry and prevented turgor from becoming as high as it otherwise would. This effect, shown experimentally by Boyer (2001) in soybean hypocotyls, caused the low water potentials (G) necessary for (X–G) to form. As can be seen in Fig. 9 (Late Morning), (X–G) was large after several hours of rapid steady elongation in the morning, as reported in Fig. 4B of Tang and Boyer (2002). By comparison, the present study shows that (X–G) became small after several hours of steady elongation in late afternoon (Fig. 9; Late Afternoon). Therefore, the increased xylem tension diminished the potential field as the day progressed. These potentials were not generated by relaxation after excision, as was claimed (Cosgrove et al., 1984). The potentials exist in completely intact plants (Boyer, 1968; Boyer et al., 1985) including maize (Westgate and Boyer, 1984; Tang and Boyer, 2002), and excision effects are small (Westgate and Boyer, 1984; Tang and Boyer, 2002). Nor were they caused by solute in the apoplast (Cosgrove and Cleland, 1983), because solute concentrations were low (Nonami and Boyer, 1987). In the present study, the solute concentration in the guttation fluid was zero and in xylem at the leaf base was equivalent to Ψs of only –0.1 MPa. Such low apoplast concentrations contributed little to G of –0.5 to –0.7 MPa. Tensions thus dominated in the apoplast. It follows that, as the day progressed, an increase in xylem tension would diminish (X–G) as shown diagrammatically in Fig. 10 (black cells; Late Morning compared to Late Afternoon). If (X–G) became smaller, less water would be taken up from the xylem and less elongation would occur when compared to the morning rates. Fig. 9. Open in new tabDownload slide Water potential profiles during Late Morning and Late Afternoon in maize leaf 5. Elongation had been steady for 2 h before these measurements were made. Data are means for three plants from Fig. 5D (closed symbols) or individual measurements for one plant reported by Tang and Boyer (2002) (open symbols). Fig. 10. Open in new tabDownload slide Diagram of tension in the water transport pathway from soil through the root to the leaf where the path splits to enter the elongating region for growth (black cells) or the mature blade for transpiration (open cells). On the left is the position in the plant, and on the right are simplified diagrams of the tension gradient in the xylem (dashed line) and apoplast of the elongating tissues (black). Note that the water potential in the xylem in the elongating region (X) is the start of the water potential gradient in the elongating tissues (X–G). Although (X–G) is a water potential generated inside the growing cells, it is mostly tension in the apoplast. Because (X) is part of (X–G), changes in (X) between the morning and afternoon may change (X–G) as shown (Late Morning versus Late Afternoon). For a three-dimensional shape of (X–G), see Fig. 10 in Tang and Boyer (2002). Labels on the tension diagram correspond to psychrometer measurements in this study, defined in Fig. 5B. Transpiration, on the other hand, was not altered by the tension build-up. The tension was insufficient to close stomata, which would have inhibited transpiration. The vapour pressure of the evaporating water would decrease slightly with increasing tensions, but for a tension increase of 0.15 MPa from Fig. 5, the vapour pressure would decrease only 0.11%, calculated from: (3) where ΔΨw is the change in tension (MPa), R is the gas constant (L MPa mol−1 K−1), T is the temperature (K), Vw is the partial molal volume of water (L mol−1), p is the vapour pressure and subscripts w and o are the water under the new tension and the original tension, respectively. The 0.11% change in vapour pressure was detected with the thermocouple psychrometer as part of the water potential measurements but was too small to show up in the transpiration measurements. Thus, while elongation was markedly and directly affected by tension, transpiration continued essentially unchanged. Significance of elongation spikes Applying P to the soil/root system caused spikes in leaf elongation rates similar in magnitude and direction to the ones occurring on a daily basis under growth conditions. For example, at the beginning of the night upward spikes appeared that denoted relief of tension. Similarly, P applied to the soil/root system caused an upward spike as tension was relieved. The reverse occurred when day began or P was removed. The tensions develop in the xylem during the day in order for water absorption to meet the demands of transpiration. Transpiration dehydrates the leaf, leaf Ψw decreases, and tension develops in the xylem. Absorption occurs but typically lags transpiration because of the time required for leaf Ψw to decrease and develop the required tension (Kramer, 1938). The reverse occurs at night. The abruptness of the day/night transitions in the controlled environment generated the daily spikes, but gradual transitions would make the spikes less obvious. In the controlled environments, the spikes eventually dissipated as absorption stabilized, indicating that the xylem tension became steady and allowed the growth-induced potential fields to develop fully. Judging from the elongation data, the field developed in about 2 h. Similar spikes followed by rate stabilization were reported in various plants when osmotica were added or removed from root media (Cramer and Bowman, 1991; Cramer et al., 1998; Frensch and Hsiao, 1994; Munns et al., 2000a, b; Passioura and Munns, 2000). This suggests that tension-induced spikes may occur widely. Causes of increased tension during the afternoon The tension increased in the afternoon because the root system appeared to become less conductive. As a consequence, the shoot had to exert more tension to meet transpiration requirements as the day progressed. McCully (1999) reported a similar decrease in root conductance in field-grown maize because emboli developed in certain large metaxylem vessels in the nodal roots. Water flow ceased in these vessels, and leaf Ψw indicated that the shoot was exerting more tension to extract soil water in the afternoon than in the morning. This behaviour is consistent with the decreased leaf Ψw and losses in leaf growth seen in the present study late in the day. The metaxylem vessels refilled with water at night (McCully, 1999), which is consistent with the increasing leaf Ψw and recovering leaf growth seen in the present study at night. In addition to embolized root xylem (Buchard et al., 1999; McCully, 1999; Shane and McCully, 1999), emboli can develop in stems (Boyer, 1971; Tyree et al., 1986; Fuchs and Livingston, 1996; Zwieniecki and Holbrook, 1998; Holbrook et al., 2001), petioles (Canny, 1997), and leaf laminae (Neufeld et al., 1992). The tension on water in the xylem causes cavitation, enhancing embolism formation, further increasing tension, and thus risking runaway losses in vascular conductance. However, terrestrial plants appear to have redundant xylem vessels, an evolutionary result that ensures the integrity of the flow path (Dickison, 2000; Shane et al., 2000). Consequently, despite the losses in root conductance, leaf enlargement continued in the afternoon in maize, but slowly. 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Journal of Experimental Botany – Oxford University Press

Published: Mar 1, 2008

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