Oecologia (1992) 92:410415

Oecologia 9 Springer-Verlag 1992

Seasonal variation in the tissue water relations of

Picea glauca

S . J . C o l o m b o and Y. T e n g *

Ontario Forest Research Institute, Ontario Ministry of Natural Resources, P.O. Box 969, 1235 Queen Street East, Sault Ste. Marie, Ontario, Canada P6A 5N5 Received October 10, 1991 / Accepted in revised form July 7, 1992

Seasonal variation in water relations of 3-yearold white spruce (Picea 9lauca (Moench) Voss) shoots, monitored with pressure-volume curves over 28 months, was closely related to shoot phenology and was sensitive to environmental fluctuations during both summer growth and winter dormancy. Turgor maintenance capacity was lowest during rapid shoot elongation from late May to early July; this was indicated by the lowest total turgor pressures, the highest (least negative) osmotic potentials at full turgor and the turgor loss point, the smallest differences between osmotic potentials at full turgor and the turgor loss point, the highest relative water contents at turgor loss and a linear decline in cell elasticity with decreasing turgor pressure. This suggests that the high susceptibility of white spruce seedlings to growth check after transplanting is largely attributable to the poor turgor maintenance capacity of this species in early summer. Abstract.

Bud development - Cell elasticity - Osmotic potential - Turgor Key words:

Water stress is a major cause of white spruce (Piceaolauca (Moench) Voss) forestry plantation failure and "planting check", a phenomenon of stunted shoot growth noted for several years following transplanting (Armson 1958; Burdett et al. 1984; Burgar and Lyon 1968; Mullin 1963). The ability of seedlings to survive and grow vigorously despite water stress can be a key factor determining the success of plantation establishment. Hsiao et al. (1976) noted that a lowering of turgor potential (UP), associated with a loss of cell water content and a drop in cell water potential (~tw), if sufficiently large and prolonged, will have adverse effects on cell metabolism and growth. Therefore, turgor maintenance capacity, the ability to * Present address: Faculty of Forestry, University of Toronto, 33 Willcocks Street, Toronto, Ontario, M5S 3B3, Canada Correspondence to: S.J. Colombo

maintain adequate turgor as cell water content and ~w decrease is an important adaptation to water stress (Jones and Turner 1978; Ritchie and Shula 1984). Turgor maintenance capacity depends in part on two tissue water relations properties (Jones and Turner 1978; Kikuta and Richter 1986): osmotic potential (~), which can be measured using the pressure-volume (P-V) technique (Scholander et al. 1965; Tyree 1976; Tyree and Hammel 1972), and the bulk modulus of elasticity (e), which is defined (Roberts et al. 1981) a s : = d~p/(dV/V)

(1)

where dV/V represents a differential change in tissue water volume. High turgor maintenance capacity is associated with a large difference between osmotic potentials at full turgor (~100) and the turgor loss point (~a-LP), A ~ (Jones and Turner 1978). Jane and Green (1983) state that plants with a low relative water content at the turgor loss point (RWCTLp) may also have high turgor maintenance capacity because they can sustain large losses of water without totally losing turgor. The relationship between turgor maintenance capacity and ~ is complex (Tyree and Karamanos 1981). High results in large changes in water potential for only small changes in water content, producing a proportionately large increase in hydraulic conductivity, and hence plants will maintain high levels of turgor so long as water is available and water transport within the plant is nonlimiting (Bannister 1987; Colombo 1987). However, high will lead to more rapid turgor loss when water supply is limited. In comparison, when ~ is low, comparatively large volumes of water will be lost with only a small decline in turgor (Grossnickle 1988; Ritchie and Shula 1984). It has been suggested that the integration of turgor pressure between full turgor and the turgor loss point may be a more comprehensive indicator of turgor maintenance capacity than either osmotic potential or cell elasticity alone (Bannister 1987; Colombo 1987; Grossnickle 1988; Kikuta and Richter 1986; Roberts et al.

411 1980). T h e s e different strategies for t u r g o r m a i n t e n a n c e are in n e e d o f f u r t h e r e v a l u a t i o n . T h e r e has b e e n a p r o l i f e r a t i o n o f i n f o r m a t i o n in recent y e a r s c o n c e r n i n g s e a s o n a l p a t t e r n s o f w a t e r relations in tree species (Blake a n d S u t t o n 1987; D e l u c i a et al. 1988; G r o s s n i c k l e 1988, 1989; O s o n u b i a n d F a s e h u n 1987; R i t c h i e a n d S h u l a 1984). This s t u d y was d e s i g n e d to d e t e r m i n e w h e t h e r s e a s o n a l p a t t e r n s o f w a t e r r e l a t i o n s in w h i t e spruce a r e closely r e l a t e d to the p h e n o l o g y o f the s h o o t a p i c a l m e r i s t e m a n d s e a s o n a l v a r i a t i o n s in w e a t h er, a n d to e v a l u a t e w a t e r r e l a t i o n s p r o p e r t i e s o f i m p o r tance to t u r g o r m a i n t e n a n c e c a p a c i t y .

model:

Materials and methods

where ~m and WPz are turgor pressures determined at 3% RWC intervals, V1 and V2 are symplast water volumes at l~/p1 and ~te2, respectively, and V is total symplast volume at full turgor. The shapes of plots of e versus tnrgor pressure were classified according to the criteria of Colombo (1987) and Roberts et al. (1981). Total turgor pressure (Werot~l)is the integral of turgor pressure between full turgor and the turgor loss point (Colombo 1987; Roberts et al. 1980). ~PTot~Lwas determined by constructing H6fler diagrams and weighing the area of each graph under the Wpcarve.

1/V~ = m(RWC) + b

where ~ is osmotic potential, and m the slope of the regression. The y-intercept (b) of this regression gave an estimate of reciprocal osmotic potential at full turgot. The turgor loss point was estimated by eye from the distribution of points on the P-V curve and was located at the point of intersection of the non-linear and linear regions of the curve. The relative water content at the turgot loss point (RWCTLp) was read directly from the graph and the osmotic potential at the turgor loss point (ll/nTLP) was calculated using Eq. (3). The difference between ~t~100 and ~g~TLPwas calculated to yield A~,~. Bulk modulus of elasticity was calculated at 3% intervals of RWC over the entire range of positive turgor as: = (~l/p1 -- ~ ] p 2 ) / [ ( V l - V 2 / V ]

Plant materials and nursery condition Shoots of white spruce seedlings were collected from operationallyproduced crops at the Ontario Ministry of Natural Resources Midburst Tree Nursery (45 ~ N, 80~ W), located approximately 90 km north of Toronto, Ontario, Canada. Seedlings were from northeastern Ontario general collection seed sources. From September to March of each year, shoots were collected from seedlings which had completed their third-year of shoot elongation. In early March of 1984 and 1985, sampling shifted from 3-year-old seedlings that had completed their third-year shoot elongation the previous year, to 2-year-old seedlings that would produce their third-year shoot growth in the current year. Soil moisture tension during the summer was maintained above - 100 kPa through irrigation.

Water potential and P - V curves Water relations parameters were estimated from ~ V curves constructed using the composite procedure of Colombo (1987), which is a modified version of the shoot transpiration method described by Hinckley et al. (1980). The major difference between the two procedures is that in the method used in this trial, each P-V curve was constructed from a population of shoots rather than from an individual shoot. From September 1983 to December 1985, one P-V curve was constructed approximately weekly during the summer and every 2 to 4 weeks during the rest of the year, using 20-30 shoots randomly collected on each date from the nursery. There was no replication of P-V curves at any one point in time. Variations in water relations were determined from trends repeated in two or more years since variance estimates at any one point were unavailable. To construct P-V curves, shoots were cut near ground level and the lower cut ends placed to a depth of about 3 cm in water overnight to allow rehydration. Throughout the day after rehydration, shoots were weighed initially (TW) and then air-dried for a period of time before determining water potential (gw) and concurrent partially-dehydrated weight (PDW), after which oven-dried shoot weight (DW) was determined. Percent relative water content (RWC) measured at a given ~ was calculated as RWC = 100 x ( P D W - D W ) / ( T W - DW)

(2)

Each shoot yielded a single point in a graph of reciprocal water potential (1/~w) versus relative water content (RWC). A composite P-V curve was produced using these 20 to 30 points. Osmotic potential at full turgor (~nl00) and at the turgor loss point (W~TLP), bulk modulus of elasticity (e), and total turgor pressure (~VTo~0 were derived from P-V curves and H6fler diagrams. From 10 to 15 points typically fell on the linear part of the P-V curve, the region over which turgor potential is zero. This line was fitted by the least-squares method with the linear regression

(3)

(4)

Growth measurements, phenological observations and weather data From May to September in 1984, shoots collected for water relations measurements were observed to assess the degree of terminal bud swelling and length of the new terminal shoot. In 1984 only, the percentage of the seedlings that had initiated terminal buds and the number of needle primordia in the developing 3rd-year terminal bud were determined using the methods of Colombo and Odlum (1984), using a separate sample of 20 shoot tips on each date. Weather data were obtained both from a weather station located at the nursery and from a weather station of the Atmospheric Environment Service of Environment Canada.

Results and discussion

Nursery environment and seedlin 9 morphology E a r l y w i n t e r w e a t h e r in all three years f e a t u r e d a r a p i d decrease in t e m p e r a t u r e in late N o v e m b e r w i t h o u t s n o w c o v e r i n g the seedling s h o o t s (Fig. 1). I n 1983 a n d 1985, s n o w c o m p l e t e l y c o v e r e d the seedlings s h o o t s in D e c e m ber, w h e r e a s in 1984, such s n o w a c c u m u l a t i o n d i d n o t t a k e p l a c e until J a n u a r y . I n 1984 a n d 1985, b u d s swelled a n d flushed in early M a y . S h o o t e l o n g a t i o n was r a p i d in b o t h 1984 a n d 1985 f r o m M a y to e a r l y June, s l o w e d in m i d to late-June, a n d b e g a n a g a i n for a s h o r t p e r i o d e a r l y in J u l y (Fig. 2B). B u d scales were o b s e r v e d a t the s h o o t apices o f the m a i n stems in 30% o f the seedlings o n M a y 30, 1984, at w h i c h time new s h o o t length was o n l y 7.4 cm. R e l a t i v e rates o f s h o o t e l o n g a t i o n a n d b u d scale i n i t i a t i o n were closely c o m p a r a b l e f r o m late M a y t h r o u g h June, 1984. B u d scale i n i t i a t i o n p r o c e e d e d r a p i d ly d u r i n g e a r l y June. N e e d l e p r i m o r d i a i n i t i a t i o n b e g a n a n d p r o c e e d e d slowly in July, w i t h a n a v e r a g e o n l y 61 needle p r i m o r d i a p r e s e n t in the t e r m i n a l b u d s on J u l y 30. T h e b u l k o f the a v e r a g e o f o v e r 475 needle p r i m o r d i a

412 40

were initiated between August 7 and October 10, with the highest rate of needle primordia initiation in mid-August (Fig. 2B).

when the rates of shoot elongation were greatest (Fig. 2B). Low values of V~ occurred during dormancy between November and March, with the lowest values of 9 ~100in November and of V~TLPin February. Both V~100 and UGTLpvaried only slightly from late May until early September 1984 (Fig. 2A). A similar seasonal pattern was reported by Tyree et al. (1978) for sugar maple (Acer saccharum Marsh.) leaves. In 1985, by comparison, I,~100and I~/gTLPgradually declined from late May to early September, as observed by Ritchie and Shula (1984) for Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) seedlings. Rapid increases in ~100 and ~TLP occurred in early May (Fig. 2A), associated with bud swell and flush (Fig. 2B). Increases in ~100 and ~TLP in coniferous species associated with the resumption of shoot elongation in the spring have been reported frequently (Colombo 1987, Grossnickle 1988, 1989, Ritchie and Shula 1984, Teskey et al. 1984, Tyree et al. 1978). In both 1984 and 1985, ~100 and ~TLP followed bimodal patterns between April and August (Fig. 2A). ~ first reached maximum (least negative) values at the end of May, decreased to a mid-summer minimum (early July in 1984 and late June in 1985), then increased to a second maximum in late July and early August. Osmotic potentials also varied in response to environmental conditions during the winter. ~ declined rapidly during October and November in 1983, 1984 and 1985 (Fig. 2A), associated with a rapid decrease in daily temperature without appreciable snow cover (Fig. 1). ~ increased briefly in December of all three years. These transitory increases were associated with increased daily temperatures in 1984 and in 1983 and 1985 with snow cover of the seedling shoots, van den Driessche (1989) has demonstrated that temperature has a large effect on osmotic potential of Douglas-fir. Thus, although osmotic potential varies seasonally in response to phenological condition, it also varies with temperature outside of the period of active shoot growth. The difference in osmotic potential between full turgor and the turgot loss point (A~), which is considered an indicator of turgor maintenance capacity and dehydration tolerance (Jones and Turner 1978), showed similar seasonal fluctuations in 1984 and 1985 (Fig. 3). The changes in Ag~ indicated that the tolerance of white spruce seedlings to dehydration was greatest from December to March, and began to decline in March to minimum values in late May. The decline in Ag~ preceded bud swelling by nearly two months. As was found by Grossnickle (1989), minimum A ~ , coincided with the period of rapid shoot elongation (Fig. 2B and 3).

Osmotic potential

Relative water content at turgor loss

The seasonal patterns in osmotic potential at full turgor (~100) and at the turgor loss point (tg~TLP)were similar but not identical in 1984 and 1985 (Fig. 2A), with the highest (least negative) values ( - 1.27 and - 1.49 MPa in 1984, and -1.00 and -1.15 MPa in 1985, respectively) measured in both years between late May and early June,

R W C T L P was, on average, lower in 1984 than in 1985 (Fig. 4B). For example, in 1984 the lowest and highest values of RWCTLP were 79 and 86.5% respectively, but were 81.8 and 92.5 %, respectively, in 1985. The ranges for both years are within those found previously (Colombo 1987, Grossnickle 1989). Drought-tolerant plants and

~t .

-I0

.

.

.

.

-~L~

~'"

"~"

~I2~"N~)"

o

-20 -30

:z o_ w

.30 20

o 10 0

gB3N D I J

F M Al~J

1

J A S 0 N O,J 984 ]

FM

A M J J A S 0 N D 1985

DATE

Fig. 1. Seasonal course of daily maximum (A) and minimum (9 temperature (top) and snow depth (bottom)

-LD

-1.5 < z~ - 2 , 0 o o

o

-2.5 -3.0 I

E" 20

I

I

I

I

I

I

I

1

I

I

I

I

I

I

I

I

I

I

I

I

I

I

1

I

l

I

600

B

9

Shoof Length

*

Needle Prirnordio

500

400

300

o~ 10

200 100 Z~ .

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

J g M A

k( A

1

.

1984

A S 0 HID 0

.

.

1985 DATE

Fig. 2A, B. Seasonal course of (A) osmotic potential at full turgor (D) and the turgor loss point (9 and (B) concurrent needle primordia (A) and shoot length (e) in white spruce seedlings

413 parison, the relative water content at which turgor loss occurs is functionally most closely to cell elasticity. Cell elasticity is the turgor loss over a given change in water content, and RWCTLP may be defined as the change in water content over which turgor declines from its maximum value to zero. Thus, RWCTLp reflects the average cell elasticity over the entire range of positive turgor.

..~ O.B

A

~o o 5~

0.4

~o

0.2

mo

Bulk modulus of elasticity 20

g ~0 5

0

ON DId F M A M I983

J J AS I984

0 N DIJ F M A M J J A S O N 1985

DATE

Fig. 3A, B. Seasonal course of (A) the differencein osmotic potential between full turgor and the turgor loss point and (B) total turgor in white spruce seedlings TURGOR

B 95

11[i

, 13,

i

i ]112115! 1 [3113115111' 3 i]2]3]11]1212] I I

]2]131

~90

o o c~

85

u

80

D

F M A

A S 0 N D

F M]A~MrJ~JPA 1985

S~O~N

DATE

Fig. 4A, B. Typical relationships between bulk modulus of elasticity (~) and turgor pressure (~e) found in this study (A) and (B) seasonal variation the e-~p relationship and relative water content at the turgor loss point in white spruce seedlings species with high turgor maintenance capacity generally have low RWCTLp, which permits stomatal opening over a wide range of water deficits (Jane and Green 1983). The results of the present study indicate that turgor maintenance capacity as indicated by RWCTLP is lowest in June, when the rate of shoot elongation is greatest. Relative water content at turgor loss was associated with seasonal osmotic adjustment: for example, from October 1983 to May 1984, RWCTLP (Fig. 4B) and W~ (Fig. 2A) followed similar trends. Changes in osmotic potential are attributable to varying moisture content, symplast volume or dissolved solute content. In c o r n -

It has been proposed (Tyree 1976) that ~ at high WP is most representative of plant cell wall elastic properties, and is, therefore, a better measure of drought tolerance than c at lowe values of We. However, it is also recognized that the dependence of ~ on WP makes the interpretation of its ecological significance difficult (Tyree and Karamanos 1981). In our view, single point values of ~, which may reflect a maximum water relations value, are not of overriding ecological significance in cases where plants experience a range of values of c over short periods of time. For this reason, our interpretation is that ~ is not necessarily a good measure of water relations or turgor maintenance capacity if considered only over a narrow range of RWC's. A better reflection of the importance of to turgor maintenance capacity may be obtained by considering cell elasticity over the full range of diurnal water potentials, which can be done using RWCTLP, the -We relationship, and WPTo~,. C is often turgor dependent (Bowman and Roberts 1985; Colombo 1987; Roberts et al. 1981; Robichaux 19841 Robichaux and Canfield 19851 Sinclair and Venables 1983). The form of the e - W e relationship characterizes the rate of change is turgor as symplast water volume decreases, and is therefore an important factor affecting turgor maintenance capacity. Estimates of e are increasingly biased as tissues approach the turgor loss point (Melkonian et al. 19811 Tyree 1981). As a result, the use of the term elasticity is technically inaccurate at low values of We. Despite this bias, values of ~ calculated at low We nevertheless partially reflect the change in bulk turgor per unit change in symplast water volume. We thus use the term ~, recognizing that at low WPsuch usage is technically inaccurate. In the present investigation, shifts in the e-WP relationship paralleled the seasonal trends in W~ and RWCTLP. During the growing season, when W~and RWC were both high, a Type 1 ~-WP relationship (Fig. 4A) predominated (Fig. 4B). During dormancy, when W~was more negative and RWCTLP lower, a Type 3 relationship was most common (Fig. 4B). Similar patterns were found in a previous greenhouse study of black spruce (Colombo 1987). The occurrence of particular forms of the ~ - We relationship as well as the absolute value of e at any RWC indicate the extent to which turgor maintenance capacity depends on: 1. water transport in response to increasing gradients in Ww (high a), or, 2. the capacity to maintain high turgor as tissue water content decreases (low ~). In this trial, maximum a usually ranged from about 10 to 15 MPa (data not shown), and seasonal variations were

414 not large. Greater seasonal variation in ~ was related to the dependence of a on Wv. Few hypotheses (cf. C o l o m b o 1987; Dainty 1972; Robichaux and Canfield 1985, Roberts et al. 1981) have been proposed concerning the ecological significance of different ~ - ~ p patterns. In general, a Type 3 relationship reflects greater and a Type 1 relationship reflects lower turgor maintenance capacity (Robichaux and Canfield 1985).

Total turgor pressure The greatest ~PTota~ (25.8 MPa) was found in January, 1984, during bud d o r m a n c y (Fig. 3B). ~VTotaldecreased rapidly from mid-March to late May, 1984, when buds became swollen and flushed (Fig. 2B). The lowest %'Tot,l (4.51 MPa) was measured M a y 28, 1984, when shoot elongation was most rapid. Low levels of ~PTotal (6.3 to 10.5 MPa) were maintained until September or October of all three years. gPTot,~ has been used to infer turgor maintenance capacity (Bannister 1987; C o l o m b o 1987; Roberts et al. 1980). Kikuta and Richter (1986) demonstrated that turgor adjustment and differences in total turgor pressure consist of two components : osmotic adjustment and adjustment of cell wall elasticity. Therefore, ~VTo,a~, which reflects both osmotic potential and cell wall elasticity, can be a more comprehensive indicator of turgor maintenance capacity than either ~ or e considered separately. ~PTot~ shows the turgor available to fully hydrated tissues. However, this capacity is seldom fully utilized, as plants experience water deficits even under well-watered conditions. Thus, although II/PTotalis indicative of turgor maintenance capacity, turgor pressure integrated between the limits of dehydration and rehydration will indicate to what extent the available total turgor is utilized (Colombo 1987; Grossnickle 1988). G r o w t h in spruce is sensitive to substrate water potential (Jarvis and Jarvis 1963). In the present study, shoot elongation and osmotic potentials declined concurrently in mid-summer during periods of high temperature and low humidity, even though nursery beds were irrigated. For example, from June 1 to July 30 in 1984 and from June 1 to June 30 in 1985, high temperatures with low humidities occurred with concurrent reductions in ~ and shoot elongation (Fig. 2A, B). A decline in ~TL~ in response to drought has been reported in white spruce (Koppenaal et al. 1991) and other coniferous species (Seller and Johnson 1985; Bongarten and Teskey 1986). The results of the present study suggest that white spruce can undergoe osmotic adjustment even when soil moisture is plentiful. In summary, white spruce is highly susceptible to growth check, which is characterized by stunted needles and p o o r leader elongation in planted trees, and is attributed primarily to post-planting moisture stress (Armson 1958; Mullin 1963; Burgar and Lyon 1968 ; Burdett et al. 1984). Our study demonstrates that white spruce is highly susceptible to growth check during shoot elongation, even under nursery conditions. O f particular importance in affecting this response were low total turgor pressure,

values of A ~ of only 0.1 to 0.2 MPa, and turgor loss occurring with the loss of as little as eight percent of total shoot water content. It might be concluded that transplant shock resulting f r o m drying soils and perturbation of the soil-root water conducting system exacerbates the occurrence of growth check in white spruce, which, as a result of its water relations characteristics, is physiologically predisposed to suffering low levels of turgor even with good moisture supply from the soil. This possibility deserves further study.

References Armson KA (1958) The effect of two planting methods on the survival and growth of white spruce (Picea glauea (Moench) Voss) in eastern Ontario. For Chron 34:252-259 Bannister P (1987) Water relations and stress. In: Moore PD, Chapman SB (eds) Methods in Plant Ecology. Blackwell London. pp 73-143 Blake TJ, Sutton RF (1987) Variation in water relations of black spruce stock types planted in Ontario. Tree Physiol 3:331-344 Bongarton BC, Teskey RO (1986) Water relations of loblolly pine seedlings of diverse geographic origins. Tree Physiol 1: 265-276 Bowman WD, Roberts SW (1985) Seasonal changes in tissue elasticity in chaparral shrubs. Physiol Plant 65:233-236 Burdett AN, Herring LJ, Thompson CF (1984) Early growth of planted spruce. Can J For Res 14:644-651 Burgar RF, Lyon NF (1968) Survival and growth of stored and unstored white spruce planted through the frost-free period. Ontario Department of Lands and Forests Research Report No. 64 Colombo SJ (1987) Changes in osmotic potential, cell elasticity and turgor relationships of second-year black spruce container seedlings. Can J For Res 17:365-369 Colombo SJ, Odlum KD (1984) Bud development in the 1982-83 overwintered black spruce container seedling crop. Ontario Ministry of Natural Resources, Forest Research Note No. 38. 4 p Dainty J (1972) Plant cell water relations: The elasticity of the celt wall. Proc R Soc Edinburgh (A) 70:89-93 Delucia EH, Schlesinger WH, Billings WD (1988) Water relations and the maintenance of sierran conifers on hydrothermally altered rock. Ecology 69: 303-311 Grossnickle SC (1988) Planting stress in newly planted jack pine and white spruce. 2 Changes in tissue water potential components. Tree Physiol 4:85-97 Grossnickle SC (1989) Shoot phenology and water relations of Picea glauca. Can J For Res 19:1287-1290 Hinckley TM, Duhme F, Hinckley AR, Richter H (1980) Drought relations of shrub species: assessment of the mechanisms of drought resistance. Oecologia 59:344-350 Hsiao TC, Acevedo E, Fereres E, Henderson DW (1976) Water stress, growth, and osmotic adjustment. Phil Trans R Soc London B 273 : 47%500 Jane GT, Green TGA (1983) Utilization of pressure-volume technique and nonlinear least squares analysis to investigate site induced stress in evergreen trees. Oecologia 57:380-390 Jarvis PG, Jarvis MS (1963) The water relations of tree seedlings. IV. Some aspects of water relations and drought resistance. Physiol Plant 16 : 501-516 Jones MM, Turner NC (1978) Osmotic adjustments in leaves of sorghum in response to water deficits. Plant Physiol 61 : 122-126 Kikuta SB, Richter H 0986) Graphical evaluation and partioning of turgor responses to drought in leaves of durum wheat. Planta 168 : 3642 Koppenaal RS, Tschaplinski TC, Colombo SJ (1991) Carbohydrate accumulation and turgor maintenance in seedling shoots and roots of two boreal conifers subjected to water stress. Can J Bot 69 : 2522-2528

415 Kramer PJ, Kozlowski TT (1979) Physiology of Woody Plants. Acad Press, New York. pp 447~452 Melkonian J J, Wolfe J, Steponkus PL (1982) Determination of the volumetric modulus of elasticity of wheat leaves by pressurevolume relations and the effect of drought conditioning. Crop Sci 22:116-123 Mullin RE (1963) Planting check in spruce. For Chron 39:252-259 Osonubi O, Fasehun FE (1987) Adaptations to soil drying in woody seedlings of African locust bean (Parkia biglobosa (Jacq.) Benth.) Tree Physiol 3:321 330 Ritchie GA, Shula RG (1984) Seasonal changes of tissue-water relations in shoots and root systems of Douglas-fir seedlings. For Sci 30:538-548 Roberts SW, Strain BR, Knoerr KR (1980) Seasonal patterns in leaf water relations in four co-occurring forest tree species: parameters from pressure-volume curves. Oecologia 46:330-337 Roberts SW, Strain BR, Knoerr KR (1981) Seasonal variation in leaf tissue elasticity in four forest tree species. Physiol Plant 52: 245-250 Robichaux, RH (1984) Variation in the tissue water relations of two sympatric Hawaiian Dubautia species and their natural hybrid. Oecologia 65 : 75-81 Robichaux RH, Canfield JE (1985) Tissue elastic properties of eight Hawaiian Dubautia species that differ in habitat and diploid chromosome number. Oecologia 66:7280 Scholander PF, Hammel HT, Bradstreet ED, Hemingsen EA (1965) Sap pressure in vascular plants. Science (Washington DC) 148 : 339-346 Seiler JR, Johnson JD (1985) Photosynthesis and transpiration of loblolly pine seedlings as influenced by moisture-stress conditioning. For Sci 31 : 742-749

Sinclair R, Venables WN (1983) An alternative method for analysing pressure-volume curves produced with the pressure chamber. Plant, Cell and Environment 6:211-217 Teskey RO, Grier CC, Hinckley TM (1984) Changes in photosynthesis and water relations with age and season in Abies amabilis. Can J For Res 14:77-84 Tyree MT (1976) Physical parameters of the soil-plant-atmosphere system: Breeding for drought resistant characteristics that might improve wood yield. In: Cannel MGR, Last FT (eds) Tree physiology and yield improvement. Acad Press, New York pp 329-348 Tyree MT (1981) The relationship between the bulk modulus of elasticity and the mean modulus of its cells. Ann Bot 47:547-559 Tyree MT, Hammel HT (1972) The measurement of turgor pressure and the water relations of plants by pressure-bomb technique. J Exp Bot 23:267-282 Tyree MT, Karamanos AJ (1981) Water stress as an ecological factor. Chap 14. In: Grace J, Ford ED, Jarvis PG (eds) Plants and their atmospheric environment. Blackwell Scientific Publications, Boston. pp 237-261 Tyree MT, Cheung YHS, MacGregor ME, Talbot AJB (1978) The characteristics of seasonal and ontogenetic changes in the tissuewater relations of Acer, Populus, Tsuga, and Picea. Can J Bot 56: 635-647 van den Driessche R (1989) Changes in osmotic potential of Douglas-fir (Pseudotsuga menziesii) seedlings in relation to temperature and photoperiod. Can J For Res 19:413~421