Trees (1997) 11: 462 468

Springer-Verlag 1997

O R I G I N A L A RT I C L E

Galina F. Antonova ? Victoria V. Stasova

Effects of environmental factors on wood formation in larch (Larix sibirica Ldb.) stems

Received: 3 July 1996 / Accepted: 7 February 1997

AbstractmEffects of temperature and precipitation on xylem cell production by the cambium, radial cell expansion and secondary wall thickening in larch stems have been studied. The observations were carried out over two seasons on ten 50- to 60-year-old trees, growing in central Siberia and chosen according to growth rate (the number of cells in radial rows of each of two of the preceding seasons was equal). The data on the number of cells in differentiation zones and mature xylem along radial rows of tracheids, radial and tangential sizes of tracheids and their lumina were used for calculating cambial activity, the rates and durations of cell development in the zones, and both the thickness and cross-sectional areas of tracheid walls. The mean day air temperature, mean maximum diurnal and mean minimum nocturnal temperatures as well as precipitation have been shown by correlation and regression analyses to affect differentially separate stages of tracheid differentiation. Throughout all the seasons it was temperature that had the main influence on the initial divisions in the xylem, radial cell expansion and biomass accumulation. However, the levels of such an effect on separate stages of cytogenesis were different, especially the influence of nocturnal temperature on xylem cell production by cambium and primary wall growth. The optimum values of temperature and precipitation for cell production by cambium, for radial cell expansion and secondary wall thickening have been calculated. These optimum values of the first and second processes proved to be practically equal, while the last differs considerably in response to temperature. The data are discussed in connection with formation of early and late tracheids. Key wordsmLarix sibirica ? Temperature ? Precipitation ? Wood formation (cambium activity, radial cell expansion, secondary wall thickening)

Introduction

G.F. Antonova ( ) ? V.V. Stasova V.N.Sukachev Institute of Forest, Siberian Branch of Russian Academy of Sciences, Krasnoyarsk, 660036, Russia

The effects of environmental factors on conifer wood formation are reflected in the number of tracheids produced by the cambium, their outer sizes, and the thickness of cell walls (Richardson 1964; Larson 1964; Denne 1971, 1974, 1976; Denne and Smith 1971; Ford et al. 1978; Necesany 1971; Mahmood 1971; Wodzicki 1960,1971; Antonova and Shebeko 1981a, 1986; Antonova et al. 1983). To understand the mechanism of the influence of ecological factors on wood formation it is important not only to evaluate the results of such influences (radial diameters and thickness of cell walls) but also to estimate the effects of the factors on the process responsible for these results. Consequent stages of formation of the cells by cambium and their development in each of differentiation zones have been found to be independent processes and their reactions to environmental factors can be different (Antonova and Shebeko 1981a; Antonova et al. 1983). These findings are supported by earlier observations (Larson 1960; Wodzicki 1964) and confirm the supposition that radial cell expansion and secondary wall thickening are under different physiological controls (Larson 1960; Richardson 1964; Wodzicki 1964; Zahner et al. 1964). That is why it is necessary to investigate the effects of ecological factors on separate stages of cytogenesis. We used such an approach in studying wood formation in Scots pine trees growing in central Siberia (Antonova and Stasova 1993). The study of the effects of both diurnal and nocturnal temperatures as well as precipitation on the processes of cell production by cambium, the growth of cambial derivatives by expansion and secondary wall thickening allowed us to find out which factor was the most important at successive stages of Scots pine tracheid differentiation, and to determine the optimum values of temperature and precipitation for each stage. The same approach was used in studying the influence of temperature and precipitation on wood formation in the stems of larch (Larix sivirica Lbd.) trees growing in the same stands where Scots pine growth was investigated. The paper presents the data on the effects of the mean day air

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temperature, the mean maximum diurnal temperature, and the mean minimum nocturnal temperature, as well as precipitation, on the number of xylem cells produced by the cambium, the extension growth and secondary wall thickening of these cells. The optimum values of factors influencing each stage of differentiation have been calculated by regression analysis.

Materials and methods

The study was carried out over two seasons (1979, 1980) at a natural stand (the site index II, density of stoking 0.8, composition 60% of Pinus sylvestris L., 20% of Larix sibirica Lbd., 10% Betula pendula Roth, 10% Picea obovata Lebed.), located 45 km north of Krasnoyarsk in the forest-steppe of Siberia. Ten 50- to 60-year-old L. sibirica trees were chosen so that the average number of tracheids in the radial rows of each of the two preceding seasons was equal and had a normal distribution. The trees with the reaction wood were eliminated. The average tree height was 20 m, and the average stem diameter was 18 cm. For extracting the samples from the larch stems a special punch was used. The sample had 0.8 cm diameter and contained the wood of the previous 2 or 3 years, the growing annual layer with cambial zone and the adjacent layer of phloem. Dead outer bark was removed before cutting the samples. The samples (one from each tree) were collected every 10 days, beginning from May to September, in a spiral up the stems, avoiding the effect of ringing. The average height of sampling was 1.3 m. The cores were placed in formalin-ethanol-acetic acid (5:90:5) and kept there before making an analysis. The cross-sections (two on each sample) were stained with 0.05% water solution of cresyl violet, which gave the specific colours of the cell layers at different stages of development (Antonova and Shebeko 1981b) and then examined at 100 1000 magnification with a light microscope. All measurements were carried out with an ocular micrometer. The error of the linear size measurements was 0.65 mm. The standard errors of the means of all the measured and calculated parameters were not more than 5%. The number of cells within the zones of cambium, radial cell expansion, secondary wall thickening and mature xylem of the annual layer being formed were calculated. In the present work all cells having approximately equal small radial sizes were considered to be cells of the cambial zone. The cambial zone included the cambial initials and their derivative mother and daughter cells (Wilson et al. 1966). The beginning of visible increased radial diameter was considered to be the beginning of radial cell expansion. Final growth of radial cell diameter and the beginning of secondary cell wall formation were defined by the appearance of pit borders and rounding of the cell corners (Murmanis and Sachs 1969). The end of the maturation zone was defined by the absence of visible traces of the cytoplasm in the tracheid lumina. The average number of tracheids in mature annual wood layers of 1979 and 1980 were 40 and 32 cells, respectively. Radial and tangential sizes of each tracheid and its lumen within the radial rows in the zones of the mature cells and cells at different stages of development were measured on eight radial rows of tracheids chosen by their maximal sizes. Selection of the larger tracheids ensured cutting the cells within the limits of the principal part of their length where the tracheid sizes are constant and thus characterized their real development. The data obtained have been used for calculating: 1. Cambial activity as the number of the divisions of fusiform cambial initials, producing both xylem and phloem derivatives in different periods of observation by Mahmood's method (Mahmood 1971). Newman's observation (1956) that one division of cambial initial at the edge of the xylem resulted in four derivative tissue cells served as the basis of this method. The

division of the fusiform cambial initial at the edge of the phloem produced two sieve cells. 2. The thickness and the cross-sectional area of tracheid walls along the radial row of annual increment. The tracheid crosssectional areas and lumen cross-sectional areas were calculated taking the tracheid shape at cross-section as a rectangle. Cell wall cross-sectional areas were calculated by subtracting lumen cross-sectional areas from tracheid cross-sectional areas. The tracheid wall cross-sectional area (or wall thickness) was used as the index of biomass accumulation in tracheid walls. Such a possibility has been shown earlier (Antonova and Stasova 1990), while studying the changes of cell wall cross-sectional area and the biomass quantity per unit of tracheid length along the radial row of tracheids. The data on temperature and precipitation have been obtained from the meteorological station at the Forest Institute approximately 10 km from the sample site. The corresponding temperatures measured were summarised for the whole period of the development, starting from the time when the cell appeared outside the given zone to the beginning of the appearance of the cell in this zone, which was determined by the duration of the development of the cell or the group of cells in the zone (Antonova and Stasova 1988). The data were used for computing of the mean day, mean maximum diurnal and mean minimum nocturnal temperatures. This was performed as follows: 1. For every period of observation the number of the cells that have finished development in the zones of radial cell expansion and secondary wall thickening was determined. 2. Duration of the development of these cell groups in the given zone was calculated by a modification of the Wodzicki method (Antonova et al. 1981a). 3. The sum of corresponding temperatures measured every day throughout the period of development, starting from the time when the cell left the given zone, was calculated. 4. The calculated sum was divided by the duration of development in the zone. For revealing the precipitation effect both the sum of precipitation during development and the index precipitation per day were used. The study of the relationship of formation, growth and development of tracheids to air temperature and precipitation was made by correlation and regression analysis using the data for each season. In addition, while studying the relationship between the initial division number, air temperature, and precipitation, the 2-year data were used both as a whole and separately for May June and July August.

Results and discussion

At the beginning of a vegetative season (the end of May June) the dependence of the number of initial divisions producing xylem cells on air temperature is positive (Fig. 1a c) and the correlation coefficients are very high (mean day temperature r = +0.86, maximum temperature r = +0.78, minimum temperature r = +0.78) In July, the warmest month, the temperature is not a limiting factor and its effect on xylem cell production by cambium is more complicated. There are some optimum values of the temperatures studied, higher temperatures cause the number of initial divisions to decrease (Fig. 1e g). According to the computation, the highest cambial activity was recorded at a mean day temperature of 20 21 C, the mean maximum diurnal temperature of 25 C and the mean minimum nocturnal temperature of 11 12 C. Lowering the nocturnal temperature to 7 8 C decreased the cambium activity of larch.

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The dependence of cambial initial divisions in the xylem side on precipitation is more adequately described by 2nddegree equations (Fig. 1d, h), than by the correlation coefficients. The residual variance of the linear equation and the 2nd-degree equation were 0.506 and 0.272 in June and 0.328 and 0.290 in July, respectively (P = 0.001 and P = 0.1). The curves obtained show precipitation of approximately 2 mm/day to be optimal for xylematic cambium initial divisions. The small difference in the precipitation necessary for the highest production of xylem cells by larch cambium in June (Fig. 1d), when the soil moisture is still available, and in July (Fig. 1 h), when precipitation is the main source of moisture, may be conditioned by the high water storage in the stem and low use of such water for transpiration (Schulze et al. 1985; Arneth et al. 1996). Besides this may be due to the ability of the larch stem to absorb moisture by the bark when the stem is washed by rain. Zahner (1963) considered this way of increasing the water storage of the inner tissues of the tree stem as essential. The contribution both of the mean day temperature and precipitation in cambium activity can be estimated using multilinear regressions (Table 1). As the regressions describe the process adequately (P = 0.05 and P = 0.01) comparison of the absolute values of the regression coefficients allow the share of each factor in the process to be estimated.

Fig. 1 a pmInfluence of the mean day temperature, mean maximum diurnal temperature, mean minimum nocturnal temperature and precipitation on the cambial initial division number in May June (a d) and July August (e h), the radial diameters (i l) and wall crosssectional areas (m p) of larch tracheids

According to these data temperature influenced cambial initial division, especially xylem cell production, more than precipitation, throughout the season. Radial diameter growth Considering the influence of the two factors on radial cell growth (Table 1), according to the coefficient values of multilinear regression, temperature also has the principal effect on radial cell expansion of larch cambium derivatives throughout the season. The minus sign before the coefficient shows that in this case the dependence is complicated. The equations of 2nd degree have been found to describe this dependence more adequately than the linear one (Fig. 1 i, g, k). By using the dependences obtained the optimum values of temperature, favouring the radial cell growth, have been determined. Of the mean day temperatures the most favourable for the growth of tracheid primary walls was 22 23 C, and of the diurnal ones 26 27 C. If the diurnal temperature rose further, the radial tracheid diameter de-

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Fig. 2mInfluence of mean maximum diurnal temperature on the rate of substance accumulation in the tracheid walls during secondary wall thickening

(mm

Fig. 3mInfluence of mean maximum diurnal temperature on the tracheid development duration in the secondary wall thickening zone

Table 1mCoefficients characterizing the dependence of cell production by cambium, radial cell expansion and secondary wall thickening of larch tracheids on temperature and precipitation Process Coefficients of multilinear regression ac Division of cambial initials in side of: Phloem+xylem May-June July-August Xylem May-June July-August Radial cell expansion (drada, mm) Secondary wall thickening (Sb, mm) (DS, mm2?day1?cell1)
a b

Comment (on precipitation)

Mean day temperature

Precipitation

3.542 0.269 2.32 1.449 +58.505 715.051 45.733

+0.327 +0.091 +0.207 +0.126 0.907 +56.99 +3.444

+0.317 +0.0165 +0.157 +0.0051 0.102 +7.680 +5.494

50.05 50.10 50.10 50.05 50.01 50.05

Per Per Per Per

day day day day

During the development period During the development period Per day

radial diameter of tracheids cell wall cross-sectional area

creased. Practically the same optima have been found for the radial growth of the tracheids of Scots pine growing in the same stand (Antonova and Stasova 1993). A decrease in growth activity and its cessation at a high diurnal temperature have been reported elsewhere (Mahmood 1971; Larson 1967; Denne 1971; Cregg et al. 1988). Since the primary cell walls occupy 7 8% of the total volume of the cell biomass (Grozdits and Ifju 1984), they do not require a large quantity of assimilates for their development. Therefore the decreased photosynthesis and assimilate transport, as well as their increased expenditure on the respiration at high temperatures, cannot be the cause of the reduced primary cell growth activity. One of the reasons for the response of growth to temperature rise may be due to the changes in the physical properties of tracheid walls. When, as a result of transpiration, the water sources in the tree stem are depleted, the xylem water potential

decreases (Hellkvist 1973; Hellkvist and Parsby 1976; Kaibiyainen et al. 1981; Kramer and Kozlowski 1979; Schulze et al. 1985). According to Nonami and Boyer (1990a, b) low water potential is the main reason for the decrease in the expansion growth rate because of changes in such physical properties of walls as flexibility and hydraulic conductivity. These physical properties can change due to the enhanced interaction of wall polysaccharides because of diminishing water activity and the action of water as a plasticizer (Nobel 1970). At the level of the cell the water stress directly influences the cell wall metabolism of cambial derivatives, reducing the incorporation of glucose in tracheid cell walls (Whitmore and Zahner 1967). Besides, enzyme activity decreases under water stress since enzymes work effectively only if they are hydrated (Suleimanov et al. 1971).

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A nocturnal temperature of 12 C has been found to affect negatively the primary wall growth. So the effects of a nocturnal temperature of 11 12 C on the processes of cell production by cambium and development of primary walls of cambium xylem derivatives are in direct opposition (Fig. 1 g, k). A rise of night temperature to 15 C or fall to 9 C resulted in increased tracheid radial diameters. These results are in agreement with earlier data for the radial cell expansion of the Scots pine growing in the same stand (Antonova and Stasova 1993). A negative effect of temperature of about 10 C on growth activity was recorded in many plants and was accounted by the state of membranes (Kursanov 1976). Although a positive influence of precipitation on radial cell expansion is evident the authors failed to determine their optimum values by the analysis of a 2nd-degree equation with one factor. However, by solving the 2nddegree regression equation with two factors, the optimum values of both the mean day air temperature (21 C) and precipitation have been determined. On this evidence, the precipitation must amount to at least 14 15 mm throughout the period of tracheid development in the radial cell growth zone. The optima of the mean maximum diurnal temperature and mean minimum night one have been found to be 27 C and 14 C, respectively. Cell wall thickening The optimum conditions for secondary wall development differ considerably from the conditions for the highest cambium activity and the maximum radial cell expansion. According to the computation, secondary wall development of the tracheids reaches maximum values at the mean day temperature of 15 17 C, the mean maximum diurnal temperature of 21 23 C and the mean minimum nocturnal temperature of 8 9 C (Fig. 1 m o). Temperature exceeding these limits causes a sharp decrease in the quantity of the biomass accumulated in tracheid walls. The same results have been obtained from the analysis of the dependence of the tracheid secondary wall development in the Scots pine growing in the same stand and during the same years (Antonova and Stasova 1993). A negative influence of night temperature on tracheid wall thickness in seedlings of Pinus sylvestris, P. resinosa and Douglas fir has been reported earlier (Denne 1971; Larson 1967; Richardson 1964). On the other hand, the substance synthesis rate, expressed as cell wall cross-section area increment per day per cell (n S/day ? cell), increases with the rise both of the mean day temperature and the mean diurnal one to 21 22 C and 26 27 C (Fig. 2), respectively. The positive influence of air temperature on wall thickening rate was also recorded by Denne (1971) and Wodzicki (1971). Stimulative action of the temperature appears to be related to the activation of enzymes and the ability of membranes to transport substances. However, at the same time, increased temperature can result in an increased moisture deficit, lower water potential in xylem, slower phloem

transport, which was recorded in many plants at temperatures higher than 22 25 C (Kursanov 1976), and increased assimilate expenditure on respiration (Larson 1967; Richardson 1964). Moreover with higher temperatures the duration of the secondary wall thickening process is reduced (Fig. 3), while the duration of tracheid development in the maturation zone has a significant influence on secondary wall thickness (Wodzicki 1971; Antonova et al.1983). The decrease of the duration of tracheid development in the secondary wall thickening zone with increased temperature was reported for other conifers (Whitmore and Zahner 1966; Denne 1971; Antonova and Stasova 1993). This appears to be related to the acceleration of the protoplast disintegration as the temperature acts undifferentially and intensifies not only the synthetases, but also hydrolases, which results in lysis of the protoplast. The latter process has a great importance as early or late finishing of the maturation phase significantly influences the tracheid wall thickness (Wodzicki and Brown 1973; Antonova and Stasova 1993). The dependence of the thickness of cell walls on the development duration in the secondary wall thickening zone (r = +071, P = 0.01) accounts for the reduction of the amount of biomass accumulated in larch tracheid walls with the rise of mean day temperature to over 16 17 C, and the mean maximum diurnal temperature to over 21 22 C (Fig. 1 m, n). According to the data of Shcherbatjuk et al. (1990), air temperature of 14 16 C is optimum for the apparent photosynthesis of Larix sibirica, growing at Lake Baikal, i.e. in the region which is very close in its climatic conditions to the region where the study has been carried out. So the increase of the tracheid wall cross-section area (or thickness) in the larch at an elevated temperature corresponds to the direct dependence of cell wall thickening on substrate availability. According to the coefficients of multilinear regression, the temperature effects on the wall cross-section area (i.e on the biomass accumulation) of tracheids are stronger than the precipitation effects (Table 1). However, the latter has a positive influence on the tracheid secondary wall thickening in conifers (Zahner 1963), and in larch in particular (Table 1). In drought years, for example 1980, this dependence is particularly distinct (r = +0.84, P = 0.05). In wet seasons, exceeding a certain moisture level causes a decrease in substance deposition, which reduces cell wall thickness. By the values of multilinear regression coefficients the precipitation influences the substance deposition rate in cell walls more than temperature (Table 1) while, as it is noted above, the final amount of biomass depends more on temperature. Such a distinction may be determined by the processes governing two characters of the wall thickening process itself the rate and duration of tracheid development in the zone. The rate depends on the transport of photosynthetates, their assimilation, compound synthesis and substance transfer into the wall. In all cases water availability is a necessary condition (Kramer 1964; Kramer and Kozlowski 1979). As mentioned above the duration of thickening

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depends significantly on the lysis of protoplast, which in turn is strongly dependent on temperature. By the results of the regression analysis of 2nd-degree equations the optimum conditions, favourable for the greatest accumulation of substances in tracheid walls, i.e. the highest biomass productivity, have been established. According to the data the mean day temperature is 16 C at precipitation of 2.3 2.5 mm/day throughout the period of maturation. The analysis of all the data reveals different influences of temperature and precipitation on different stages of cytogenesis resulting in wood formation. So, if the processes of cell production by cambium and radial cell expansion are similar in their temperature requirements, the process of secondary wall thickening differs sharply. However, the former two processes can also sometimes be different in their temperature requirements. For example, in July, a rise of the mean minimum nocturnal temperature to 10 11 C promotes an increase of the number of xylematic initial divisions, while the development of tracheid radial diameters is minimum at such temperatures. Similar dependences were reported for Scots pine (Antonova and Stasova 1993). Different influence of temperature and precipitation on the separate stages of tracheid differentiation shows some independence of the stages taking part in the integral process of wood formation. It is the difference in the requirements of warmth and moisture necessary for primary and secondary cell wall development that determines the formation of early and late tracheids. The formation of late-wood is initiated by the water stress arising in the tree tissues as a result of the absence of precipitation in the depletion of the water storage in the soil. The biochemical reasons for the events in the cambial zone resulting in late-wood formation have been connected to the changes in the contents and composition of some polysaccharides in cell walls in the cambial zone (Antonova 1996). The development of the radial diameters of larch early tracheids occurs mainly in June, of late ones in July, when most of the early tracheids are in the maturation zone (Antonova and Stasova 1992). The thickening of early tracheid walls was recorded mainly in July. High temperatures in July promote intensified synthesis of cell wall components, but reduce the time of tracheid development in the secondary wall thickening zone. As a result the early tracheids have thin walls. Due to the rise in temperature in July the number of cambium initial divisions decreases as does the radial diameter of late tracheids. In August, when the development of late tracheid secondary walls occurs, the temperature conditions are favourable for the use of photoassimilates in synthetic processes, and the accumulation of substances in cell walls, which leads to the formation of tracheids with thick walls. Thus, it is impossible to reach simultaneously the largest radial diameters and the largest wall thickness of tracheids. Consequently, a solution to the productivity problem by simultaneous increase of cell number, radial diameter and wall thickness of tracheids is not feasible. Therefore, the solution to the productivity problem must be based on a compromise between the conditions necessary for the

processes involved in wood formation. However, it appears possible to control the process resulting in the formation of wood with required properties, i.e. containing a higher percentage of early or late tracheids, which in its turn depends on how the wood is to be used.
AcknowledgementsmThe authors thank Dr. V.D. Stakanov for the data on meteorological factors and V.D. Perevoznikova for technical assistance.

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