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Department of Land, Air and Water Resources, University of California, Davis, California 95616. ABSTRACT ... In this paper, we study the effectof temperature on spatial ... h at the appropriate temperature before photography for growth.
Plant Physiol. (1988) 87, 529-532 0032-0889/88/87/0529/04/$0 1.00/0

Effect of Temperature on Spatial and Temporal Aspects of Growth in the Primary Maize Root' Received for publication September 25, 1987 and in revised form February 22, 1988

ALI M. PAHLAVANIAN AND WENDY KUHN SILK* Department of Land, Air and Water Resources, University of California, Davis, California 95616 ABSTRACT In the range 16 to 29°C, increases in temperature caused large (twoto threefold) increases in growth velocity, growth strain rate, and biomass deposition rate in primary roots of maize, Zea mays L. Temperature had small effects on root diameter, fresh weight density, and dry weight density, and negligible effects on length of the growth zone and growth strain at particular positions.

The spatial distribution of growth in the primary root of maize has been known since the work of Erickson and colleagues in the 1950s (7, 8). Growth is conveniently measured with the root tip as origin of the coordinate system since, empirically, a steady (time invariant) pattern is found in this 'co-moving' reference frame. Growth velocity, i.e. rate of displacement of a cellular particle from the root tip, increases with distance until a constant velocity is achieved at the base of the growth zone. The derivative of velocity with respect to position is the relative elemental growth rate or longitudinal strain rate. A plot of relative elemental growth rate versus position shows the spatial distribution of elongation growth. During growth, cellular particles accelerate through the growth zone and experience in a temporal sequence the velocities and strain rates that are usually shown as functions of position. The past decade has seen the development of a comprehensive framework for growth analysis, based on concepts from continuum mechanics. The relationship between spatial and temporal aspects of growth has been explored (2, 11, 13-15). A particularly useful relationship is the 'growth trajectory,' a plot of particle position versus time. If growth is steady (i.e. if the plot of growth velocity versus position is time invariant), then, in a cell file, successive root cells have similar growth trajectories (11, 14). In this important special case, the growth trajectory provides a quantitative description of spatial-temporal interrelationships and can be used to infer the time course of developmental variables whose spatial distribution is known. The growth trajectory can also be used to infer the length of material elements of root as they are displaced through the elongating zone. Since element length is the distance between basal and apical ends of the element, the growth trajectory of the apical end of an element can be subtracted from the trajectory of the basal end to estimate segment length as a function of time or position (9, 11). In this paper, we study the effect of temperature on spatial and temporal distributions of growth velocity, strain rate, diameter, and density in the primary root of maize. In addition, we explore spatial-temporal relationships by examining element

length as a function of time and position at different temperatures between 16 and 29°C. MATERIAL AND METHODS Experimental and Numerical Methods. Seeds of Zea mays L. (cv WF9 x mol7) were germinated, seedlings were cultivated, and roots were marked for growth analysis as described in previous publications (16, 17). All seeds were germinated at 29°C for 30 h. Selected seedlings with terminal radicles 3 to 5 mm long were transplanted to growth medium (moist vermiculite wetted with 4 ml 0.1 mm CaC12 per g vermiculite) in plexiglass boxes incubated at 16, 19, 24, or 29°C. For most experiments, seedlings were allowed to grow until roots were 5 cm long. The incubation times were 48 h at 16°C, 36 h at 19°C, 25 h at 24°C, and 17 h at 29°C. Roots which were 5 + 0.5 cm long were selected for marking with an ultrafine 'uniball' pen with water soluble black ink. Marked roots were allowed to grow undisturbed for 1 to 2 h at the appropriate temperature before photography for growth analysis. Numerical methods for growth analysis and deposition rates were as described in previous publications (16, 17). Length of the growth zone was determined by recording for each root the position at which maximum growth velocity first occurred and averaging these positions within temperatures. Semi-Empirical Growth Trajectories. In our experiments, marks were diluted by growth, and mark trajectories could be followed for only about 8 h. A semiempirical growth trajectory was constructed by choosing marks with different initial positions. First, the growth trajectory was estimated by numerical integration of the velocity field (11, 13). Then individual marks were identified on five roots grown at 29°C. The initial position of each mark was assigned the time associated with the position on the estimated trajectory, i.e. the marks in the initial time frame were plotted on the solid line. Subsequent positions at 15-min intervals were plotted for each of the marks to obtain a composite growth

trajectory.

RESULTS Longitudinal Growth. A temperature increase caused an increase in growth velocity at all locations (Fig. 1A). The smallest relative effect was in the most apical region. Local elongation rate is characterized by the longitudinal strain rate (relative elemental growth rate) which increases with temperature at all locations (Fig. 1B). Maximum strain rate occurred near 5.5 mm and ranged from 0.17 h- at 16°C to 0.40 h - 1 at 29°C. The length of the growth zone, 12 mm, was not significantly affected by temperature (Table I). Thus, whether they were growing rapidly at high temperature or more slowly at lower temperature, tissue elements elongated until they were displaced 12 mm from the apex. Growth Trajectories and Element Lengths. Growth trajectories measured over an 8 h period (Fig. 2, symbols) were in good

1 Supported by grant DCB8417504 from the National Science Foundation. 529

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Plant Physiol. Vol. 87, 1988

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Distance from root tip (mm) FIG. 1. Characterization of longitudinal growth. A, Velocity (of displacement from root tip) as a function of position. Growth velocity increased with temperature at all locations. B, Growth strain rate (relative elemental growth rate) obtained as the derivative of velocity with respect to position. Strain rate increased with temperature.

Table I. Length of the Growth Zone as a Function of Temperature n Temperature Length of Growth Zone mM °C 7 12.34 ± 1.08 16 11.49 ± 1.23 19 8 24 9 12.07 ± 0.71 12.15 + 1.39 29 10 agreement with the growth trajectory calculated as the integral of particle velocity over time (Fig. 2, solid line). It can be seen that, for the most part, later positions of initially apical particles overlap the earlier positions assigned to more basal marks. Thus, displacement of a material particle follows the pattern computable from the instantaneous velocity field. This confirms that, at least over an 8 h period, growth of the corn root was fairly steady, in agreement with Erickson's conclusions from streak photo-

graphs (7, 8). Temperature increases shifted the growth trajectory to the left (Fig. 3A). Displacement from 2.5 mm to 12 mm required 17 h at 16°C and less than 8 h at 29°C. Length of a material root element can be obtained from growth trajectories of neighboring particles. At a particular time, element length varied with temperature (Fig. 3B). But when element length is shown as a function of position, temperature had a smaller effect (Fig. 3C). That is, the amount of elongation seems to have been synchronized with displacement to produce

a profile of relative growth which is less dependent on temperature-induced rate changes. Whether it moved from 2 to 7 mm quickly at a high temperature or slowly at a lower temperature, an element of root tissue which was initially 0.1 mm long was 0.6 mm long at the more basal location. This agrees with preliminary observations (17) which were made on the basis of previously published work on corn roots in different laboratories. Root Thickness. During growth, root elements expand in radius as well as length. In the apical millimeter, new cell files are added; and root radius increases rapidly with distance from tip. In the more distal regions cells expand in width, and intercellular spaces develop. The plot of root radius versus distance increases more slowly in the 3- to 12-mm region. (The thickening associated with secondary growth begins distal to the primary growth zone shown here.) When roots of the same length (6 cm) were compared, temperature had a small but significant effect on root shape (Fig. 4). Roots grown at 19°C were, on average, 1.0 mm thick at the base of the growth zone; while roots grown at 24 or 29°C were 1.3 mm in diameter. The apical 2 mm of tissue appears to have had the same shape at three temperatures, but beyond the region of cell division the roots grown at colder temperature were more cylindrical; the roots grown at higher temperatures were more conical. Fresh Weight and Dry Weight. The distributions of fresh weight and dry weight (per unit root length) are important aspects of root structure. These properties change slowly with time, root length, and temperature. Roots 6 cm long all had fresh weight density which increased with distance in the apical 3-mm region (Fig. 5A). Temperature effects were not significant here. In the distal part of the growth zone, fresh weight increased more slowly with distance. Per unit length, the roots grown at 29°C were slightly heavier than those grown at the two lower temperatures. Dry weight per unit length, in contrast to fresh weight, peaked in the second and third millimeters (Fig. 5B). Apparently, in the rapidly expanding zone, the root accumulates water at least as rapidly as it deposits biomass. Roots grown at 29°C had a slightly greater dry weight than those grown at the lower temperatures. Profiles of dry weight density (Fig. 5B) are not smooth or closely spaced enough for good spatial resolution of the biomass (dry weight) deposition rate profile. Since the growth rate was faster at higher temperatures (Figs. 1 and 3B), it is clear from the similarity in graphs of biomass at different temperatures that the rate of biomass production must be greater in the faster

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FIG. 3. Growth trajectories and element lengths as a function of temperature. A, Growth trajectories estimated by numerical integration of the velocity field. Temperature increases caused the particles to move more rapidly through the growth zone. B, Length (in mm) versus time for an element initially extending from z = 2.50 mm to z = 2.60 mm. At higher temperatures, element length increased more rapidly with time, although mature (final) length was probably independent of temperature. C, Element length versus position. Temperature had a smaller effect on growth strain as a function of position.

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growing roots. Calculations based on the continuity equation (10, 13, 14) confirm that temperature had a large effect on rate of biomass production (Table II). This is to be expected, since temperature increased the rate of development without large changes in root density or morphology. Especially between 24 and 290C, net local biomass production rate, calculated from the

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Table II. Biomass Deposition Rates at Different Temperatures Biomass Deposition Temeraur P Temperature Rate Rt mm ,g dry weight mm - I h °C 19 3 19 20 3 24 30 3 29 14 6 19 21 6 24 35 6 29 o

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continuity equation, at the location 6 mm from the tip, increases from 21 ug mm-' h-l to 35 ,g mm-' h.

DISCUSSION The results of this study show that temperature has large effects on developmental rates and small or negligible effects on the synchronized sequence of developmental events. Thus growth velocity, growth strain rate, and biomass deposition rate are strongly temperature dependent. Root shape (diameter versus position curves) and root density are slightly temperature dependent, and length of the growth zone and total strain at any location are independent of temperature. These temperature effects differ from the effects of water stress on root development. Marking experiments on corn roots have revealed that the length of the growth zone is shortened by water stress, while the time over which growth occurs is independent of water stress (12). Relatively few growth analyses based on marking experiments are found in the physiological literature. However, tests of the relationships found here can be made by examination of anatomical records. In roots of maize, like many other monocots, cell division occurs only in a small region near the tip. Gandar (10) has confirmed that cell division ceases distal to z = 3 mm. Furthermore, the distribution of growth velocity and cell division rate are thought to be steady. If these two assumptions are valid, in the distal 9 mm of the growth zone element length at any position relative to element length at, say, z = 3 mm, can be estimated as the ratio in cell lengths at the two positions, 1(z)l 1(3). The limit of the growth zone can be identified as the region where cell length becomes invariant with position. Thus, the general validity of relationships shown here can be checked by computations based on cell lengths. From anatomical studies (3, 4) it seems that wheat roots and onion roots, like the maize roots of this study, appear to have growth zones whose length, while shortened by water stress, is unaffected by temperature. Less universal is our inference that strain (relative length increase) varies only with position and not with temperature-affected growth rate.Carmona and Cuadrado (4) found that, in the onion root, cell size increases with temperature at the apical end of the elongation zone but is invariant with temperature at the basal edge of the growth zone. If these

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two relationships are generally true, then total strain in the 'elongation only' zone must decrease with temperature. Bertaud and Gandar (2) also found growth strains were smaller at a higher temperature in roots of timothy grass. It is not clear whether the numerical methods used to obtain our Figures 3B and 3C are adequate to reveal the finer details of the interrelationships among element size, position, and temperature. A small change in velocity at an apical position would be compounded through the numerical integration to result in large variation in element length in distal regions. And the relative uncertainty is greatest in measurement of apical velocity because of both digitizing error and naturally occurring temporal oscillations in size of the root cap. Baldovinos (1) has published data on cell size in corn roots as a function of position and temperature. These data indicate that cell length increases with temperature at all locations. Calculations show that relative cell length change in the 3 to 5 mm region is invariant with temperature, in agreement with the conclusions reached here. On the other hand, Erickson's observation (6) of invariance of mature metaxylem cell length with temperature would appear to contradict our conclusions. Studies of cell length profiles in roots grown at different temperatures are needed to resolve this question. LITERATURE CITED 1. BALDOVINos G 1953 Growth of the root tip. in WE Loomis, ed, Growth and Differentiation in Plants. Iowa State College Press, Ames, pp 27-54 2. BERTAUD D, P GANDAR 1975 Referential descriptions of cell proliferation in roots illustrated using Phleum pratense L. Bot Gaz 146: 275-287 3. BURSTROM H 1953 Studies on growth and metabolism of roots IX. Cell elongation and water absorption. Physiol Plant 6: 262-276 4. CARMONA M, A CUADRADO 1986 Analysis of growth components in Allium roots. Planta 168: 183-189 5. DIEZ J, J LoPEZ-SAEZ, F GONZALEz-BERNALDEZ 1970 Growth components in Allium roots. Planta 91: 87-95 6. ERICKSON R 1959 Integration of plant growth processes. Am Nat 63: 225-235 7. ERICKSON R, D GODDARD 1951 An analysis of root growth in cellular and biochemical terms. Growth Symp 10: 89-116 8. ERICKSON R, K SAX 1956 Elemental growth rate of the primary root of Zea mays. Proc Am Philos Soc 100: 487-498 9. ERICKSON R, W SILK 1980 The kinematics of plant growth. Sci Am 242: 134-

151 10. GANDAR P 1980 The analysis of growth and cell production in root apices. Bot Gaz 141: 131-138 11. GANDAR P 1983 Growth in root apices. I. The kinematic description of growth. II. Deformation and the rate of deformation. Bot Gaz 144: 1-10, 11-19 12. SHARP R, W SILK, T HSIAO 1988 Growth of the maize root at low water potentials. I. Spatial distribution of expansive growth. Plant Physiol. 87: 5057 13. SILK W 1984 Quantitative descriptions of development. Annu Rev Plant Physiol 35: 479-518 14. SILK W, R ERICKSON 1979 Kinematics of plant growth. J Theor Biol 76: 481501 15. SILK W, S HAIDAR 1986 Growth of the stem of Pharbitis nil: analysis of longitudinal and radial components. Physiol Veg 24: 109-116 16. SILK W, T HsIAO, U DIEDENHOFEN, C MATSON 1986 Spatial distributions of potassium, solutes, and their deposition rates in the growth zone of the primary corn root. Plant Physiol 82: 853-858 17. SILK W, R WALKER, J LABAVITCH 1984 Uronide deposition rates in the primary root of Zea mays. Plant Physiol 74: 721-726