Planta

Planta (1989) 177:6(~73

9 Springer-Verlag 1989

A kinematic analysis of tepal growth in Lilium longiflorum Kevin S. Gould * and Elizabeth M. Lord** Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA

Abstract. Time-lapse marking experiments indicate that the growth of tepals in Lilium longiflorum

Thunb. from 3.7 m m to maturity is triphasic. Phase I (tepal lengths 3.7-10 ram) is characterized by spatial and temporal variation in growth rate and, in the epidermis, a random distribution of mitoses with an acropetal increase in cell area. During phase II (10-90 mm) cell elongation and (later) cell division is restricted largely to basal regions. Cell division ceases when tepals are less than one-third of their mature length of 155 mm. Phase III (90-155 ram) is characterized by the gradual transition from basal to apical growth, and a modification of epidermal cell shape. A sharp peak in growth at the extreme tip of the tepal coincides with anthesis. Key words: Cell division - Cell size - Growth analysis - Lilium (tepal growth) - Tepal growth

Introduction

There is a paucity of quantitative information on the growth and development of floral organs. This is despite Greyson's (1972) proposition that descriptions of changes in the relative contributions of cell size and cell number to growth patterns are powerful tools for examining phylogenetic trends. Previous workers have described the ontogeny and histogenesis of the perianth (Satina 1944; Boke I948; Tepfer 1953; Tucker 1959; Kaplan 1968; Dermen and Stewart 1973; Nishino 1976) and-or the fusion events leading to the formation * Present address: Department of Botany, University of Auckland, Private Bag, Auckland, New Zealand ** To whom correspondence should be addressed Abbreviations: LRGR = local relative growth rate; RER = rela-

tive elemental rate of growth

of a corolla tube (Daniel and Sattler 1978; Nishino 1978, 1982, 1983a, b; Dubuc-Lebreux and Sattler 1984). Boke (1948) determined from staining intensities of cells in transverse and longitudinal section that, for Vinca rosea, both sepal and petal primordia exhibit a short initial period of apical and marginal growth followed by intercalary growth near the base. Daniel and Sattler (1978) provided good quantitative data on the spatial distribution of mitoses from sections of four corolla tubes of Solanum dulcamara following colchicine treatment. Conclusions on the growth of an organ based on sections alone presuppose (i) a steady-state distribution of growth centers, and (ii) a close relationship between meristematic activity and actual enlargement of the organ. Marking experiments have shown that in lily anthers, the regions of growth are constantly shifting, so that a longitudinal section through any one developmental stage would overemphasize the importance of growth of a particular region (Gould and Lord 1988). In the absence of kinematic data on the distribution of growth, the same criticism might well hold true for the perianth. If the growth of the perianth is indeed a nonsteady system, then the colchicine treatment used by Daniel and Sattler (1978) could have masked local differences in cell-division activity, producing instead a cumulative picture of all the dividing regions over the exposure period. Moreover, there is evidence that organ enlargement and the pattern of cell division are not tightly correlated. Both shoots and roots can grow normally for a period after cell division has been completely inhibited by irradiation with gamma rays (Foard and Haber 1961 ; Haber 1962; Foard 1971), or following colchicine treatment (Foard et al. 1965). We aim to provide a kinematic description of perianth growth, by providing quantitative data

K.S. Gould and E.M. Lord: Analysis of tepal growth in Lilium

67

on the spatial distribution of growth, epidermal cell size and mitotic activity along tepals of Lilium longiflorum Thunb. from a young stage (3.7 m m long) to maturity (approx. 155 m m long). Tepals are the members of the kind of perianth that is not differentiated into calyx and corolla (Esau 1977). Tepals of Lilium are particularly large and elongate rapidly (Erickson 1948), and are, therefore, excellent material for this kind of study.

determine the average velocity of displacement v(i) of any one point over 5 d, estimated by differentiation using a quadratic, five-point smoothing formula (Erickson 1976): v0) = [ - 2 X(i _ 2) - -

SOn) = Vi,(n+ I ) - -

Materials and methods Bulbs of Lilium longiflorum cv. Nellie White (Dahlstrom& Watt Bulb Farms, Smith River, Cal., USA) were planted in pots and grown in a greenhouse in Riverside until floral buds were formed. At least two weeks prior to marking, the pots were transferred to a growth chamber at 2 5 ~ with a photon fluence rate of 1 mmol (photons). m - 2. s- 1 (Philips, Eindhoven, The Netherlands; cool white fluorescent lamps) and an 18-h photoperiod.

Marking experiments. One of the three sutures that unite the outer whorl of adjacent tepals was marked, using a toothpick, with an approximately equidistant file of dots of carbon as a viscous mixture with water. The dots were not more than 1 mm apart initially. In total, 40 tepals were marked over a six-month period, one tepal per plant. The initial bud length varied from 3.7 to 156.6 ram. For buds less than 6 mm in length, the youngest leaves and bracts had to be bent back or excised before marking. This procedure did not affect the overall relative rate of elongation as compared to control (unmarked) tepals, the lengths of which were measured daily over a 14-d period. Each marked tepal was photographed alongside a reference scale using Kodak Technical Pan black and white film (Eastman Kodak, Rochester, N.Y., USA), and the tepals were rephotographed at 24-h intervals over 3-30 d. Intervals shorter than 24 h were tested; however, the overall growth in these cases was not sufficient to resolve clearly any spatial differences in growth rate. Additional marks were applied when the tepals had grown so that adjacent dots were always less than 5 mm apart. Prints were enlarged to a final magnification of 40 times and developed for maximum contrast. The distance separating each dot from the base of the tepal was recorded from the prints using a Summagraphics (Fairfield, Conn., USA) digitizer and bit pad data tablet coupled to an IBM (Boca Raton, FI., USA) personal computer. Data manipulations were performed using the spreadsheet software Supercalc 4 (Computer Associates International, San Jose, Cal., USA). For each set of data over a 24-h time-lapse, a running refit analysis was undertaken (Erickson 1976; Hunt 1982), using overlapping sets of four consecutive points as the measured distances. Any increment in the distance between the four points, when divided by the original distance, gave a measure of the local relative growth rate (LRGR) for that segment of tepal. The L R G R of each region was plotted against distance from the base of the tepal (the median distance for the original set of four points). Relative elemental rate of growth (RER) may be defined as the rate of elongation of an infinitesimally small point along an organ at any one instant in time (Erickson 1976; Silk 1984). The R E R was calculated for sets of data taken over five or more consecutive days. The first step in the analysis was to

1 X(i

1 ) -~ 1 X(i + 1 ) -~

2 x(i + 2)1 / 10 t

where x0)= distance of that point from the base of the tepal on day i, and t = the time interval (1 d). This operation was undertaken for every mark along the tepal, and the resultant velocities were plotted against distance from the base. From this plot, the R E R (S) was calculated as the slope between any three points, estimated by:

Vi,(n-l)/Xi,(n+l)--Xi(n-1)

where n = the mark number from the base. Relative elemental growth rate (units-d-i) was plotted against distance f}om the base of the tepal. The R E R profiles indicate the spatial distribution of growth, and provide more smoothing than the LRGR. For phase I, computations of L R G R were chosen to bring out the rapidly shifting growth peaks. For phases II and III, R E R was computed to emphasize the apparent basal and apical trends. (Plots of L R G R for phases II and I I I - not shown - were in good agreement with R E R plots.)

Cell measurements. Ten tepals (of lengths ranging from 4.8 to 145 mm) from different control plants were fixed in formalinacetic acid or 90% ethanol. They were partially cleared in 80% ethanol overnight at 70 ~ C, washed, and then stained overnight by the Feulgen procedure (see O'Brien and McCully 1981). They were slowly dehydrated over 24 h through an ethanol series, cleared in Histo-Clear (National Diagnostics, Somerville, N.J., USA), and mounted on glass slides with Permount (Fisher Scientific Co., Fair Lawn, N.J., USA). A narrow strip of abaxial epidermis in these cleared mounts, approx. I mm in from the midrib and extending from the base to the tip of each tepal, was examined under a light microscope. Using an ocular grid, the total number of nuclei, as well as those undergoing mitosis, were counted for sequential grid areas, measuring 0.4 mm 2 for tepals smaller than 57 mm or 0.6 mm 2 for larger ones. The spatial distribution of cell frequencies within each tepal was analyzed by )~2. Mean cell areas were estimated by dividing the grid area by the total number of nuclei. Internal cell layers in these cleared tepals were also examined for mitotic figures, though it was not possible to follow a discrete file of cells in these tissues.

Results

Growth profiles. Marking did not perturb the insitu relative rate of elongation (0.103. d - ~), as measured previously for anthers (Gould and Lord 1988). The growth of lily tepals from 3.7 m m to maturity can be separated into three distinct phases, as determined from the surface-marking experi-. ments (Table 1). Our observations are based on a total of 217 plots showing the spatial distribution of L R G R and a further 50 plots of RER. Phase I is a period of spatial and temporal variation in growth rate. It occurred from the earliest stage examined (3.7 mm) to a tepal length of 1013 mm. The growth profile was not one of r a n d o m fluctuation. Rather, there was a progressive rise

68

K.S. Gould and E.M. Lord: Analysisof tepal growth in Lilium

Table 1. Summaryof marking experiments on tepals of Lilium longiflorum. Data from 217 plots of relative growth rate. The number of tepals from which each set of plots was derived is shown in parentheses

Phase III (90 mm to anthesis, during the decline phase of growth) was characterized by a shift from basal to apical growth (Fig. 3). Again, plots of R E R an L R G R were similar at comparable tepal lengths. Basal regions elongated more slowly, while ever more distal regions grew faster. The transition culminated in the exclusive growth at the tip, coinciding with the onset of anthesis.

Number of plots Length

Position of growth maximum (% distance from base)

Phase mm

Total

0 25

26-50 51 75 76-100

I

46 (11) 32 (8) 49 (15) 36 (10) 20 (8) 14 (8) 20 (9)

12 22 37 32 15 6 1

11 5 7 3 4 3 3

II

III

3.7- 9.9 10- 19.9 20- 29.9 30-- 59.9 60-- 89.9 90-119.9 120-150.0

16 3 0 0 0 2 7

Cell area. When viewed collectively, the spatial profiles of epidermis cell areas of the 10 tepals form a developmental sequence (Fig. 4a-j). In the three youngest tepals examined (lengths 4.8, 5.0, and 7.2 mm) epidermal cells at the tip were significantly larger than those at the base (P0.05). In the next two larger tepals (Fig. 4g, h) basal cells were highly significantly larger than more apical ones (P < 0.001). The transition to phase III is shown clearly in the cell-area profile of a 104.4-mm tepal (Fig. 4i). For this tepal, and all smaller ones, all cells were a similar, columnar shape, and cell area is, therefore, an appropriate index of cell length. In the largest tepal examined (145 mm, at anthesis) there were regional differences in cell shape, from columnar in the basal, trichome zone, through highly irregular cells with wavy anticlinal walls in more

7 2 5 1 1 3 9

and-or fall in L R G R along the tepal. The location of the growth peak did not shift predictably on a day-to-day basis (Fig. 1). The peak was least often located at the distal quarter of the tepal (Table

1). Phase II (tepal length 10-90 mm, during the exponential phase of growth) was characterized by strong basal growth, with a progressive decline in growth rate toward the tip (Fig. 2; Table 1). Plots of R E R were similar to those of L R G R . Initially, the progressive decrease in growth was linear with respect to increasing distance away from the base (Fig. 2a). In older tepals, the plot of R E R versus position was curvilinear (Fig. 2b). In 23 out of 137 plots of phase-II growth, small, transient spurts of growth were observed at the extreme tip of the tepal (Fig. 2 b). These peaks were normally smaller than those at the base, recorded in Table 1.

0.3

/

A

0.3

0.2

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~ o

00 "

14.1

"

-O.t

-

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0

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~

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DISTANCE FROMTEPALBASE (mm)

"

U.I

""

.

r

z

'

O

1

2

3

4

5

6

7

B

DISTANCE FROMTEPAL BASE (mm)

Fig. I a, b. Local relative growth profiles of one Lilium tepal over six consecutive days during phase I. Initial length (mm): c3-E3 6.3, day 1 2; zx-zx6.8, day 2 3; m-a 7.6, day 3-4; A-A 8.2, day 4-5; o-o 8.7, day 5 6. For clarity, the profiles of days 1-3 are shown in a; those of days 3-6 are shown in b

K.S. Gould and E.M. Lord: Analysis of tepal growth in Lilium

0.20

Z ,-,

0 20

a

!

69

t

0.t5

0.t5

o.io

o.lo

0.05

0.05

0.00

I

0

!

4 B 12 DISTANCEFROMTEPALBASE (mm)

0.00

|

10 20 30 DISTANCE FROMBASE (mm)

40

Fig. 2a, b. Relative-elemental-rate profile for lily tepals during early and late phase II. Initial length (mm): a 11.2, day 3; b 36.7, day 15

0.35 G"

~. 0.3o '9C

0.t5 0.i0

i

f'~.-s

Z i-,r

..

. ,..,

o.o5 0.00

. "...,

Ill::~:"

9 I

0

5;

t00

150 DISTANCE FROM TEPAL BASE (mm]

Fig. 3. Relative-elemental-rateprofiles of one lily tepal over

three consecutive days during phase III. Length (ram): - 111.1;--- 119.0; ... 132.2 (anthesis)

central regions, to more regular polyhedral cells at the tip (Fig. 4j). Cell area is not an accurate index of cell length in the mature tepal, therefore. This could account for the absence of an increase in cell size at the extreme tip of the mature tepal (a sharp rise in longitudinal growth at the apex was characteristic of tepals at anthesis, as shown by marking experiments). Cell division. Mitosis ceases in the abaxial epidermis of lily tepals when they are less than one-third of their mature length (only 3 out of 11 265 cells were dividing in the 39.2-mm tepal, and no mitotic figure was observed in the next stage examined, tepal length 48.8 mm). Cell division in the inner parenchyma and adaxial epidermis apparently ceases at a similar stage; the largest tepal in which mitoses were observed in these tissues was 39.2 m m long. Overall mitotic indices of the abaxial epidermis were extremely low, ranging from 0.03% (tepal length 39.2 ram) to 1.5% (12.8 ram), and it is difficult to assess the importance of local variations.

There were no significant spatial differences in mitotic index (P>0.05) in the 4.8-mm tepal (Fig. 5a). In the 12.8-mm tepal there were two discrete bands of mitoses, one in the basal 10% and the other, with higher counts, peaking at 60% of the length from the base (Fig. 5 b). This bimodal distribution of the mitotic index was very similar to that given by Daniel and Sattler (1978)for a 1.2-mm-long corolla of Solanum dulcamara. In the 20.4-mm lily tepal (Fig. 5c) mitotic figures were most common in the basal 25%, although a second, smaller band was present near the midpoint. In the 39.2-mm tepal, mitotic figures occurred exclusively at the base (Fig. 5 d). Distributions of mitoses in the inner tissues of each tepal were very similar to those of the abaxial epidermis at comparable stages. Discussion

There are three distinct phases of growth of the lily tepal from the 3.7-mm stage onwards. Steadystate kinematics (in which the spatial distribution of growth does not change over time) apply only to the growth during phase II. This phase of predominantly basal growth is not simply the: result of a basal intercalary "meristem". The onset of phase II precedes the shift of mitosis to the base, and phase-II growth outlasts cell division altogether. Our data would indicate, therefore, that the pattern of growth is not correlated with the spatial distribution of mitosis. This observation has been reported previously for different experimental systems. In anthers a waveforin pattern of growth persists both during the phase of cell division, and long after the last cell has divided (Gould and Lord 1988). Wheat seedlings irradiated with x-rays so that mitosis is completely inhibited will produce one new leaf primordium in the normal phyllotact-

70

K.S. Gould and E.M. Lord: Analysis of tepal growth in Lilium 700

a:

1800

f

IGO0

600

1400 500 1200 400

F:=

2

I000

4

1000

2400

800

1900

600

1400

400

2

900

4

900 (12) (21..) c" co r---,-m

u t-'(12)

10

I0

30

20

20

30

40

3300 2700

700 2100

500

1500

300

4

2

900

6

iO00

6000

800

4500

600

3000

9o0

400

4

t0

20

30

40

50

t500

t2

i0001

800 700

600

4

B

12

,

t 2u

Distance

from base

mm

Fig. 4a-i. Variation in epidermis cell area along 10 lily tepals, lengths (ram) a 4.8; b 5.0; c 7.2; d 12.8; e 20.4; f 39.2; g 48.8; h 56.0; i 104.4; j 144.6 (mature). Class intervals (ram): a-h 0.4; i, j 0.6. Local differences in cell shape in the mature tepal are shown. In the younger tepals, all cells were a similar, columnar shape

K.S. Gould and E.M. Lord: Analysisof tepal growthin Lilium 1.5

x a_1 -c~ ~--

9,-~

0.0

c.~

2.5

5

a

0.5

2

4

1 C

2 I 0

1.5

1.5

0.0

4

8

12

16

20

4

t2

2.5 2.0

0.5

b

3

2.0 cD

71

1.0 i 0.5 0.0

d

t0

Distance from base

20

30

mm

Fig. Sa--d. Variation in mitotic index along the length of the epidermisof four lily tepals, lengths (mm) a 4.8 ram; b 12.8ram; e 20.4; d 39.2 mm

ic position (Foard 1971). Cellular differentiation of leaf and root primordia in 7-irradiated seedlings parallels normal development (Foard and Haber 1961), and leaf primordia formed prior to the treatment maintain the normal allometry in terms of leaf length and width after mitosis is inhibited (Haber 1962). Colchicine-treated roots continue to produce lateral root primordia (Foard et al. 1965). While cell division does not modify the growth pattern, there is evidence that the growth pattern itself, or else factors which control the growth pattern, can modify the spatial distribution of mitosis. In tepals, the shift of mitosis to the extreme base follows the growth shift at the onset of phase II. In young anthers, the pattern of cell division complements the pattern of growth that persists both during and after cell division. The processes of cell division and cell elongation would appear, therefore, to be coupled by a common, underlying factor. The kinematics of phase-I growth, a period of spatial and temporal variation in relative growth rate, remain the least well-understood. Phase-I growth profiles of tepals were similar to the growth profiles of lily anthers throughout their development (Gould and Lord 1988). Unlike in anthers, however, there was no regular or predictable directionality to the shifting growth peak. P a t c h e s of cells along the tepal suddenly elongated at rates

substantially higher than those of other regions, apparently at random. It is difficult to correlate the growth data from marking experiments with the cell-size profiles of phase-I tepals, in which cells at the tip were invariably larger than those at the base. Green (1976) has shown that the cell length in a particular region is an integral of all that region's previous developmental histories (rates and patterns of cell division and cell elongation from inception). In other words, the cell-area profile of any one phase is the result of what has occurred at the cellular level in previous stages. There may be an additional phase of tepal growth, one of predominantly apical growth, occurring earlier than what we have termed phase I (i.e. at primordial stages). During phase I the spatial and temporal variation in growth rate results in an overall diffuse growth zone encompassing most of the tepal; this would serve to accentuate differences in the cell-area profile that had been established during the earlier phase. Further work is required on the spatial distribution of growth of lily tepals at the primordial stages. The shift from basal to apical growth during phase III (see Fig. 3), might be interpreted as the transport or diffusion of any residual growth factor from phase II. During phase II of tepal growth, mitotic divisions in the anther cease, meiosis is

72

K.S. Gould and E.M. Lord: Analysis of tepal growth in Lilium

completed, and pollen differentiates. The pollen of lily is a rich source of gibberellins (Barendse et al. 1970), a plant hormone which has been implicated in the elongation growth of petals at anthesis (Pharis and King 1985). Phase III of tepal growth (the expansion wave from the base to the apex) may well be induced by gibberellins transported from the stamens to the tepals. The sharp peak in growth at the tip in the mature tepal coincides with anthesis, and may actually initiate the separation of tepals from the closed bud (separation proceeds basipetally). The epidermal cells of Ipomoea tricolor also undergo rapid enlargement and modification of shape during anthesis (Phillips and Kende 1980). Goethe (1790) was the first to suggest that petals and leaves are structural homologues. In general, ontogenetic and cytohistological studies have supported this theory (Tepfer 1953; Tucker 1959; Kaplan 1968; Dermen and Stewart 1973 ; Nishino 1976), though Dermen and Stewart (1973) found that in Prunus persica internal tissues of the calyx are derived mostly from the third layer of the floral apical meristem (in leaves, the internal tissues are derived exclusively from the second layer). It would be interesting, then, to compare our observations on the later stages of growth of the perianth with those of leaves. The most comprehensive analyses of leaf growth have been undertaken on tobacco. Richards and Kavanagh (1943) reexamined Avery's (1933) data on growth of the tobacco leaf. They calculated the strain rates for four leaf lengths, and showed clearly the transition from predominantly basal growth (phase II, in our terminology) to a more centrally located growth peak (phase III). Poethig and Sussex (1985) examined the profiles of relative rate of elongation and mitotic index for one leaf, originally 10 mm long, over eight consecutive days. A period of spatial variation in relative growth rate and mitotic index immediately preceded the phase of basal growth. This earlier stage may equate to phase I of tepal growth. However, since the leaf was clearly in a transitional stage at the start of the analysis, it is difficult to be certain. Further work on the early growth distribution of the foliage leaf is required. The available evidence would indicate that tepals and leaves share common patterns of growth, supporting the theory that members of the perianth are leaf homologues. The three phases of tepal growth were clearly defined from the marking experiments. It is possible that the three phases correspond to the lag, exponential, and decline phases of growth. Phase I would not have been predicted from the cell pro-

files alone, and none of the phases would have been so clearly delimited from the mitotic counts alone. On the other hand, the cell-area profiles of younger tepals indicate that there is an even earlier phase of growth, at the primordial stage, which is not readily accessible to marking. It would be interesting to compare the spatial aspect of tepal growth with the material one by presenting a history of the development through time of small portions of the tepal. By combining kinematic analysis and the more usual procedures of plant microtechnique it is possible to obtain a more complete description of the growth of an organ. We thank Dr. Wendy Silk (University of California, Davis) for her expert advice during the course of this study, Dr. Paul Green (Stanford University) for prereviewing the manuscript, and Jeffrey Hill for his editorial comments. Dahlstrom Watt Bulb Farms provided the lily bulbs. This work was supported by National Science Foundation grant PCM-8512062 and by Biomedical Research grant No. 2 S07-RR07010-5.

References Avery, G.S., Jr. (1933) Structure and development of the tobacco leaf. Am. J. Bot. 20, 565-592 Barendse, G.W.M., Rodriques-Pereira, A.J., Berkers, P.A., Driessen, F.M., van Eyden-Emons, A., Linskens, H.F. (1970) Growth hormones in pollen, styles and ovaries of Petunia hybrida and Lilium species. Acta Bot. Neerl. 19, 175 186 Boke, N.H. (1948) Development of the perianth in Vinca rosea L. Am. J. Bot. 35, 413-423 Daniel, E., Sattler, R. (1978) Development of perianth tubes of Solanum dulcamara: implications for comparative morphology. Phytomorphology 28, 151-171 Dermen, H., Stewart, R.N. (1973) Ontogenetic study of floral organs o f peach (Prunus persica) utilizing cytochimeral plants. Am. J. Bot. 60, 283-291 Dubuc-Lebreux, M.-A., Sattler, R. (1984) Quantitative distribution of mitotic activity during early corolla development of Solanum dulcamara L. Bot. Gaz. 145, 22-25 Erickson, R.O. (1948) Cytological and growth correlations in the flower bud and anther of Lilium longifIorum. Am. J. Bot. 35, 729-739 Erickson, R.O. (1976) Modelling of plant growth. Annu. Rev. Plant Physiol. 27, 407-434 Esau, K. (1977) Anatomy of seed plants, 2nd edn. John Wiley, New York Foard, D.E. (1971) The initial protrusion of a leaf primordium can form without concurrent periclinal cell divisions. Can. J. Bot. 49, 1601-1603 Foard, D.E., Haber, A.H. (1961) Anatomic studies of gammairradiated wheat growing without cell division. Am. J. Bot. 48, 438446 Foard, D.E., Haber, A.H., Fishman, T.N. (1965) Initiation of lateral root primordia without completion of mitosis and without cytokinesis in uniseriate pericycle. Am. J. Bot. 52, 58(~590 Goethe, J.W. (1790) Versuch die Metamorphose der Pflanzen zu erkl~iren. Gotha Gould, K.S., Lord, E.M. (1988) Growth of anthers in Lilium longiflorum: a kinematic analysis. Planta 173, t61 171 Green, P.B. (1976) Growth and cell pattern formation on an

K.S. Gould and E.M. Lord: Analysis of tepal growth in Lilium

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axis: critique of concepts, terminology, and modes of study. Bot. Gaz. 137, 187-202 Greyson, R.I. (1972) Alternative goals for flower morphology. In: Advances in plant morphology, pp. 28-32, Murty, Y.S., Johri, B.M., Mohan Ram, H.K., Varghese, T.M., eds. Sarita Prakashan, Meerut, India Haber, A.H. (1962) Nonessentiality of concurrent cell divisions for degree of polarization of leaf growth. I. Studies with radiation-induced mitotic inhibition. Am. J. Bot. 49, 583589 Hunt, R. (1982) Plant growth curves. The functional approach to plant growth analysis. University Park Press, Baltimore, Md., USA Kaplan, D.R. (1968) Structure and development of the perianth in Downingia bacigalupii. Am. J. Bot. 55, 406420 Nishino, E. (1976) Developmental anatomy of foliage leaves, bracts, calyx and corolla in Pharbitis nil. Bot. Mag. Tokyo 89, 191-209 Nishino, E. (1978) Corolla tube formation in four species of Solanaceae. Bot. Mag. Tokyo 91, 263~77 Nishino, E. (1982) Corolla tube formation in six species of Apocynaceae. Bot. Mag. Tokyo 95, 1-17 Nishino, E. (1983a) Corolla tube formation in the Tubiflorae and Gentianales. Bot. Mag. Tokyo 96, 223-243 Nishino, E. (1983 b) Corolla tube formation in the Primulaceae and Ericales. Bot. Mag. Tokyo 96, 319-342 O'Brien, T.P., McCully, M.E. (1981) The study of plant structure: principles and selected methods. Termarcarphi, Melbourne, Australia

Pharis, R.P., King, R.W. (1985) Gibberellins and reproductive development in seed plants. Annu. Rev. Plant Physiol. 36, 517-568 Phillips, H.L., Kende, H. (1980) Structural changes in flowers of Ipomoea tricolor during flower opening and closing. Protoplasma 102, 199-215 Poethig, R.S., Sussex, I.M. (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165, 158-169 Richards, O.W., Kavanagh, A.J. (1943) The analysis of the relative growth gradients and changing form of growing organisms: illustrated by the tobacco leaf. Am. Naturalist 77, 385-399 Satina, S. (1944) Periclinal chimeras in Datura in relation to development and structure (a) of the style and stigma (b) of calyx and corolla. Am. J. Bot. 31, 493-502 Silk, W.K. (1984) Quantitative descriptions of development. Annu. Rev. Plant Physiol. 35, 479-518 Tepfer, S.S. (1953) Floral anatomy and ontogeny in Aquilegia formosa var. truncata and Ranunculus repens. Univ. Calif. Publ. Bot. 25, 513 648 Tucker, S.C. (1959) Ontogeny of the inflorescence and 1Lheflower in Drimys winteri var. chilensis. Univ. Calif. Publ. Bot. 30, 257-336

Received 11 April; accepted 30 August 1988

A kinematic analysis of tepal growth in Lilium longiflorum.

Time-lapse marking experiments indicate that the growth of tepals in Lilium longiforum Thunb. from 3.7 mm to maturity is triphasic. Phase I (tepal len...
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