A morphometric analysis of leaf development in Vitis riparia, and grape cultivars Concord and Vivant

CHRISTIAN R. LACROIX' AND USHER POSLUSZNY Qepartment of Botany, University of Guelph, Guelph, Ont., Canada NlG 2W1

Received January 22, 1990

LACROIX, C. R., and POSLUSZNY, U. 1991. A morphometric analysis of leaf development in Vitis riparia, and grape cultivars Concord and Vivant. Can. J . Bot. 69: 400-406.

This study investigates the initiation of leaf shape in three taxa of Vitis from a quantitative point of view. Leaf characters, such as angles between major veins, ratios of the length of leaf lobes, of leaf lobes and sinuses, and of petioles and leaf lobes, were measured on leaves of different sizes and compared against leaf blade length (an indirect measure of develop- mental time) to see if there were differences between them at different developmental stages, and between taxa. Two trends were observed. Characters dealing with angles between major leaf veins, and those dealing with the ratio of the distance to the first point of branching of the major leaf vein of a lobe and the length of that leaf lobe, showed relatively little change over leaf blade length compared to more variable characters such as those involving the leaf petiole, leaf sinuses, or leaf lobes. If we assume that leaves of different lengths represent leaves at different stages of development, we can say that the characters dealing with angles or venation do not change extensively over time. However, characters dealing with ratios of the distance to a leaf sinus and lobe length, ratios of the length of two leaf lobes, or those dealing with the ratio of the length of the petiole and lobe length showed a stronger indication of change over leaf blade length. The parameters of interest in most of these ratios (petiole length or sinus depth compared against the length of a leaf lobe) varied more at different leaf blade lengths. It was also possible to distinguish between taxa for characters dealing with leaf lobes, petioles, and sinuses.

Key words: morphometry, leaves, Vitis, development, characters, shape.

LACROIX, C. R., et POSLUSZNY, U. 1991. A morphometric analysis of leaf development in Vitis riparia, and grape cultivars Concord and Vivant. Can. J . Bot. 69 : 400-406.

Cette Ctude examine I'initiation de la forme de la feuille d'un point de vue quantitatif chez trois taxa du genre Vitis. Des caracteres comprenant certains parametres de la feuille, tels les angles entre les veines principales, les rapports entre la longueur des lobes de la feuille, des lobes et des sinus, et du petiole et des lobes, ont CtC mesurCs sur des feuilles de diffkrentes longueurs et compares 2 la longueur du limbe (une mesure indirecte de son stade de dCveloppement), pour determiner si les mesures de ces caractkres different a diffkrents stades de dCveloppement et entre taxa. Deux patrons ont CtC observts. Les caracteres comprenant les angles entres les veines principales de la feuille et ceux mesurant le rapport entre la distance au premier point d'embranchement de la veine principale d'un lobe et la longueur totale de ce lobe changent tres peu sur diffkrentes longueurs du limbe de la feuille en comparaison aux charactbres plus variables comme ceux qui comprennent le pCtiole, les sinus et les lobes. Supposant que les feuilles de diffkrentes longueurs representent des feuilles 2 differents stades de dCveloppement, on peut conclure que les caracteres qui comprennent les angles ou la nervation ne changent pas consi- dCrablement dans le temps. Cependant, les caracteres qui comprennent les rapports entre la distance du point d'attachement du pCtiole sur la feuille 2 un sinus et la longueur d'un lobe, les rapports entre la longueur de deux lobes, ou les rapports entre la longueur du petiole et la longueur d'un lobe dCmontrent un changement plus accentuC sur diffkrentes longueurs du limbe de la feuille. Les parametres d'intCr&t dans la plupart de ces rapports (la longueur du pCtiole ou la profondeur d'un sinus en comparaison a la longueur d'un lobe) varient plus i diffkrentes longueurs du limbe de la feuille. I1 a CtC Cgalement possible de distinguer entre taxa en utilisant les caracteres comprenant les lobes de la feuille, le pCtiole ei les sinus.

Mots clks : morphomCtrie, feuilles, Vitis, dCveloppement, caracteres, forme.

Introduction Merrill 1986; Sugiyama and Hara 1988), as well as our visual

Ampelographic characters (i.e., characters used for the identification of grape vines) are diverse and specific. Char- acters that apply to fully developed leaves are considered important in distinguishing between commercially cultivated grape varieties (Galet 1979; Office International de la Vigne et du Vin 1983). Although there is always some degree of variation between leaves within a specific taxon, certain rec- ognizable features persist throughout later stages of develop- ment and give the leaf a basic shape or structure. Are these specific features present or distinguishable in the early stages of development of leaf primordia?

Several recent studies on leaf development (Dengler 1984; Gould et al. 1986; Jeune 1987; Meicenheimer et al. 1983;

observations on young stages of leaf development in certain Vitis taxa (C. R. Lacroix and U. Posluszny, unpublished) con- firm that differences between basic leaf shapes are visible at very early stages of development, especially with respect to pubescence and to the prominence of leaf lobe tips and leaf sinuses. Of further interest in Vitis riparia and cultivars Vivant and Concord is the quantitative analysis of some leaf param- eters at different stages of development to determine if they are also established from initiation. For the purposes of this study, three taxa were selected: V. riparia, cultivar Concord, a hybrid of uncertain origin but with a strong Vitis labrusca parentage, and cultivar Vivant, another hybrid with a complex background involving 'Concord'. Although the leaves of all three taxa share a common structure. that is thev have five

'Present address: Department of ~ i ~ l ~ ~ ~ , University of Prince lobes and palmate venation, they are different frombne another Edward Island, 505 University Ave., Charlottetown, P.E.I., Canada in several ways, especially in the general shape of their lobes CIA 4P3. and the prominence or depth of sinuses between lobes.

Pnnted In Canada 1 Impnmi: au Canada

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LACROIX AND POSLUSZNY 40 1

The characters of interest deal with several structural fea- TABLE 1. Description of characters used tures of Vitis species. For example, angles between the major Character Points veins of the fully developed leaf have been the subject of category No. Description on Fig. 1 investigation for several years in the Vitaceae (Dorsey 1912; Galet 1979; Viala and PCchoutre 1910). However, major vein Angles 676 Angle to first lobe 1-2-3 angles have never been measured in early stages of initiation 677 Angle lobe 1 - lobe 2 3-24

and during development to see if they differ. Similarly, char- 679 Angle lobe 3 - lobe 4 5-2-6 680 Angle to fifth lobe 1-2-7

acters such as the location of the initiation of the first lateral vein on the major vein of a leaf lobe have not been investigated 660 Ratio 1st vein lobe Illobe 1 2-1212-3

developmentally. The same also applies to ratios of the length 66 1 Ratio 1st vein lobe 2llobe 2 2-13/24 663 Ratio 1st vein lobe 4llobe 4 2-1512-6

between major leaf lobes or between major leaf lobes and 664 Ratio 1st vein lobe 5llobe 5 2-1612-7 sinuses.

Although the final shape of the leaf involves many factors (Cusset 1986; Steeves and Sussex 1989), early events of ini- tiation are believed to play an important role in development. The quantitative analysis of growth patterns has provided insight into the elaboration of leaf shape (Cogliatti and Guitman 1984; Dengler 1984; Wolf et al. 1986). This type of analysis, however, has rarely been extended to the very earliest stages of initiation or the early establishment of specific leaf struc- tures. Therefore, the major objectives of this study are (i) to determine if specific quantitative characters (angles between major leaf veins, and ratios of the length of several leaf param- eters) change significantly during development, and (ii) to determine if there are differences between taxa in the expres- sion of these characters.

I Materials and methods

Developing shoots of Vitis riparia Michx., Vitis cv. Vivant and Vitis cv. Concord were collected during the summer of 1989 from the vineyards of the Horticultural Research Institute of Ontario at Vineland, Ontario.

A total of 12 twigs bearing 11-18 leaves were collected for each taxon over four dates (July 19, August 3, August 30, September 20). A total of 529 leaves (186 V. riparia leaves, 176 'Vivant' leaves, and 167 'Concord' leaves) ranging in age from early initiated pri- mordia to mature leaves were measured for 19 characters developed by the authors (Table 1). Leaves less than 30 mm in length were measured under a Zeiss dissecting microscope, using a graticule for greater accuracy.

Each character was classified in one of five categories (Table 1). The first category included characters dealing with angles measured between the major veins of the leaf. These veins radiate out from one common point (Fig. 1, point 2). This point served as reference for most of the other characters. The second category also included char- acters dealing with leaf venation, such as ratios of the distance to the first lateral vein of the main vein of a leaf lobe from the common junction point 2 (Fig. 1) against the length of that leaf lobe. The third category involved leaf sinuses. Ratios of the length of a leaf lobe measured from the junction of the major veins (Fig. 1, point 2) against the distance to the lowest point of a sinus from that same point of reference were determined. For the fourth category, ratios of the length of a leaf lobe were measured against the length of another leaf lobe using a common point of reference (Fig. I, point 2). The final category included ratios of the length of the petiole against the length of four major lobes of the leaf. Leaf blade length, which was con- sistently measured as the distance between points 2 and 5 (Fig. l ) , was log transformed and served as the indirect measure of develop- mental time. All characters were tested to determine if there was sufficient evidence to indicate whether the normality or homogeneity of variance assumptions had been violated before performing the sta- tistical analyses on the data set.

The mainframe S A S I S T A P statistical package was used to per- form a nested analysis of variance (ANOVA) for each character of inter-

Sinuses 694 Ratio lobe llsinus 1 2-312-8 695 Ratio lobe llsinus 2 2-312-9 696 Ratio lobe 21sinus 1 2 4 / 2 4

Lobes 688 690 69 1 693

Petiole 683 684 686 687

Ratio lobe Illobe 2 Ratio lobe lllobe 4 Ratio lobe lllobe 5 Ratio lobe 4llobe 5

Ratio petiolellobe 1 Ratio petiolellobe 2 Ratio petiolellobe 4 Ratio petiolellobe 5

est (SAS Institute Inc. 1985~). The data were analyzed for the best fitting model according to the following general expression:

where c-r is the intercept, P l x i is the linear component, PA2 is the quadratic component, and ei is the error term. It was determined from preliminary analyses of a subset of the data, by plotting the meas- urements of an individual character against leaf blade length, that the best fitting model would not go beyond quadratic. Because we are dealing with correlated data (i.e., measurements taken from sequen- tial leaves on a twig), each component of the model was tested indi- vidually using the analysis of variance. In the event that the quadratic component tested nonsignificant, the next lower order model, linear in this situation, was adopted. The data were also analyzed for dif- ferences between taxa for each of the components of the best fitting model,using contrasts, a multiple comparisons procedure. All graphs were produced using mainframe SAS/GRAPHa (SAS Institute Inc. 19856).

Results

Results from the ANOVA for each character indicated no sig- nificant differences between the four collection dates. Before attempting to describe the statistical results obtained for char- acters in each of the five categories outlined in Table 1, namely venation, angles, lobes, petioles, and sinuses, the analysis of a specific character will be described in detail as a guide for the interpretation of the other results displayed in Table 2.

Character number 633 refers to a measurement in the ven- ation category; Table 1 offers a description of this character. The measurement is a ratio of the distance to the first lateral vein of the main vein of leaf lobe 1 measured from a reference point (Fig. 1, points 2-15), against the length of that lobe (Fig. 1, points 2-6). Therefore, character number 663 is the ratio of the distance between the following points: 2-1512-6 (Fig. 1). Reference to Table 2 shows that for character 663 the quadratic component of the model, as well as the linear component and the intercept were not significant for differ- ences between varieties. The same letter was therefore used to designate this for each taxon. The overall measure of the quad-

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VOL. 69. 1991

between leaf blade length and the characters dealing with the lower leaf lobes, i.e., characters number 660 and 664 for lobes 1 and 5 , respectively (Fig. 1 , points 2-3 and 2-7).

1 FIG. 1. Diagram representing a typical Vitis leaf. The location of

specific points of reference used to measure the different parameters described in Table 1 are labelled.

ratic component, however, indicates that there is a change in the ratio over leaf blade length (Table 2). Figure 2 is a rep- resentation of this character versus our indirect measure of developmental time (leaf blade length). Figures 2-6 show the best fitting regression lines for the response of representative characters versus leaf blade length for each of the categories described below. Data points are omitted to reveal the pattern more clearly.

Angles Characters 676 (angle to the first lobe) and 677 (angle

between lobes 1 and 2), are nonsignificant for the presence of a quadratic component in the model describing the change in the angle between major veins of a leaf with leaf blade length (Table 2). However, a linear component was present in these characters. Figure 3 shows a graph of regression lines for char- acter 677 (Fig. 1, angle formed by points 3-2-4) versus leaf blade length. In this situation, angles tended toward lower val- ues at increasing leaf blade lengths. For character 676, how- ever, angles tended toward higher values at increasing leaf blade lengths. On the other hand, character 680 (angle to fifth lobe) tested significant for the presence of a quadratic com- ponent in the model and character 679 (angle between lobes 3 and 4) did not show any relationship over leaf blade length. In addition, the analysis did not reveal any differences between cultivars for any of the above characters.

Venation The trend described above for character 663 in the intro-

ductory section of the results also applies for the opposite upper leaf lobe (character 661, venation of lobe 2). Although these characters did not provide any distinction between taxa when plotted versus leaf blade length, the general trend was a change in these ratios over leaf blade length. No relationship was seen

Sinuses Measurements involving ratios between lobe length and

sinus length tested significant for a quadratic component for characters 695 and 696 (Tables 1, 2), indicating a change in the ratio versus leaf blade length. Character 694 did not show any relationship to leaf blade length. In addition to the above results, it was possible to distinguish between taxa for char- acters 695 and 696. For character 695 (Table l ) , all three taxa were distinguishable. Figure 4 shows a graph of regression lines for the three taxa for character 695, the ratio of the lengths of leaf lobe 1 and sinus 2 (Fig. 1, points 2-312-9) over leaf blade length. For character 696, a measure of the ratio of the length of lobe 2 against the distance to sinus 1 (Fig. 1, points 2-4/24), V. riparia was distinguishable from the other two taxa.

Lobes All characters in this category, with the exception of char-

acter 691, tested significant for the presence of a quadratic component for the models involving ratios between leaf lobe lengths and their response over leaf blade length (Fig. 1, points 2-5). This signifies a change in the ratios over leaf blade length. Character 691, however, which is a ratio of the length of lobe 1 (Fig. 1, points 2-3) to the length of lobe 5 (Fig. 1, points 2-7), was the only one that did not show any relation- ship with changing leaf blade length. It was also possible to distinguish V . riparia from the other two cultivars in at least one of the components of the model describing the relationship between the ratios and leaf blade length for characters 688, 690, and 693 (Tables 1, 2). Figure 5 shows a graph of regres- sion lines for the three taxa for character 688 (Fig. 1, points 2-312-4) over leaf blade length and is representative of the trend exhibited by the other characters in this category.

Petiole Ratios of the length of the petiole to the length of a leaf

lobe measured against overall leaf blade length (Fig. 1, points 2-5) showed a consistent pattern for all the characters in this category (Tables 1, 2; 683, 684, 686, 687). The quadratic co'mponent was significant for all the characters in this cate- gory. Indications of change in these ratios versus leaf blade length were strongest in this category. In addition, it was pos- sible to distinguish 'Concord' from V. riparia and 'Vivant' in all of the components of the model. Figure 6 shows a graph of regression lines for the three taxa for character 686 (Fig. 1, points 1-212-6) over leaf blade length.

Discussion

The results of this study confirm, to some extent, our visual observations of early stages of leaf development in the same taxa (C. R. Lacroix and U. Posluszny? unpublished). Early events of development or early stages of initiation are impor- tant in determining the "basic" shape of the leaves of Vitis riparia and cultivars Vivant and Concord. The characters in the categories of angles and venation did not show as much change as those in the categories of petiole, sinuses, and lobes when regressed against leaf blade length. This means that once one of these characters can be measured on a young leaf, it

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LACROIX AND POSLUSZNY 403

TABLE 2. Results of statistical analysis of characters

Between taxa

P F V. riparia 'Vivant' Overall

'Concord' P Character No.

676

677

679

680

Model component

Angles

0.55 a 0.91 a

- 0.94 a 2.38 a

A

-

-

1.13 a 2.05 a 1.06 a

Venation -

-

-

1.17 a 0.45 a 1.03 a 0.46 a 0.56 a 0.11 a

-

- Sinuses

- -

A

7.31 a 8.51 a 2.65 a 9.04 a 2.94 a

39.68 a Lobes

3.91 a 1.04 a

22.74 a 1.42 a 0.01 a

24.45 a - -

- 16.71 a 7.84 a

26.00 a Petiole

8.75 a 8.93 a

22.98 a 6.3 a 5.46 a

34.44 a 7.17 a 5.54 a

37.54 a 5.65 a 4.43 a

27.88 a

Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear Intercept

Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear Intercept

Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear Intercept

Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear In tercep t

Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear Intercept Quadratic Linear Interceut

NOTE: Taxa with the sarnc Iettcrs within a line are not s~gnificantly different from each other. *Significan~ at the 0.05 Icvcl. df = 30; unmarked P values are nonsignificant; -, not applicable.

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CAN. J . BOT. VOL. 69, 1991

VIVANT -- CONCORD

LEAF BLADE LENGTH mm LEAF BLADE LENGTH mm

LEAF BLADE LENGTH mm LEAF BLADE LENGTH mm

LEAF BLADE LENGTH mm

FIGS. 2-6. Best fitting regression lines for representative characters (Table 1) plotted against leaf blade length for each of three taxa: V. riparia, and cultivars Vivant and Concord. Fig. 2. Character number 663 (venation). Fig. 3. Character No. 677 (angles). Fig. 4. Character No. 695 (sinuses). Fig. 5. Character No. 688 (lobes). Fig. 6. Character No. 686 (petiole).

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LACROK AND POSLUSZNY 405

does not vary extensively when it is measured on leaves of similar or geater size. Characters involving leaf sinuses and petioles, however, showed strong indications of change over leaf blade length. In addition, distinction between individual taxa using the above approach proved useful only for char- acters dealing with the categories of petiole, lobes, and sinuses (Table 1). This study is the first to our knowledge to look at the expression of ampelographic leaf characters over a full range of leaf sizes from young primordia to mature leaves as opposed to mature structures only. Biological interpretation of the statistical results is discussed briefly below for each of the categories outlined in Table 1.

Angles Plots of the angles between major leaf veins versus leaf blade

length did not show a clear pattern and did not provide any distinction between the three taxa. The overall variability of angles between major leaf veins was apparent in the data. According to Dorsey (1912), variation in measured angles within taxa is not uncommon

Venation The two characters dealing with the venation of upper leaf

lobes (Table 1, characters 661 and 663) showed the same type of response when their measurements were compared over leaf blade length (Fig. 2, Table 2). The relative distances between the points of interest on the upper leaf lobes expressed in the ratio varied little over the range in leaf blade length in com- parison to more variable characters in the categories of lobes, sinuses, and petioles. Although a trend in the ratio over leaf blade length was observed, distinction between taxa was not possible in any of the above venation characters. No relation- ship was found between characters dealing with the lower leaf lobes (Table 1, characters 660 and 664) and leaf blade length.

Sinuses The ratio of the length of a leaf lobe over that of a leaf sinus

(characters 695 and 696), when regressed against leaf blade length, showed stronger indications of change than any of the above categories. The differential rate of growth of these two parameters (leaf lobes and sinuses) during development is most likely responsible for this pattern. Sinus depth also varies to different extents within taxa. In addition, the dinstinction between cultivars was not clear for all characters in this cat- egory (Table 2). For character 695, all three taxa were distin- guishable, whereas for character 696 V . riparia could be singled out.

Lobes Characters involving ratios of the length of major leaf lobes

(Table 1; 688,690,693) showed the same type of pattern when they were plotted against leaf blade length, with the exception of character 691, which did not show any relationship (Table 2). A quadratic component characterizes the response of these ratios over leaf blade length, indicating changes in the relative proportions of the parameters of the ratios on leaves at different stages of development.

Petiole The greatest amount of change in the ratio of the length of

the petiole and that of one of the four major leaf lobes was observed in the three taxa for characters in this category when they were analyzed against leaf blade length. This can be explained by the fact that both the petiole and the leaf lobes

grow at different relative rates during development. This is, therefore, reflected in the changing values of the ratios of the above characters over leaf blade length. In addition, 'Concord' was clearly distinguishable from V . riparia and 'Vivant' in its response (Table 2, Fig. 6) in all the characters in this category.

The overall results of this study show two trends for char- acters that were measured on leaves at different stages of development. The first trend involves characters in the cate- gories of angles and venation. The change in these ratios or angles, analyzed against leaf blade length, was minimal. Therefore, the relative relationship between the parameters that were measured in the ratios did not vary as extensively at dif- ferent stages of leaf development as those measured for char- acters in the category of petiole and sinuses. It appears that leaf features such as the basic pattern of major veins are estab- lished early in development and change relatively little after their initiation in comparison to more variable characters such as those dealing with the leaf petiole or leaf sinuses.

Characters in the categories of lobes, sinuses, and petiole, on the other hand, showed stronger indications of change in their ratios over leaf blade length. Differences in the relative rate of growth of the parameters of these ratios can account for differences in the measurement of ratios on leaves at dif- ferent stages of development. The establishment of these sin- uses is believed to occur gradually, by differential growth of adjacent meristematic areas of the leaf blade (Cusset 1986). The leaf petiole, on the other hand, seems to grow maximally at different times compared with the rest of the leaf, almost behaving as a separate organ (Hammond 1941).

Several quantitative studies dealing with aspects of leaf development provide evidence for the early initiation of "basic" leaf shape (Cogliatti and Guitman 1984; Delisle 1938; Njoku 1956; Wolf et al. 1986). An allometric study by Guerrant (1982), dealing with the ontogeny of flowers of Del- phinium nudicaule, illustrates how heterochrony (differences in the timing of developmental processes) results in morphol- ogical differences among related taxa with the use of variables such as size, age, and shape. This approach could lend itself to aspects of leaf development explored in this study, espe- cially as it applies to characters where the distinction between taxa is possible. For example, if we consider the petiole cat- egory, 'Concord' was distinguishable from the other two taxa on the basis of characters dealing with the ratio of the length of the petiole over the length of one of the major leaf lobes. If we consider the distinction between taxa as being the result of differences in the timing of petiole and leaf lobe develop- ment, relationships between taxa with reference to specific characters could be clarified. However, this type of approach would need to be applied to a broader range of taxa to be tested adequately.

Acknowledgements

This investigation was supported by Natural Sciences and Engineering Research Council of Canada operating grant A6260 and strategic grant G1993 to Usher Posluszny. The authors are grateful to Dan Ryan for statistical advice, and to Christopher Briand and Dr. Terrence Walters for their com- ments and suggestions on the manuscript.

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