Annals of Botany 89: 115-124, 2002
© 2002 Annals of Botany Company
Periods of Organogenesis in Shoots of Nothofagus dombeyi (Mirb.) Oersted (Nothofagaceae)
1Department of Botany, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Quintral 1250, 8400 Bariloche, Argentina, 2Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina and 3Unité Mixte CIRAD–CNRS–EPHE–INRA–Université Montpellier II AMAP, TA40/PS2, Boulevard de la Lironde, 34398 Montpellier Cedex 5, France
* For correspondence. Department of Botany, Universidad Nacional del Comahue, Quintral 1250, 8400 Bariloche, Argentina. E-mail: jpuntier{at}crub.uncoma.edu.ar
Received: 28 June 2001; Returned for revision: 16 August 2001; Accepted: 1 October 2001.
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ABSTRACT |
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The organogenetic cycle of main-branch shoots of Nothofagus dombeyi (Nothofagaceae) was studied. Twelve samples of 52–59 parent shoots were collected from a roadside population between September 1999 and October 2000. Variations over time in the number of nodes of terminal and axillary buds, and the length, diameter and number of leaves of shoots derived from these buds (sibling shoots) were analysed. The number of nodes of buds developed by parent shoots was compared with the number of nodes of buds developed, 1 year later, by sibling shoots. The length, diameter and number of leaves of sibling shoots increased from October 1999 to February 2000 in those shoots with a terminal bud. However, extension of most sibling shoots, including the first five most distal leaf primordia, ceased before February due to abscission of the shoot apex. Axillary buds located most distally on a shoot had more nodes than both terminal buds and more proximal axillary buds. The longest shoots included a preformed part and a neoformed part. The organogenetic event which initiated the neoformed organs continued until early autumn, giving rise to the following year’s preformation. The absence of cataphylls in terminal buds could indicate a low intensity of shoot rest. The naked terminal bud of Nothofagus spp. could be interpreted as a structure less specialized than the scaled bud found in genera of Fagaceae and Betulaceae.
Key words: Bud, cataphyll, leaf primordia, apex abortion, organogenesis, preformation, neoformation, Nothofagus dombeyi, shoot growth.
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INTRODUCTION |
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Rhythmic growth is usual amongst woody species from temperate and cold regions and contrasts with the continuous growth pattern found in some tropical trees (Hallé et al., 1978). In species with rhythmic growth, an axis portion extended in any one year (termed the annual shoot, or simply the shoot) may be distinguished by observation of between-shoot limits along an axis (Hallé et al., 1978; Caraglio and Barthélémy, 1997). The development, between two consecutive periods of shoot extension, of a bud with external cataphylls (non-photosynthetic leaves) and internal green-leaf primordia is typical of these species (e.g. Heuret et al., 2000). Those organs which were part of a bud before shoot extension are known as preformed organs (Caraglio and Barthélémy, 1997). In some woody species it is known that, in addition to preformed leaves, at least some shoots may have a set of neoformed leaves, which extend as they differentiate from the apical meristem (e.g. Macdonald et al., 1983; Davidson and Remphrey, 1994). The presence in a shoot of preformed and neoformed leaves indicates that the shoot concerned results from at least two separate organogenetic events. The times of the year when these events occur are important in understanding the role of environmental factors in leaf and shoot growth (Roloff, 1987). The extent of preformation and neoformation may depend on the position of a shoot in the crown of a tree (Davidson and Remphrey, 1994; Souza et al., 2000). Despite these recent advances, very few studies have considered the periods of the year in which organogenesis takes place (but see Hallé et al., 1978; Roloff, 1987; Gruber, 1995). To perform this type of study, an adequate knowledge of a species’ morphology and architecture is necessary so as to overcome the restrictions imposed by both the destructive nature of bud-structure inspection and intraspecific variations in the occurrence of neoformation. Categorization of individuals, axes and shoots may allow repeated sampling of homogeneous populations of shoots which would give an insight into the periodicity of organogenesis.
Nothofagus is considered one of the key genera in the understanding of the evolution of the southern hemisphere biota (Hill, 1992; Hill and Dettmann, 1996; Veblen et al., 1996). Traditionally classified as a member of the Fagaceae, this genus has recently been included in the monogeneric family Nothofagaceae on morphological, developmental and biogeographical grounds (Jones, 1986; Hill and Jordan, 1993; Takhtajan, 1997). Until recently, however, little information concerning the vegetative morphology and development of Nothofagus species was available (Hill, 1992; Manos, 1997; Rozefelds and Drinnan, 1998). In the last decade several studies on South American species of this genus have contributed to fill this gap (Thiébaut et al., 1997; Puntieri et al., 1998, 1999; Raffaele et al., 1998; Barthélémy et al., 1999; Souza et al., 2000; Stecconi et al., 2000). Nothofagus dombeyi (Mirb.) Oersted is one of the most abundant species and has the largest individuals within this genus. Recent studies on this species have allowed categorization of axes (Puntieri et al., 1998; Barthélémy et al., 1999). In young N. dombeyi trees, each shoot of the most vigorous categories of axes, trunk and main branches, usually consists of preformed and neoformed leaves (Puntieri et al., 2000). However, the time of year when leaf differentiation occurs (i.e. the organogenetic cycle) has not been reported for this or any other species of Nothofagus. In the present study, the sampling of shoots from a homogeneous population of N. dombeyi trees was extended over 1 year to gain insight into the period or periods of the year when preformed and neoformed leaves of vigorous shoots are initiated from the meristems. The composition of buds initiated in two successive years was also compared.
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MATERIALS AND METHODS |
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Shoot sampling and measurements
A population of young N. dombeyi trees was chosen for the present study. The population is located between 10 and 30 km east of Villa La Angostura, Argentina, close to national route 231 which runs in a south-east to north-west direction (40°47'S, 71°40'W, Parque Nacional Nahuel Huapi, Argentina). Annual precipitation in this area averages 800 mm and mean annual temperature is 8·1 °C (Conti, 1998). The soil in the area consists of successive layers of volcanic ash, is rich in superficial organic matter and has a slightly acidic pH (Scoppa, 1998). The selected trees constitute the regeneration cohort which established naturally after road construction, between 3 and 6 m from the north-eastern margin of the road. These individuals have the architecture typical of vigorous young trees of this species, with a single or forked vertical axis (trunk) and one to three vigorous horizontal main branches developed in axillary positions from the distal end of each trunk shoot (Puntieri et al., 1998, 2000; Barthélémy et al., 1999). From a random sample of 57 trees, it was estimated that their age was about 14·4 years (s.d. = 2·6 years), their height about 4·8 m (s.d. = 1·5 m) and their basal diameter about 104·7 mm (s.d. = 44·4 mm). The number of such trees along the 20 km of roadside chosen exceeds 5000, most of which are developing close to the canopy of adult trees. For each sample, a group of trees was randomly selected.
This study was centred on the distal shoots of main branches of the selected trees because of (a) the potentiality of these shoots to develop neoformed organs (Puntieri et al., 2000), and (b) their large number and low variability in terms of branching capability compared with trunk shoots (see Puntieri et al., 1998). Twelve samples of 52–59 main-branch shoots each were collected monthly between 10 Sep. 1999 and 10 Jun. 2000, and one sample was collected on 10 Aug. 2000 and another on 10 Oct. 2000. Each sample unit consisted of a shoot extended at the distal end of a main branch of a tree during the 1998–1999 growth period and all structures which derived either axillary or terminally from that shoot (Fig. 1). Hereafter, these shoots will be referred to as parent shoots. To keep within-sample variability low, three restrictions were imposed on the otherwise random selection of parent shoots: (1) all parent shoots had more than ten leaves and did not have branches developed during parent shoot extension; (2) the main branch which included the parent shoot had developed for at least 2 years since its initiation from the tree trunk; and (3) only one parent shoot was sampled from each main branch. Each parent shoot sampled was bearing, depending on the sample concerned, buds or shoots (hereafter referred to as sibling shoots), which were either axillary or, less frequently, terminal. Terminal bud abortion after shoot extension is a common event in this and other species of Nothofagus (Fig. 1).
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The length (to the nearest 1 mm), basal diameter (to the nearest 0·1 mm) and number of nodes of each parent shoot were recorded at each sampling time. The four most distal healthy-looking (not evidently affected by exogenous factors such as herbivory) buds or sibling shoots of each parent shoot were numbered from 1 to 4 according to their relative position counted from the parent shoot’s distal end (Fig. 1A–C). Throughout the following text, the expressions ‘parent-shoot bud’ and ‘sibling shoot’ will be applied in reference to these distal organs. Previous observations indicate that in N. dombeyi, the shoots most likely to develop preformed and neoformed leaves are those initiated close to the distal end of a parent shoot.
The number of cataphylls and the number of green-leaf primordia of each parent-shoot bud were recorded after manual dissection under a stereo-microscope (60x). The number of nodes of a bud was computed by adding together the numbers of cataphylls and green-leaf primordia. For each sibling shoot, the length, basal diameter, number of cataphylls, number of green leaves and number of terminal leaf primordia (whenever the apex was functional; Fig. 2A) were recorded. The number of nodes of a sibling shoot was obtained by summing its numbers of cataphylls and green leaves.
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In this species, a dead apex may be identified either by the absence of terminal leaf primordia (Fig. 2B) or by the presence of abortive leaf primordia, which differ from functional leaf primordia both in size and shape (Fig. 2C). Previous observations on this species led us to the conclusion that both the presence of abortive terminal leaf primordia and the death of the shoot apex imply the end of the activity of a shoot’s apex; the expression ‘dead apex’ will be used in the following text to refer to both conditions. In all sibling shoots collected between February and October 2000 with a dead apex, the most distal axillary bud was dissected and its cataphylls and green-leaf primordia counted.
Mean values were obtained for the length, diameter and number of leaves of parent shoots of each sample. Numbers of nodes of parent-shoot buds were averaged for each relative position (1–4) of each sample. Sibling shoots with a functional or dead apex were considered separately in all analyses. For the latter group and for each position, within-sample averages were computed for the length, diameter, number of cataphylls, number of green leaves, number of distal leaf primordia and number of cataphylls and green-leaf primordia of the distal axillary bud of sibling shoots. Since sibling shoots with a functional apex were few and corresponded mostly to relative position 1, mean values of length, diameter, number of cataphylls, number of green leaves and number of nodes of the terminal bud of these shoots were computed only for relative position 1. The proportion of sibling shoots with a dead apex was calculated for each relative position on the parent shoot and for each sample.
Statistical analyses
To ensure independence of data within samples, only data of one sibling shoot were extracted from each parent shoot for each statistical comparison. The small number of sibling shoots with a functional apex for most samples led us to select, in the first place, a group of parent shoots in which the position-1 sibling shoot had a functional apex. The remaining parent shoots were randomly assigned to each of the other four conditions (sibling shoots with a dead apex in positions 1–4). After this classification of parent shoots, each of the five groups of sibling shoots (sibling shoots with a functional apex and sibling shoots with a dead apex in relative positions 1, 2, 3 and 4) consisted of between seven and 12 sample units for each sample.
Sibling-shoot length, diameter and number of nodes were compared between samples (ten samples) and between shoot groups (five types) by means of two-way ANOVA (GLM procedure for unbalanced designs; Zar, 1984). The interaction between sample and shoot group was also evaluated. Two-way ANOVA was also used to compare the number of terminal leaf primordia and axillary leaf primordia between samples (seven samples) and between the five shoot groups mentioned above.
The number of nodes of buds formed distally on parent shoots (data from September and October 1999 samples, pooled) and that of buds formed distally on sibling shoots in relative positions 1–4 on the parent shoots (data from August and October 2000 samples, pooled) were compared. Two-way ANOVA (GLM) was applied, with time of bud initiation (1998–1999 or 1999–2000 growing seasons) and bud position (terminal or axillary in relative positions 1–4) as factors.
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RESULTS |
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Size of parent shoots and sibling shoots
The length of parent shoots was similar for all samples (Fig. 3A). The basal diameter of parent shoots increased particularly from November 1999 onwards (Fig. 3B). The number of both green leaves and cataphylls of parent shoots was similar for all samples (Fig. 4A, B).
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The length and number of green leaves of all sibling shoots increased notably between October and December 1999; further, less notable increases in length and number of green leaves were found for sibling shoots with a functional apex (Figs 3A and 4A). The diameter of sibling shoots in all positions increased gradually between October 1999 and May 2000 (Fig. 3B). The number of cataphylls was similar for all samples and for sibling shoots in all positions (Fig. 4B). The length, diameter and number of nodes of sibling shoots depended both on their relative position on the parent shoot and on the sample considered (Table 1). Differences among sibling shoots in different positions were greater in terms of length and number of nodes than in terms of diameter. The interaction between sibling-shoot position and sampling time was significant for the length (P < 0·001) and number of nodes (P < 0·05) but not for diameter (Table 1). The length, number of green leaves and diameter of sibling shoots in position 1 with a functional apex tended to be more similar to those of sibling shoots with a dead apex in position 1 than to those of more proximal sibling shoots with a dead apex (Figs 3 and 4).
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Most buds of parent shoots sampled in September and October 1999 had a well-developed apex (Fig. 5). By October 1999, all of these buds had started to swell and break. The number of sibling shoots with a dead apex increased sharply between November 1999 and January 2000, more notably so for proximal sibling shoots than for distal sibling shoots (Fig. 5). By April 2000, the proportion of sibling shoots with a dead apex had stabilized for all positions on the parent shoots.
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Number of nodes of terminal and axillary buds
Terminal and axillary buds of parent shoots sampled in September and October 1999 consisted, on average, of two cataphylls (usually one or none in terminal buds) and 12 green-leaf primordia (Fig. 6). Between October and November 2000, as the number of unfolded leaves of sibling shoots increased, the number of green-leaf primordia at their distal end decreased to about four (Fig. 6A); no cataphyll primordia were found (Fig. 6B). In those sibling shoots with a functional apex, the number of green-leaf primordia at their distal end increased from November 1999 to April 2000, and did not change significantly thereafter (Fig. 6A). Sibling shoots with a dead apex had one to three (rarely two or three more) abortive green-leaf primordia at their distal end after shoot extension (Fig. 6A). The embryonic lamina of each of these primordia was pale brown and flexible (like those of leaf primordia of terminal and axillary buds) for the first sampling dates, and dark brown and brittle for the last sampling dates, prior to their abscission.
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The number of green-leaf primordia of axillary buds developed distally on sibling shoots with a dead apex increased between February and April 2000 and remained constant thereafter (Fig. 6A). Whereas the number of green-leaf primordia of the most distal axillary bud decreased from distal to proximal sibling shoots, the number of cataphylls of this bud was always about two for all positions and samples (Fig. 6B).
The mean number of nodes per bud was maximal for axillary buds in relative position 1 on the parent shoot (September and October 1999 samples) and the most distal axillary bud from sibling shoots in position 1 (August and October 2000 samples); axillary buds in positions 2–4 and terminal buds had fewer nodes, irrespective of the year of bud development (F = 13·4, P < 0·001; Table 2). Terminal buds had a mean number of nodes similar to that of axillary buds in positions 3 and 4 (Table 2). For each relative position on the parent shoots (terminal and axillary 1–4), the mean number of nodes of parent-shoot buds was similar to that of sibling-shoot buds (F = 0·51, P > 0·1; Table 2). The interaction between bud position and time of bud development did not have a significant effect on the number of nodes per bud (F = 2·10, P > 0·05).
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Comparison of the number of nodes between buds and sibling shoots
The frequency distribution of the number of nodes of buds corresponding to September and October 1999 samples (all positions included) was similar to that of the number of unfolded leaves of sibling shoots sampled between November 1999 and January 2000, irrespective of the condition of the apex of the sibling shoots (Fig. 7A, B). Sibling shoots with a functional apex sampled between February and October 2000 had, on average, more unfolded leaves than both sibling shoots with a functional apex sampled up to January 2000 and sibling shoots with a dead apex sampled from February 2000 onwards (Fig. 7B, C).
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DISCUSSION |
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Leaf differentiation and apex abortion in N. dombeyi shoots
The present study indicates that each main-branch shoot of young N. dombeyi trees results from one or two events of leaf differentiation. Most of these shoots consist exclusively of stem and leaves which were differentiated in the previous growing season, mostly in late summer, and which remained enclosed in a bud throughout autumn and winter. The proximal part of all other shoots also corresponds to the enlargement of preformed organs. The late-summer period of leaf differentiation prior to the development of winter buds seems to be, according to the limited information available, the norm for vigorous shoots of trees from temperate and cold regions (e.g. Roloff, 1987; Gruber, 1995; Nicolini, 2000; Nitta and Ohsawa, 2001; Sabatier and Barthélémy, 2001). In vigorous shoots of N. dombeyi, apex persistence in late spring and summer, after the extension of preformed organs, is closely linked with the occurrence of a second event of leaf-primordia initiation and the simultaneous unfolding of some of these primordia. The present results comply with other studies on Nothofagus in which the development of neoformed organs was found only in the most vigorous shoots; in these studies, as in the present one, the number of neoformed organs (for shoots of a similar size) was less than 30 % the number of preformed organs (Puntieri et al., 2000; Souza et al., 2000). Comparisons with other species are not straightforward since the extent of both preformation and neoformation has been shown to vary markedly according to external conditions, genotype and gradients within the plant (Davidson and Remphrey, 1994).
Differentiation of neoformed leaves in N. dombeyi starts without the apex of the growing shoots ever being completely depleted of primordia. Using the scale of sampling chosen for the present study (monthly), no rest period was detected after extension of preformed organs. However, results of a previous study on the same species, in which weekly non-destructive measures of shoots were made, support the idea of a period of a low rate of extension intervening between preformation and neoformation extension (Puntieri et al., 1998). Annual shoots with two flushes of growth separated by a bud, i.e. recurrently flushing shoots (Caraglio and Barthélémy, 1997), were not found in the present study. Recurrently flushing shoots have been reported for Nothofagus species from New Zealand (Ogden et al., 1996), Australia (Read and Brown, 1996) and South America (including N. dombeyi; Thiébaut et al., 1997) as well as for species of Fagus and Quercus (Fagaceae; Collin et al., 1996; Thiébaut et al., 1997; Heuret et al., 2000). For N. dombeyi, recurrently flushing shoots have been observed by the present authors only in cases of traumatic apex death, so that the second flush derived from an axillary rather than a terminal bud. Comparative studies on several species of Nothofagus may help to determine whether or not the two flushes of growth cited so far correspond with the extensions of preformed and neoformed organs.
For some weeks between late spring and early summer, organogenesis and extension are simultaneous in N. dombeyi shoots with a functional apex. By mid-summer (February), leaf and shoot extension stops but organogenesis continues, thus leading to the accumulation of leaf primordia at the terminal bud. These primordia correspond with the preformed organs of the shoot which should extend in the following spring. Therefore, the preformed organs of a shoot derived from a terminal bud differentiate in the same organogenetic event as the neoformed organs of the previous year’s shoot. The organogenetic cycle found here for N. dombeyi resembles that found for other tree species in which the constituent leaves of some shoots result from two organogenetic events (Critchfield, 1960; Hallé and Martin, 1968; Hallé et al., 1978).
The high frequency of apex death after shoot extension found in the present study for N. dombeyi is in accordance with previous results (Puntieri et al., 1998). Shoot apex death in this species is usually accompanied by abscission of the one to three (sometimes more) most distal internodes and corresponding leaf primordia of these shoots, as found for other woody species (Garrison and Wetmore, 1961; Macdonald et al., 1983). This pattern of apex abortion would explain results of previous studies on this and other Nothofagus species, in which some shoots were found to have fewer nodes after their extension period than the buds from which these shoots derived (Puntieri et al., 2000; Souza et al., 2000). However, in the present study, buds and sibling shoots with an aborted apex had, despite the abortion of distal primordia, a similar number of nodes. This disagreement with previous results may derive from the involvement in apex death of a major (in terms of the number of shoots affected) factor(s) acting before the onset of neoformation development, and a minor factor(s) acting after the onset of neoformation (compare Figs 4 and 5). This implies that some shoots with neoformed leaves could have been included among those with a dead apex.
Terminal and axillary buds of N. dombeyi
Terminal and axillary buds of N. dombeyi differ in their composition. The one or two most proximal leaf primordia of a terminal bud in N. dombeyi usually have a well-developed primordium of a lamina, which is frequently only partly covered by its stipules and appears to be partly unfolded by the time of bud hardening. These primordia do not complete their extension; they dry out and abscise after bud break. In axillary buds, on the other hand, the two or three most proximal leaf primordia do not have a trace of lamina primordium. Thus, although the proximal leaves of shoots derived from either terminal or axillary buds may be described as cataphylls (i.e. they do not have a green lamina) when observed after full extension, these two types of cataphylls differ in their early developmental stages and, perhaps, in their functionality.
Terminal buds of this species may be described as naked buds, like those of other Nothofagus spp. (Barthélémy et al., 1999). The naked terminal bud of Nothofagus could be described as less specialized than the scaly buds of northern hemisphere species of Fagaceae and Betulaceae (e.g. Roloff, 1987; Nitta and Ohsawa, 1998; Nicolini, 2000), which would lend support the theory that Nothofagus occupies a basal position in the evolution of the so-called ‘Fagalean’ complex (Fagaceae–Nothofagaceae–Betulaceae; Hill and Dettmann, 1996; Jordan and Hill, 1999). Cataphylls have developed from green leaves on many occasions throughout the evolution of plants. One of the reasons for the absence of specialized protective leaves in the terminal buds of at least some Nothofagus species could be the more maritime environmental conditions which prevailed in the southern hemisphere during Quaternary times, as compared to those in the northern hemisphere (Markgraf et al., 1996). The absence of specialized leaves in terminal buds of N. dombeyi might reflect a low intensity of shoot rest during winter (Hallé et al., 1978; Nitta and Ohsawa, 2001) and, perhaps, an evolutionary transition from continuous to rhythmic axis growth. This idea agrees with the continuous axis extension observed in seedlings of an Australian Nothofagus species (Read and Brown, 1996).
According to the results presented here, terminal buds of N. dombeyi have two to four fewer nodes than axillary buds in a similar position within the tree crown. This contrasts with results found for other tree species in which the number of primordia of axillary buds was either similar to (Sabatier and Barthélémy, 2001) or less than (Rivals, 1965; Thorp et al., 1994) that of terminal buds. Axillary buds in positions 2–4 on main-branch shoots of N. dombeyi are, in this respect, more similar to terminal buds than to axillary buds in position 1. This means that terminal-bud abortion results in an increase in the basipetally decreasing leaf preformation gradient (i.e. more apical control).
Shoot position, structure and function
The present study has evidenced the existence of structural gradients among shoots developed in different positions close to the distal end of parent shoots. Differences between shoots with respect to the development or not of neoformed organs may imply functional differences. The extension of preformed organs in N. dombeyi comes to an end in early summer. The development of neoformed organs would allow shoots to increase their length whenever beneficial environmental conditions occur during mid- and late summer. However, these shoots may suffer from cold spells during that period.
The development or not of neoformed organs is closely linked with the persistence of the apex. The ultimate causes of shoot apex abortion in woody plants are unknown, although several hypotheses have been proposed (Garrison and Wetmore, 1961, and references therein). The present study suggests that at least for main branches of N. dombeyi, the closer a shoot develops to its parent shoot’s distal end, the lower the probability of abortion of its apex. This gradient in the probability of apex abortion among shoots in different positions may arise from environmental gradients (e.g. quality/quantity of incoming radiation) or from endogenous gradients (perhaps in relation to shoot vigour; see Kurian and Reddy, 1999). Despite the existence of gradients in the extent of preformation and the occurrence of neoformation among sibling shoots derived from the same parent shoot, the diameter growth achieved by these sibling shoots after extension was similar. This determines differences between these shoots in the length/diameter relationship and, therefore, in their flexibility and load-bearing capacity (e.g. of snow; Givnish, 1995; Payette et al., 1996; Valinger and Fridman, 1997).
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ACKNOWLEDGEMENTS |
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The authors are grateful to M. Stecconi, A. Passo and L. D’Atri for their assistance in this work, J. Kervella for valuable comments, and the Delegación Regional Patagonia of the Administración de Parques Nacionales for granting permission to collect plant material for this study. This study is part of research projects B 096 (Universidad Nacional del Comahue) and PEI 0800/98 (CONICET).
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LITERATURE CITED |
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Barthélémy D, Puntieri J, Brion C, Raffaele E, Marino J, Martinez P. 1999. Morfología de las unidades estructurales y modo de desarrollo básico de especies patagónicas de Nothofagus Blume (Fagaceae). Boletín de la Sociedad Argentina de Botánica 34: 29–38.
Caraglio Y, Barthélémy D. 1997. Revue critique des termes relatifs a la croissance et a la ramification des tiges des végétaux vasculaires. In: Bouchon J, Reffye P de, Barthélémy D, eds. Modélisation et simulation de l’architecture des plantes. Paris: INRA Editions, Science Update, 11–87.
Collin P, Badot PM, Millet B. 1996. Croissance rythmique et développement du chêne rouge d’Amerique, Quercus rubra L. cultivé en conditions contrôlées. Annales des Sciences Forestières 53: 1059–1069.
Conti HA. 1998. Características climáticas de la Patagonia. In: Correa MN, ed. Flora Patagónica VIII (I). Buenos Aires: INTA, 31–47.
Critchfield WB. 1960. Leaf dimorphism in Populus trichocarpa. American Journal of Botany 47: 699–711.[CrossRef]
Davidson CG, Remphrey WR. 1994. Shoot neoformation in clones of Fraxinus pennsylvanica in relation to genotype, site and prunning treatments. Trees 8: 205–212
Garrison R, Wetmore RH. 1961. Studies in shoot-tip abortion: Syringa vulgaris. American Journal of Botany 48: 789–795.[CrossRef]
Givnish TJ. 1995. Plant stems: biomechanical adaptation of energy capture and influence on species distributions. In: Gartner B, ed. Plant stems: physiology and functional ecology. San Diego: Academic Press, 3–49.
Gruber F. 1995. Morphology of Silver fir (Abies alba Mill.). II. Root branching, architectural model and crown analyses. Flora 190: 135–153.
Hallé F, Martin R. 1968. Etude de la croissance rythmique chez Hevea brasiliensis Müll. Arg. (Euphorbiaceae – Crotonoïdées). Adansonia 8: 475–503.
Hallé F, Oldeman RAA, Tomlinson P. 1978. Tropical trees and forests. An architectural analysis. Berlin: Springer-Verlag.
Heuret P, Barthélémy D, Nicolini E, Atger C. 2000. Analyse des composantes de la croissance en hauteur et de la formation du tronc chez le chêne sessile, Quercus petraea (Matt.) Liebl. (Fagaceae) en sylviculture dynamique. Canadian Journal of Botany 78: 361–373.[CrossRef]
Hill RS. 1992. Nothofagus: evolution from a southern perspective. Trends in Ecology and Evolution 7: 190–194.[CrossRef]
Hill RS, Dettmann ME. 1996. Origin and diversification of the genus Nothofagus. In: Veblen TT, Hill RS, Read J, eds. The ecology and biogeography of Nothofagus forests. Yale: Yale University Press, 11–24.
Hill RS, Jordan GJ. 1993. The evolutionary history of Nothofagus (Nothofagaceae). Australian Journal of Systematic Botany 6: 111–126.[CrossRef]
Jones JH. 1986. Evolution of the Fagaceae: The implications of foliar features. Annals of the Missouri Botanical Gardens 73: 228–275[CrossRef]
Jordan G, Hill RS. 1999. The phylogenetic affinities of Nothofagus (Nothofagaceae) leaf fossils based on combined molecular and morphological data. International Journal of Plant Sciences 160: 1177–1188.[CrossRef][ISI][Medline]
Kurian R, Reddy Y. 1999. Pattern of shoot growth in Zizyphus mauritiana and Z. oenoplia. Annals of Botany 84: 289–295.
Macdonald AD, Mothersill DH, Caesar JC. 1983. Shoot development in Betula papyrifera. III. Long-shoot organogenesis. Canadian Journal of Botany 62: 437–445.
Manos PS. 1997. Systematics of Nothofagus (Nothofagaceae) based on rDNA spacer sequences (ITS): Taxonomic congruence with morphology and plastid sequences. American Journal of Botany 84: 1137–1155.[Abstract]
Markgraf V, Romero E, Villagrán C. 1996. History and paleoecology of South American Nothofagus forests. In: Veblen TT, Hill RS, Read J, eds. The ecology and biogeography of Nothofagus forests. Yale: Yale University Press, 354–386.
Nicolini E. 2000. Nouvelles observations sur la morphologie des unités de croissance du hêtre (Fagus sylvatica L.). Symétrie des pousses, reflet de la vigueur des arbres. Canadian Journal of Botany 78: 77–87.[CrossRef]
Nitta I, Ohsawa M. 1998. Bud structure and shoot architecture of canopy and understorey evergreen broad–leaved trees at their northern limit in East Asia. Annals of Botany 81: 115–129.
Nitta I, Ohsawa M. 2001. Geographical transition of sylleptic/proleptic branching in three Cinnamomum species with different bud types. Annals of Botany 87: 35–45.
Ogden J, Stewart GH, Allen RB. 1996. Ecology of New Zealand Nothofagus forests. In: Veblen TT, Hill RS, Read J, eds. The ecology and biogeography of Nothofagus forests. Yale: Yale University Press, 25–82.
Payette S, Delwaide A, Morneau C, Lavoie C. 1996. Pattern of tree stems decline along snow-drift gradient at treeline: a case study using stem analysis. Canadian Journal of Botany 74: 1671–1683.
Puntieri J, Barthélémy D, Martinez P, Raffaele E, Brion C. 1998. Annual-shoot growth and branching patterns in Nothofagus dombeyi (Fagaceae). Canadian Journal of Botany 76: 673–685.[CrossRef]
Puntieri J, Raffaele E, Martinez P, Barthélémy D, Brion C. 1999. Morphological and architectural features of young Nothofagus pumilio (Poepp. et Endl.) Krasser (Fagaceae). Botanical Journal of the Linnean Society 130: 395–410.[CrossRef]
Puntieri J, Souza MS, Barthélémy D, Brion C, Nuñez M, Mazzini C. 2000. Preformation, neoformation and shoot structure in Nothofagus dombeyi (Nothofagaceae). Canadian Journal of Botany 78: 1044–1054.[CrossRef]
Raffaele E, Puntieri J, Martinez P, Marino J, Brion C, Barthélémy D. 1998. Comparative morphology of annual shoots in seedlings of five Nothofagus species from Argentinian Patagonia. Comptes Rendus de l’Académie des Sciences de Paris, Sciences de la vie 321: 305–311.
Read J, Brown MJ. 1996. Ecology of Australian Nothofagus forests. In: Veblen TT, Hill RS, Read J, eds. The ecology and biogeography of Nothofagus forests. Yale: Yale University Press, 131–181.
Rivals P. 1965. Essai sur la croissance des arbres et sur leurs systèmes de floraison (Application aux espéces fruitières). Journal d’Agriculture Tropicale et de Botanique Appliquée 12: 655–686.
Roloff A. 1987. Morphologie der Kronenentwicklung von Fagus sylvatica L. (Rotbuche) unter besonderer Berücksichtigung neuartiger Veränderungen. I. Morphogenetischer Zyklus, Anomalien infolge Prolepsis und Blattfall. Flora 179: 355–378.
Rozefelds AC, Drinnan AN. 1998. Ontogeny and diversity in staminate flowers of Nothofagus (Nothofagaceae). International Journal of Plant Sciences 159: 906–922.[CrossRef]
Sabatier S, Barthélémy D. 2001. Bud content in relation to shoot morphology and position on vegetative shoots of Juglans regia L. (Juglandaceae). Annals of Botany 87: 117–123.
Scoppa CO. 1998. Los suelos. In: Correa MN, ed. Flora Patagónica VIII (I). Buenos Aires: INTA, 15–30.
Souza MS, Puntieri J, Barthélémy D, Brion C. 2000. Bud leaf primordia content and its relation to shoot size and structure in Nothofagus pumilio (Poepp. et Endl.) Krasser (Nothofagaceae). Annals of Botany 85: 547–555.
Stecconi M, Puntieri J, Barthélémy D. 2000. Annual shoot-growth in Nothofagus antarctica (G. Forster) Oersted (Fagaceae) from northern Patagonia. Trees 14: 289–296.
Takhtajan A. 1997. Diversity and classification of flowering plants. New York: Columbia University Press.
Thiébaut B, Serey I, Druelle J, Li J, Bodin A, Rechain J. 1997. Forme de la plantule et architecture de quelques hêtres, chiliens (Nothofagus) et chinois (Fagus). Canadian Journal of Botany 75: 640–655.
Thorp GT, Aspinall D, Sedgley M. 1994. Preformation of node number in vegetative and reproductive proleptic shoot modules of Persea (Lauraceae). Annals of Botany 73: 13–22.
Veblen TT, Donoso C, Kitzberger T, Rebertus A. 1996. Ecology of Southern Chilean and Argentinean Nothofagus forests. In: Veblen TT, Hill RS, Read J, eds. The ecology and biogeography of Nothofagus forests. Yale: Yale University Press, 293–353.
Valinger E, Fridman J. 1997. Modelling probability of snow and wind damage in Scots pine stands using tree characteristics. Forest Ecology and Management 97: 215–222.[CrossRef]
Zar JH. 1984. Biostatistical analysis. New Jersey: Prentice Hall.
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