| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Anatomy and Morphology |
INRA, UMR DAP, INRA-SUPAGRO-CIRAD-Université Montpellier II, équipe ‘Architecture et Fonctionnement des Espèces Fruitières', 2 place Pierre Viala, 34060, Montpellier, Cedex 1, France
Received for publication September 12, 2006. Accepted for publication June 4, 2007.
ABSTRACT
Branching is a key factor in the evolutionary diversification of plants and is a main criterion for plant architecture analysis. Among descriptive features, acrotony is defined as increased vigor of the vegetative proleptic branches (from dormant buds), from the proximal to the distal part of the parent growth unit. I hypothesized that acrotony could be extended to other, usually poorly described, architectural traits. The study was conducted on two architecturally contrasting apple (Malus xdomestica) cultivars, ‘Pitchounette' and ‘Chantecler.' The proportion and size of various offspring entities were assessed according to their position along the shoot for 2 years after parent shoot growth. Acrotony was characterized by two inverse phenomena: an acropetal decrease in the proportion of latent buds and of laterals that aborted, and an acropetal increase in the proportion of reproductive laterals among growing laterals. Distally located reproductive laterals had more spur leaves and flowers and higher fruit set and flowered earlier than reproductive laterals lower on the parent annual shoot. The results suggest that the length-based criterion used for acrotony should be integrated into a general conceptual framework in which the organogenetic potential of the axillary meristem increases from the proximal to the distal part of the annual shoot, leading to greater branching density, larger offspring, and a greater propensity for flower bud formation over consecutive years.
Key Words: acrotony • apple tree • growth habit • latent bud • lateral abortion • Malus xdomestica • organogenesis • Rosaceae
Investigations on plant form and the underlying morphological and developmental mechanisms dramatically increased in the past decades by taking advantage of new concepts in plant morphology, especially those of architectural analysis (Hallé et al., 1978
). The architecture of a plant—whether a tree, a shrub, or an annual, a land or an aquatic plant—depends on the spatial and temporal arrangements of its parts and is based on morphological traits at the scale of a single shoot (e.g., rhythmic vs. continuous growth) and branch complex (e.g., immediate or sylleptic vs. delayed or proleptic branching). The architectural analysis eventually leads to the definition of concepts at the whole-plant scale such as the architectural model (basic growth strategy of a plant) and reiteration (repetition of all or a part of the architectural model; see Barthélémy and Caraglio, 2007
for a recent review of architectural concepts).
A main feature at the branch scale is acrotony, usually defined as the increase in vigor (length, diameter, number of leaves) of the vegetative proleptic branches (from dormant buds) from the bottom to the top position of the parent growth unit (Champagnat, 1954
; Bell, 1991
; Vincent, 1995
; Cook et al., 1998
; Lauri and Lespinasse, 2001
; Brunel et al., 2002
). The expression "apical control" is also used with similar meaning (Brown et al., 1967
; Wilson, 2000
). Acrotony is often considered a main factor governing tree as opposed to shrub development, the latter being characterized by stronger growth of branches at the base of the plant, i.e., basitony, according to Champagnat (1954)
and Crabbé (1981)
. However, these differences in branching patterns related to growth habit may be questioned because in the first case acrotony refers to branching at the annual branch scale, whereas in the second case basitony refers to branching at the whole plant scale. Indeed, at the annual branch scale acrotony is observed on both trees and shrubs. Acrotony typically gives rise to a whorl of branches, defining the rhythmicity of branching, which is a major determinant of plant architecture (Hallé et al., 1978
). According to Champagnat and colleagues (Champagnat, 1966
; Champagnat et al., 1971
) and others (Bory and Clair-Maczulajtys, 1988
), the differential growth of laterals along the parent shoot may occur as early as bud burst, in which case distal buds are the only ones to develop, reflecting a gradient of precedence that would appear during dormancy or later. When later, all buds begin to develop, but only distal ones grow longer, reflecting correlative influences between them.
Powell (1995)
and Guédon et al. (2001)
extended the definition of acrotony to offspring entities including cones, flowers, and lateral branches. Indeed, reports on various species describe an acrotonic trend for features other than shoot length: number of fruit per spur (Walsh, 1979
), number of preformed appendages in the bud, and/or bud mass (Champagnat, 1965
; Walsh, 1979
; Puntieri et al., 2002
; Costes, 2003
). The relationships between acrotony and vegetative growth have been documented and include, e.g., the probability of a second growth flush within the same growing season on apricot (Costes et al., 2000
) and the rate and duration of shoot elongation on Picea (Powell, 1995
). The relationships may also involve sexuality, e.g., the patterns of distribution of reproductive structures depending on branch position along the parent shoot on Picea (Powell, 1995
). According to Guédès (1977)
on Aesculus, the acrotony concept can be extended to the within-bud pattern of development, with larger buds at the axil of the preformed leaves beneath the flower cluster. Acrotony then illustrates hierarchic relationships between adjacent buds along the same parent shoot at spatial and temporal levels, among preformed as well as among neoformed organs. It encompasses both organogenesis and actual growth.
The apple was chosen in this study because it offers a relevant biological model with an acrotonic behavior, i.e., an increase of the length of proleptic branches in distal positions (Cook et al., 1998
), that may be depressed by shoot reorientation away from the vertical (Wareing and Nasr, 1961
; Crabbé, 1969
; Lakhoua and Crabbé, 1975
; Crabbé and Lakhoua, 1978
; Lauri and Lespinasse, 2001
) and the lack of an extended dormant period (typically related to mild winters; Cook et al., 1998
; Cook and Jacobs, 1999
). Apple has complex axillary branching with three main lateral types: latent bud, vegetative laterals, and reproductive laterals. The latter type is composed of basal spur leaves and a terminal flower cluster. One or two bourse-shoots may develop as relay axes at the axil of basal spur leaves (Fig. 1B) (Pratt, 1988
). Previous studies on apple tree architecture have shown that the sequence of development of the perennial shoot from one year to the next, e.g., the ability of a reproductive lateral to produce another reproductive lateral leading to the bourse-over-bourse phenomenon (Fig. 1C), partly depends on genotype (Looney and Lane, 1984
; Lauri et al., 1995
). A broad range of genotype-related branch architecture (typically high branching frequency and branches composed of short laterals vs. low branching frequency and branches composed of long laterals; Lespinasse and Delort, 1986
; Forshey et al., 1992
) has been documented. The fate and ultimate length of laterals are related to the density of branching which depends on both the frequency of bud latency (Lauri et al., 1995
, 1997
), with latent buds often mixed within the branching zones (Costes and Guédon, 2002
), and the physiological abortion of laterals (known as lateral extinction in a horticultural context; Lauri et al., 1995
). Traits that are known to vary according to position within tree architecture include frequency of flowering (Lauri et al., 2006
), number of spur leaves and flowers of the reproductive shoot in relation to fruit set (Dennis, 1986
), lateral abortion (Lauri et al., 1995
; Costes et al., 2003
), and bourse-over-bourse (Lauri et al., 1997
). However, no studies have been done on a possible acrotonic pattern, i.e., a pattern at the annual shoot level, in the expression of these traits.
|
). To better understand acrotony in apple, I studied the same plant material during the first 2 years of lateral growth. More precisely, I attempted to answer three main questions. (1) Is the proportion of growing laterals vs. latent buds, and the proportion of reproductive vs. vegetative laterals among growing laterals, changed by the position along the parent shoot? (2) Is the upward increase in length that characterizes vegetative laterals also applicable to the number of spur leaves and flowers of the reproductive laterals? (3) Is there an acrotonic trend in the sequence of development of the laterals over the first 2 years after parent shoot growth? MATERIALS AND METHODS
Plant material and sites
The experiment included two apple Malus xdomestica Borkh. cultivars with contrasting growth and flowering habits: the cultivar ‘Pitchounette' (formerly known as the advanced selection X.3318; Lauri and Lespinasse, 2001
), characterized by upright growth of vigorous shoots and higher branching frequency with a strong pattern of alternate flowering from one year to the next; and the cultivar Belchard ‘Chantecler', hereafter referred to as ‘Chantecler', with a lower vigor and branching frequency, and a regular pattern of flowering (Lauri and Lespinasse, 2001
; Lauri and Trottier, 2004
).
The experiment included trees in two experimental plots in the Institut National de la Recherche Agronomique (INRA), experimental fields at Île d'Arcins (IA) and Toulenne (TO), near Bordeaux, in the southwest of France (approximately, 44°30' N, 0°15' W). In each plot, 40 to 45 trees per cultivar, grafted onto Malling 9 (M.9) rootstock, were planted in two adjacent rows, one cultivar per row, with planting distances of 5 m between the rows and 2 m between trees within the row. This system made it possible to establish and maintain scaffold branches in a horizontal position along a wire at a height of approximately 2.2 m on which the studied shoots (48 to 60, depending on the cultivar and the experimental site, Table 1), hereafter referred to as parent shoots, were branched. Parent shoots grew in 1994 in IA and in 1995 in TO. Trees were 5-yr-old at the beginning of the study at both sites. Significant differences in shoot growth and branching were found at the two sites, with more vigorous shoot growth (length, number of nodes) and lower branching frequency at IA than at TO (Table 1). This lower branching frequency at IA was related to a higher number of nodes of parent shoots at IA than at TO because both sites had a similar number of growing laterals (ca. 23; Table 1). There were no significant interactions between site and cultivar for these characteristics, meaning that each cultivar retained its own growth and branching patterns at both sites. Growth orientation was orthotropic, with secondary leaning resulting from the weight of the shoots themselves, leading to wider angles from the vertical in IA than in TO (Table 1). However, there was a highly significant interaction between cultivar and site for branch orientation, preventing simple interpretation (see significant differences between cultivars in TO but not in IA; Table 1). The shoots were not manipulated (pruned or bent) during the experiment. Chemical fruit thinning was used to control fruit load and was supplemented, if necessary, by hand-thinning at the end of the physiological drop (end of May) to leave one fruit per fruitful reproductive lateral.
|
Data analysis compared the effects of the relative position of the lateral on the parent shoot on the studied features, for each combination of cultivar and site. The variability of parent shoot length (Table 1) was accounted for by computing the relative position of each lateral, i.e., by dividing the number of the lateral parent node from bottom by the total number of nodes of the parent shoot. Four zones were determined from proximal (relative positions included in the interval [0 to 0.25]), to distal (relative positions included in the interval [0.75 to 1]). These zones will be hereafter referred to as zone 1 to zone 4, respectively.
The first two analyses were done with Y1 data. A first analysis focused on the proportion of lateral types, i.e., G over all lateral types (G/G+L) and reproductive laterals over all growing laterals (R/G). A second analysis concerned three reproductive lateral features: the number of spur leaves and flowers; the fruit set (number of reproductive laterals with at least one fruit in the total number of reproductive laterals; Lauri et al., 1996
); and for IA only, the flowering date. A third analysis focused on the frequency of transition from a growing lateral, either V or R, in year Y1 to an S in year Y2, represented as (GY1 
SY2)/ GY1, and from either R or V lateral in year Y1 to R lateral in year Y2, represented as sequence (RY1 RY2)/RY1 and sequence (VY1 RY2)/VY1, respectively (Fig. 1C). As in previous papers (Lauri et al., 1995
, 1997
), these three transitions will be hereafter referred to as lateral abortion, bourse-over-bourse, and trend toward flowering, respectively.
Statistical analyses were done using Statistica software (StatSoft France, 2005
). The Fisher F test followed by Newman–Keuls multiple mean comparison test was used to compare normally distributed data (i.e., length, number of nodes, angle from vertical, and number of growing laterals of parent shoots; number of spur leaves and flowers of the reproductive lateral; flowering date), and the Kruskal–Wallis H test followed by multiple mean comparison test was used for non-normally distributed data (i.e., branching frequency and relative frequency of lateral types in year Y1; frequency of transitions between years Y1 and Y2). For comparisons between zones of the number of spur leaves and flowers of reproductive laterals and flowering date, all reproductive laterals of all the parent shoots of a given cultivar–site combination were considered within each zone. For comparisons between zones of the relative frequency of lateral types in year Y1, fruit set, and frequency of transitions between years Y1 and Y2, a frequency was computed for each zone of each shoot and statistics were calculated on the mean frequency for each zone of all shoots of a given cultivar–site combination. Only relative frequencies for each individual shoot zone, and means, with at least five values, were considered.
RESULTS
Branching characteristics in year Y1
The frequency of growing laterals in year Y1 was higher for Pitchounette than for Chantecler at both sites (Fig. 2A). For both cultivars and sites, the frequency of growing laterals increased significantly from zone 1 (less than 0.20) to zone 4 (0.55 to 0.90; Fig. 2A). At the TO site, values were higher in zone 2 than in zone 3 for both cultivars. The proportion of reproductive laterals among growing laterals differed greatly depending on the cultivar; values were high regardless of the position for Chantecler, except a significant decrease in zone 4 in TO site, and values were lower with a continuous increase from zone 1 or 2 to zone 4 for Pitchounette (Fig. 2B).
|
|
|
The present study on apple clearly supported the extension of the acrotony concept to a range of differentiation (e.g., latent vs. vegetative and reproductive laterals) and growth (e.g., number of spur leaves and flowers of reproductive laterals) features at the level of the parent annual shoot. To my knowledge, no such study has been published. These acrotonic gradients affected the dynamics of branch architecture at least over the first two years of lateral branch development following parent shoot growth. Although differences were reported between sites and cultivars, convergent trends were observed.
Differentiation and growth expression of acrotony
An acrotonic trend was found for the proportion of growing laterals among all buds in Chantecler and Pitchounette. This trend is consistent with the results of Fisher (1984)
, Greene and Autio (1994)
, and Brunel et al. (2002)
, who found a greater proportion of latent buds in the proximal and medial zones than in the distal one. The increase of the proportion of growing laterals in zone 2 at the TO site (Fig. 2A) may be interpreted as a specific case of acrotony, not between consecutive annual growth as usually described but between consecutive growth units within the same annual growth (Crabbé, 1984
; Lauri and Térouanne, 1998
). In our study, these two growth units were caused by a drought during parent shoot growth in this site in June 1995, when shoots were reaching half of their final length. Below the intra-annual growth arrest, axillary buds developed at the same time as the parent shoot resumed its growth, giving rise in the same year to short sylleptic shoots. The auxin-insensitivity of overwintered buds below the winter growth arrest has been proposed to explain their spring burst (Cline et al., 2006
). I suggest that the same concept can be extended to non-overwintered buds provided they branch below an intra-annual growth arrest. The proportion of reproductive laterals within growing laterals also had an acrotonic tendency on Pitchounette, for which the proportion of reproductive laterals in year Y1 is generally low (Lauri and Lespinasse, 2001
). This result is consistent with previous results on apricot, which produces more flowers on the second growth unit than on the first one within a same annual growth (Clanet and Salles, 1974
).
The relationship between the number of spur leaves and, to a lesser extent, the number of flowers of the reproductive laterals and fruit set is well documented (Dennis, 1986
; Lauri et al., 1996
). In the current study, these features and the relationships between them varied with both the position along the shoot and the cultivar. Whereas in Chantecler, the three variables increased dramatically from the base to the distal zone, position along the shoot did not consistently affect fruit set in Pitchounette. The lack of effect was probably related to the low proportion of reproductive laterals (Fig. 2B) together with longer parent shoots (Table 1), i.e., to more carbohydrate resources, for Pitchounette than for Chantecler. This could reduce competition between individual reproductive laterals along the same shoot for Pitchounette, enhancing their fruit set ability (Lauri and Térouanne, 1999
).
Lescourret et al. (2000)
found that peach flowers located in the distal part of the shoots were more precocious than flowers in the proximal part. The present study confirmed this trend on Chantecler, which flowered four to five days sooner on reproductive laterals in the distal and medial zones than on those in the proximal zone. Our results suggest that this earlier flowering date is a part of the acrotonic gradient in the reproductive lateral development, a gradient that includes morphological traits, i.e., number of spur leaves, number of flowers, and fruit set. The absence of an acrotonic gradient for the flowering date on Pitchounette could be related to the low proportion of reproductive laterals and thus to less competition between them in this cultivar. The differences between the two cultivars for fruit set and flowering date would then suggest that the expression of acrotonic gradients for these two traits is positively related to competition between individual reproductive laterals along the same annual shoot.
The acrotony concept may be applied to the change in the proportions of the lateral types (latent, vegetative, reproductive) from the proximal to the distal zone. Previous results have shown that the three lateral types can be ranked according to the potential for organogenesis, i.e., number of preformed appendages within the overwintered bud and/or size of the bud. Indeed, the latent bud is smaller than the bud that gives rise to a growing lateral (Brunel et al., 2002
), and among growing laterals, the flower bud has a higher potential for organogenesis than does the vegetative bud (Fulford, 1966
; Abbott, 1977
; Crabbé and Escobedo Alvarez, 1991; Huang, 1996
). The increased frequency of growing laterals at the expense of latent buds and the increased frequency of reproductive laterals within growing laterals at the expense of vegetative laterals upward along the parent shoot (Fig. 2) should therefore be interpreted as a consequence of the increasing organogenetic potential up the parent shoot (from latent to vegetative, from vegetative to reproductive, and among the reproductive laterals enhanced fruit set ability). The intensity of these changes from one lateral type to another lateral type depends on the cultivar: Chantecler, with high flowering in year Y1, only had a change between latent buds and reproductive laterals, whereas Pitchounette, with low flowering in year Y1, had an acrotonic gradient in both the change between latent buds and growing laterals and, within the growing laterals, between vegetative and reproductive laterals.
Branch architecture dynamics
Acrotony illustrates the competitive relationships between laterals along the same annual growth of the parent shoot. This competition is probably not directly related to the carbon physiology in the branch, such as patterns of resource assimilation, distribution, and utilization, as defined by the "branch autonomy" theory. In this theory, the autonomous physiological unit varies throughout the year but is generally larger than the annual shoot (Watson, 1986
; Sprugel et al., 1991
; Lacointe et al., 2004
).
The genetic and physiological control of lateral organogenesis begins as soon as the axillary meristem develops during metamer growth (Shimizu-Sato and Mori, 2001
; Brunel et al., 2002
). Therefore, the hierarchy between laterals, whether they are latent buds, vegetative laterals, or reproductive laterals, is determined early in parent shoot growth.
Branching involves the formation of the axillary meristem, its differentiation, and the subsequent growth of the lateral. The former two steps, at the organogenetic level, are likely to be controlled by various factors such as a genetic control (in apple bud, for example, growth potential is negatively correlated with KNAP2 expression; Brunel et al., 2002
) and hormones (Shimizu-Sato and Mori, 2001
). In the latter case, a balance between auxin and cytokinin is assumed, the former inhibiting axillary bud growth and the latter promoting it (Stirnberg et al., 1999
; Cook and Bellstedt, 2001
; Cook et al., 2001
; Tantikanjana et al., 2001
). Wilson and Gartner (2002)
hypothesized that hormone action is indirect in stimulating parent shoot cambial activity, creating competitive sinks for carbohydrates with the parent branch. Our analysis of lateral development revealed that once the axillary meristem forms, lateral growth and possibly abortion in the year following parent shoot growth also depends on a late organogenesis process. Lateral abortion could well illustrate this phenomenon. As noted by Lauri et al. (1995)
, lateral abortion can affect meristems that have already differentiated flowers, where it is related to the abortion of potential bourse-shoots within the preformed bud. It is likely that the preformed bourse-shoots are poor competitors for metabolites because they form late within the bud and are small, i.e., two- to three-leaf primordia by the end of the growing season (Pratt, 1988
, 1990
; Crabbé and Escobedo-Alvarez, 1991
), compared to the 10 leaves enclosed in the vegetative bud (Rivals, 1965
). The increased downward frequency of lateral abortion would then suggest intense competition for carbohydrates with laterals located farther up the annual parent shoot and/or with cambial activity greater in the proximal than in the distal part of the parent shoot (Forshey and Elfving, 1989
; Barnola and Crabbé, 1993
).
The growth potential of the parent shoot and especially growth rhythm, which may lead to more than one growth unit in the same year, are presumably important in triggering the within-year acrotonic pattern, giving rise to different lateral types and, in the case of reproductive laterals, to different numbers of spur leaves and flowers, different dates of flowering, and different fruit sets. This study showed that the distal zone was characterized by the following three phenomena: higher bourse-over-bourse, i.e., higher organogenesis in the terminal bud of the bourse-shoot, lower lateral abortion, and lower proportion of latent buds. The last two phenomena led to an increased branching density in the distal zone than in the proximal zones. This finding is supported by Crabbé (1985)
, who documented greater competition between zones of laterals than between individual laterals on the one-year-old branching system. In our study, the upward increase in the frequency of flowering in year Y1 and in bourse-over-bourse would indicate that this higher organogenetic potential was reinforced over at least two years. These results would well agree with the hypothesis that once a priority is given to an organ, a self-organization process (positive feedback) leads to the greater development of that organ at temporal (earlier development) and spatial (higher organogenesis and growth potential) levels. This concept is illustrated by various studies on fruit set and fruit development in peach (Lescourret et al., 2000
) and apple (Lauri and Trottier, 2004
), and on branch hierarchy (Novoplansky, 2003
). This process could apply to both source capacity (i.e., longer vegetative laterals supply more photosynthates) and sink strength (e.g., larger reproductive laterals have higher fruit set potential and fruit demand). The greater and earlier development of distally located laterals leads to a poorly branched proximal zone made of latent buds and of aborted laterals, and highly branched distal and possibly medial zones with vigorous vegetative laterals and/or larger reproductive laterals, depending on the cultivar (Lauri and Lespinasse, 2001
).
In the current debate on the molecular basis and phytohormonal control of plant development, apical dominance (the inhibition of growth of laterals along the current annual shoot) is often considered a leading conceptual framework (e.g., Benett and Leyser, 2006
). In contrast, acrotony receives much less attention. One of the likely reasons is that apical dominance occurs on both annual herbaceous and perennial plants, whereas acrotony occurs largely on perennials. However, the integration of a detailed understanding of hierarchical relationships between laterals within the growing shoot (apical dominance) and within the two-year branch complex, i.e., including the parent shoot with its laterals (acrotony), provides a framework for the analysis of the architectural development of perennial plants. Although annual and perennials probably have common regulation mechanisms, perennial plants, and especially trees, undoubtedly have patterns not found in annual plants. Indeed, as evidenced in the present study, the competitive interactions between laterals not only resulted from a greater organogenetic potential and growth of some laterals, but also depended on the physiological abortion (i.e., growth followed by death) and latency (i.e., no expression of growth) of the remaining laterals. Recent molecular studies showing strong relationships between axillary meristem formation and vascular differentiation (Schmitz and Theres, 2005
) also suggest the involvement of the vascular system in these architectural patterns. Together these elements provide a conceptual framework for the study of the expression of hierarchies between branches, not only within a same branch complex but also within the whole plant.
FOOTNOTES
1 The author thanks J.-M. Lespinasse for help in setting up experiments and for valuable discussions on apple shoot architecture, F. Delort, L. Fouilhaux and G. Garcia for help in recording and typing field data, G. Wagman for improving the English, and two anonymous reviewers for helpful comments and suggestions. 
LITERATURE CITED
Abbott D. L.. 1977. Fruit-bud formation in Cox's Orange Pippin. Annual Report of Long Ashton Research Station for 1976, 167-176.
Barnola P. Crabbé J.. 1993. L'activité cambiale, composante active ou passive dans les réactions de croissance de l'arbre. Acta Botanica Gallica 140: 403-412.[ISI]
Barthélémy D. Caraglio Y.. 2007. Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Annals of Botany 99: 375-407.
Bell A.. 1991. Plant form—an illustrated guide to flowering plant morphology Oxford University Press, Oxford, UK.
Bennett T. Leyser O.. 2006. Something on the side: axillary meristems and plant development. Plant Molecular Biology 60: 843-854.[CrossRef][ISI][Medline]
Bory G. Clair-Maczulajtys D.. 1988. Aptitude au débourrement des bourgeons et répartition des glucides dans la pousse d'un an de l'Ailanthus glandulosa Desf. (Simarubacées). Bulletin de la Société Botanique de France 135, Actualités Botaniques 1: 81-90.
Brown C. L McAlpine P. P. Kormanik R. G.. 1967. Apical dominance and form in woody plants: a reappraisal. American Journal of Botany 54: 153-162.[CrossRef][ISI]
Brunel N. Leduc N. Poupard P. Simoneau P. Mauget J. C. Viémont J. D.. 2002. KNAP2, a class I KN1-like gene is a negative marker of bud growth potential in apple trees (Malus domestica [L.] Borkh). Journal of Experimental Botany 53: 2143-2149.
Champagnat P.. 1954. Les corrélations sur le rameau d'un an des végétaux ligneux. Phyton 4: 1-102.[Medline]
Champagnat P.. 1965. Physiologie de la croissance et de l'inhibition des bourgeons: dominance apicale et phénomènes analogues. In W. Ruhland [ed.], Hanbuch der Pflanzenphysiologie, vol. 15 1106-1164 Springer Verlag, Berlin, Germany.
Champagnat P.. 1966. Quelques caractères de la ramification du rameau d'un an des végétaux ligneux. Société Pomologique Française, 96ème session 9-36.
Champagnat P. Barnola P. Lavarenne S.. 1971. Premières recherches sur le déterminisme de l'acrotonie des végétaux ligneux. Annales des Sciences Forestières 28: 5-22.
Clanet H. Salles J. C.. 1974. Contribution à l'étude de la fructification de l'abricotier dans des conditions climatiques différentes. Annales de l'Amélioration des Plantes 24: 97-127.
Cline M. G. Yoders M. Desai D. Harrington C. Carlson W.. 2006. Hormonal control of second flushing in Douglas-fir shoots. Tree Physiology 26: 1369-1375.[ISI][Medline]
Cook N. C. Bellstedt D. U.. 2001. Chilling response of ‘Granny Smith' apple lateral buds inhibited by distal shoot tissues. Scientia Horticulturae 89: 299-308.[CrossRef]
Cook N. C. Bellstedt D. U. Jacobs G.. 2001. Endogenous cytokinin distribution patterns at budburst in Granny Smith and Braeburn apple shoots in relation to bud growth. Scientia Horticulturae 87: 53-63.[CrossRef]
Cook N. C. Jacobs G.. 1999. Suboptimal winter chilling impedes development of acrotony in apple shoots. HortScience 34: 1213-1216.
Cook N. C. Rabe E. Keulemans J. Jacobs G.. 1998. The expression of acrotony in deciduous fruit trees: a study of the apple rootstock M.9. Journal of the American Society for Horticultural Science 123: 30-34.
Costes E.. 2003. Winter bud content according to position in 3-year-old branching systems of ‘Granny Smith' apple. Annals of Botany 92: 581-588.
Costes E. Fournier D. Salles J. C.. 2000. Changes in primary and secondary growth as influenced by crop load effects in ‘Fantasme®' apricot trees. Journal of Horticultural Science & Biotechnology 75: 510-519.[ISI]
Costes E. Guédon Y.. 2002. Modelling branching patterns on 1-year-old trunks of six apple cultivars. Annals of Botany 89: 513-524.
Costes E. Sinoquet H. Kelner J. J. Godin C.. 2003. Exploring within-tree architectural development of two apple tree cultivars over 6 years. Annals of Botany 91: 91-104.
Crabbé J.. 1969. Répartition spatiale et caractéristiques de la croissance des ramifications suscitées par l'arcure de la pousse d'un an de boutures de pommier. Bulletin de Recherche Agronomique de Gembloux 4: 220-239.
Crabbé J.. 1981. The interference of bud dormancy in the morphogenesis of trees and shrubs. Acta Horticulturae 120: 167-172.
Crabbé J.. 1984. Vegetative vigor control over location and fate of flower buds, in fruit trees. Acta Horticulturae 149: 55-63.
Crabbé J.. 1985. Aspects of the apical control on branching on one-year-old caulinary axes of woody plants. Acta Universitatis Agriculturae, Brno, Czechoslovakia 33: 555-560.
Crabbé J. Escobedo-Alvarez J. A.. 1991. Activités méristématiques et cadre temporel assurant la transformation florale des bourgeons chez le Pommier (Malus xdomestica Borkh., cv. Golden Delicious). In C. Edelin [ed.], L'arbre, biologie et développement, 2ème Colloque International sur l'Arbre 369-379 Naturalia Monspeliensia, Hors Série, Montpellier, France.
Crabbé J. Lakhoua H.. 1978. Arcure et gravimorphisme chez le Pommier. Mise en évidence d'effets gravimorphiques sur bourgeons isolés, après induction de ces effets en diverses conditions. Annales des Sciences Naturelles, Botanique et Biologie Végétale 19: 126-140.
Dennis F. G.. 1986. Apple. In S. P. Monselise [ed.], CRC Handbook of fruit set and development 1-44 CRC Press, Boca Raton, Florida, USA.
Fisher J. B.. 1984. Tree architecture: relationships between structure and function. In R. A. White [ed.], Contemporary problems in plant anatomy 541-589 Academic Press, New York, New York, USA.
Forshey C. G. Elfving D. C.. 1989. The relationship between vegetative growth and fruiting in apple trees. Horticultural Reviews 11: 229-287.
Forshey C. G. Elfving D. C. Stebbins R. L.. 1992. Training and pruning apple and pear trees American Society for Horticultural Science, Alexandria, Virginia, USA.
Fulford R. M.. 1966. The morphogenesis of apple buds. IV. The effect of fruit. Annals of Botany 30: 597-606.
Greene D. W. Autio W. R.. 1994. Notching techniques increase branching of young apple trees. Journal of the American Society for Horticultural Science 119: 678-682.
Guédès M.. 1977. L'anticipation des bourgeons et des rameaux—Esquisse morphologique. Botanische Jahrbücher 3: 336-361.
Guédon Y. Barthélémy D. Caraglio Y. Costes E.. 2001. Pattern analysis in branching and axillary flowering sequences. Journal of Theoretical Biology 212: 481-520.[CrossRef][ISI][Medline]
Hallé F. Oldeman R. A. A. Tomlinson P. B.. 1978. Tropical trees and forests. An architectural analysis Springer-Verlag, Berlin, Germany.
Huang H.. 1996. Flower bud development in apple trees as related to node formation. Journal of Fruit and Ornamental Plant Research 4: 95-107.
Lacointe A. Deléens E. Ameglio T. Saint-Joanis B. Lelarge C. Vandame M. Song G. C. Daudet F. A.. 2004. Testing the branch autonomy theory: a 13C/14C double-labelling experiment on differentially shaded branches. Plant, Cell & Environment 27: 1159-1168.[CrossRef]
Lakhoua H. Crabbé J.. 1975. Arcure et gravimorphisme chez le Pommier. III. Effets de diverses époques d'arcure échelonnées de l'automne au débourrement printanier. Bulletin de Recherche Agronomique de Gembloux 10: 65-74.
Lauri P. É. Lespinasse J. M.. 2001. Genotype of apple trees affects growth and fruiting responses to shoot bending at various times of year. Journal of the American Society for Horticultural Science 126: 169-174.
Lauri P. É. Maguylo K. Trottier C.. 2006. Architecture and size relations—an essay on apple (Malus x domestica, Rosaceae) tree. American Journal of Botany 93: 357-368.
Lauri P. É. Térouanne É.. 1998. The influence of shoot growth on the pattern of axillary development on the long shoots of young apple trees (Malus domestica Borkh). International Journal of Plant Sciences 159: 283-296.[CrossRef][ISI]
Lauri P. É. Térouanne É.. 1999. Effects of inflorescence removal on the fruit set of the remaining inflorescences and development of the laterals on one year old apple (Malus domestica Borkh.) branches. Journal of Horticultural Science & Biotechnology 74: 110-117.[ISI]
Lauri P. É. Térouanne É. Lespinasse J. M.. 1996. Quantitative analysis of relationships between inflorescence size, bearing-axis size and fruit-set: an apple tree case study. Annals of Botany 77: 277-286.
Lauri P. É. Térouanne É. Lespinasse J. M.. 1997. Relationship between the early development of apple fruiting branches and the regularity of bearing—an approach to the strategies of various cultivars. Journal of Horticultural Science 72: 519-530.[ISI]
Lauri P. É. Térouanne É. Lespinasse J. M. Regnard J. L. Kelner J. J.. 1995. Genotypic differences in the axillary bud growth and fruiting pattern of apple fruiting branches over several years—an approach to regulation of fruit bearing. Scientia Horticulturae 64: 264-281.
Lauri P. É. Trottier C.. 2004. Patterns of size and fate relationships of contiguous organs in the apple (Malus domestica Borkh.) crown. New Phytologist 163: 533-546.[CrossRef][ISI]
Lescourret F. Inizan O. Génard M.. 2000. Analyse de l'étalement temporal de la floraison et influence sur la variabilité intra-arbre de la chute et de la croissance précoce des pêches. Canadian Journal of Plant Science 80: 129-136.[ISI]
Lespinasse J. M. Delort J. F.. 1986. Apple tree management in VERTICAL AXIS: appraisal after ten years of experiments. Acta Horticulturae 160: 120-155.
Looney N. E. Lane W. D.. 1984. Spur-type growth mutants of McIntosh apple: a review of their genetics, physiology and field performance. Acta Horticulturae 146: 31-46.
Novoplansky A.. 2003. Ecological implications of the determination of branch hierarchies. New Phytologist 160: 111-118.[CrossRef][ISI]
Powell G. R.. 1995. The role of acrotony in reproductive development in Picea. Tree Physiology 15: 491-498.[ISI][Medline]
Pratt C.. 1988. Apple flower and fruit: morphology and anatomy. Horticultural Reviews 10: 273-308.
Pratt C.. 1990. Apple trees: morphology and anatomy. Horticultural Reviews 12: 265-305.
Puntieri J. G. Stecconi M. Barthélémy D.. 2002. Preformation and neoformation in shoots of Nothofagus antarctica (G. Forster) Oerst. (Nothofagaceae) shrubs from northern Patagonia. Annals of Botany 89: 665-673.
Rivals P.. 1965. Essai sur la croissance des arbres et sur leurs systèmes de floraison (application aux espèces fruitières). Journal d'Agriculture Tropicale Botanique Appliquée 12: 655-686.
Schmitz G. Theres K.. 2005. Shoot and inflorescence branching. Current Opinion in Plant Biology 8: 506-511.[CrossRef][ISI][Medline]
Shimizu-Sato S. Mori H.. 2001. Control of outgrowth and dormancy in axillary buds. Plant Physiology 127: 1405-1413.
Sprugel D. G. Hinckley T. M. Schaap W.. 1991. The theory and practice of branch autonomy. Annual Review of Ecology and Systematics 22: 309-334.[CrossRef][ISI]
StatSoft France.. 2005. STATISTICA (software for data analysis), version 7.1 http://www.statsoft.fr.
Stirnberg P. Chatfield S. P. Leyser H. M. O.. 1999. AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. Plant Physiology 121: 839-847.
Tantikanjana T. Yong J. W. H. Letham D. S. Griffith M. Hussain M. Ljung K. Sandberg G. Sundaresan V.. 2001. Control of axillary bud initiation and shoot architecture in Arabidopsis through the SUPERSHOOT gene. Gene & Development 15: 1577-1588.[CrossRef]
Vincent G.. 1995. Étude expérimentale de la ramification acrotone d'un Pelargonium ligneux (géranium rosat). Canadian Journal of Botany 73: 1557-1566.
Walsh C. S.. 1979. The effects of node position, shoot vigor, and strain on ‘Delicious' apple spur development. Journal of the American Society for Horticultural Science 104: 825-828.
Wareing P. F. Nasr T. A. A.. 1961. Gravimorphism in trees. I. Effect of gravity on growth and apical dominance in fruit trees. Annals of Botany, NS, 25: 321-340.
Watson M. A.. 1986. Integrated physiological units in plants. Trends in Ecology and Evolution 1: 119-123.[CrossRef]
Wilson B. F.. 2000. Apical control of branch growth and angle in woody plants. American Journal of Botany 87: 601-607.
Wilson B. F. Gartner B. L.. 2002. Effects of phloem girdling in conifers on apical control of branches, growth allocation and air in wood. Tree Physiology 22: 347-353.[ISI][Medline]
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
