AOBPreview originally published online on January 11, 2007
Annals of Botany 2007 99(3):375-407; doi:10.1093/aob/mcl260
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INVITED REVIEW |
Plant Architecture: A Dynamic, Multilevel and Comprehensive Approach to Plant Form, Structure and Ontogeny
1 INRA
2 Cirad, Unité Mixte de Recherche (UMR) Cirad-Cnrs-Inra-Ird-Université Montpellier 2, ‘botAnique et bioinforMatique de l'Architecture des Plantes’ (AMAP), TA40/PS2, Boulevard de la Lironde, 34398 Montpellier Cedex 5, France
* For correspondence. E-mail daniel.barthelemy{at}cirad.fr
Received: 20 May 2006 Returned for revision: 31 July 2006 Accepted: 20 September 2006 Published electronically: 11 January 2007
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ABSTRACT |
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TOP
ABSTRACT
INTRODUCTIONBackground and Aims: The architecture of a plant depends on the nature and relative arrangement of each of its parts; it is, at any given time, the expression of an equilibrium between endogenous growth processes and exogenous constraints exerted by the environment. The aim of architectural analysis is, by means of observation and sometimes experimentation, to identify and understand these endogenous processes and to separate them from the plasticity of their expression resulting from external influences.
Scope: Using the identification of several morphological criteria and considering the plant as a whole, from germination to death, architectural analysis is essentially a detailed, multilevel, comprehensive and dynamic approach to plant development. Despite their recent origin, architectural concepts and analysis methods provide a powerful tool for studying plant form and ontogeny. Completed by precise morphological observations and appropriated quantitative methods of analysis, recent researches in this field have greatly increased our understanding of plant structure and development and have led to the establishment of a real conceptual and methodological framework for plant form and structure analysis and representation. This paper is a summarized update of current knowledge on plant architecture and morphology; its implication and possible role in various aspects of modern plant biology is also discussed.
Key words: Plant morphology, plant architecture, level of organization, growth, branching, differentiation, morphogenetic gradients, physiological age, meristem, annual shoot, phenotypic plasticity, ontogeny, phase change
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INTRODUCTION |
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Progress in our understanding of plants has increased dramatically in recent decades and research in this domain has given rise to analytical, methodological and theoretical innovations on various aspects of plant science (Sattler and Rutishauser, 1997; Hedden et al., 2002; Turnbull, 2005).
Plant form, development and evolution have been analysed under the functional view of biomechanics (Niklas, 1992, 2005; Rowe and Speck, 2005) and pollination ecology or population biology (White, 1979; Harper, 1985; Diggle, 2003; Friedman and Harder, 2004, 2005). The importance of phenotypic plasticity, phenology and crown architecture in evolutionary plant ecology or in the understanding of community and stand structure, functioning and production has been stressed by several authors (Givnish, 1984; King, 1998; Diggle, 1999, 2002; Huber et al., 1999; Alpert and Simms, 2002; Novoplansky, 2002; Wright et al., 2002; Oborny, 2004; Sachs, 2004; Damascos et al., 2005; de Kroon et al., 2005; Pearcy et al., 2005; Wolfe and Mazer, 2005).
Since its introduction and definition by von Goethe (1790), plant morphology has had a successful history and it is commonly accepted that plants are modular organisms that develop by the repetition of elementary botanical entities whose morphological, dimensional, functional and anatomical features change during ontogeny and according to several processes variously called heteroblasty, phase change, life stages, maturation, ageing, age states or morphogenetic progression (Goebel, 1900; Troll and Rauh, 1950; Robbins, 1957; Wareing, 1959, 1961; Nozeran et al., 1971, 1982; Nozeran, 1978, 1984; Gatsuk et al., 1980; Greenwood, 1987, 1995; Poethig, 1990; Jones, 1999, 2001; Claßen-Bockoff, 2001; Kaplan, 2001). As plant morphology deals with plant form and/or structure and with their temporal and/or topological changes during ontogeny and even phylogeny, it is therefore relevant to practically all the disciplines of modern plant biology cited above (Sattler, 1978; Roloff, 1988; Sattler and Rutishauser, 1997; Gleißner, 1998; Claßen-Bockhoff, 2000, 2005; Kaplan 2001; Scotland et al., 2003; Wiens, 2004; Mueller, 2006).
The study of plant architecture emerged as a new scientific discipline some 30 years ago, and derived, in several ways, from earlier works on plant morphology (Hallé and Oldeman, 1970; Oldeman, 1974; Hallé et al., 1978). An original feature of architectural studies is that they were initiated in tropical regions and were, at first, concerned with the analysis of the aerial vegetative structure of tropical trees (Hallé and Oldeman, 1970). Since their definition, architectural concepts have provided powerful tools for studying plant form or even tropical forest structure and the understanding of its dynamics (Oldeman, 1974, 1983, 1990; Hallé et al., 1978; Vester, 1997). Investigations based on these concepts quickly spread to temperate species (Edelin, 1981; Caraglio and Edelin, 1990; Gleißner, 1998; Nicolini, 1998; Grosfeld et al., 1999; Millet et al., 1999; Sabatier and Barthélémy, 1999; Claßen-Bockhoff, 2000; Stecconi et al., 2000), herbs (Jeannoda-Robinson, 1977; Blanc, 1978; de Castro e Santos, 1981; Gay, 1993; Cremers and Edelin, 1995; Rua and Gróttola, 1997; Perreta et al., 2000), lianas (Cremers, 1973; Coudurier, 1992; Caballé, 1998) and root systems (Atger and Edelin, 1994a, b; Jourdan and Rey,1997a, b). The architecture of a plant depends on the nature and on the relative arrangement of each of its parts; it is, at any given time, the expression of an equilibrium between endogenous growth processes and exogenous constraints exerted by the environment. The aim of architectural analysis is to identify these endogenous processes and to separate them from the plasticity of their expression resulting from external influences by means of observation and sometimes experimentation. Considering the plant as a whole, from germination to death, architectural analysis is essentially a global, multilevel and dynamic approach to plant development. For each species, at each stage of development and in each environmental condition, careful qualitative and quantitative morphological or even anatomical observations are made on varying numbers of individuals, depending on the complexity of the architecture. Small plants can be analysed, observed and manipulated directly but this is hardly possible when plants reach several metres high. For the highest and biggest trees, some qualitative observations can be carried out from ground level (Barthélémy et al., 1989, 1991; Millet et al.,1998b; Nicolini, 1998) but the use and practice of destructive methods are most generally necessary for more precise analysis and data collection (Heuret et al., 2000, 2002; Passo et al., 2002). Results of field observations are summarized in a series of diagrams that symbolize successive growth stages or developmental steps, whereas quantitative analyses are grouped and made according to this qualitative knowledge. The validity of these diagrams and analyses is then checked by comparing them with reality and they must apply to the architecture of any individual of the same species encountered in the field for the study to be considered as complete.
Applicable to any kind of plant, architectural analysis has proved to be one of the most efficient means currently available for the study of the organization of complex arborescent plants. Architectural concepts appear to be of particular interest for the understanding of crown construction in trees. Completed by precise morphological observations and innovative computational aspects, recent research in this field has greatly increased our understanding of plant structure and development and has led to the establishment of a real conceptual and methodological framework for plant form analysis and understanding (Barthélémy et al.,1997a; Bouchon et al., 1997; Caraglio and Barthélémy, 1997; de Reffye and Houllier, 1997; Godin and Caraglio, 1998; de Reffye et al., 1998; Guédon et al., 2001, 2003; Hu and Jaeger, 2003; Yan et al., 2004).
The present paper describes major concepts and notions that are currently used in plant architecture and morphology description. It aims to provide a summarized update of our knowledge in this field. The possible applications, implications and roles of plant architecture in modern and current plant research are discussed.
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MORPHOLOGICAL BASES AND CRITERIA FOR PLANT ARCHITECTURE DESCRIPTION AND ANALYSIS |
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Plant morphology, in its historical and broader sense and as a synthetic discipline (see, for example, Sattler, 1978; Claßen-Bockoff, 2001; Kaplan, 2001; Mueller, 2006), may be considered as one of the main ‘inspiring soul’ of plant architecture studies. In this section, however, we will only illustrate the main morphological traits that are commonly used in plant architectural analysis (for a more comprehensive and general illustration and survey of other morphological traits we refer the reader to Troll, 1937 or Bell, 1991). These traits are well documented in previous synthetic works (Hallé and Oldeman, 1970; Hallé et al., 1978) and they may be grouped according to four major categories: (1) growth process, (2) branching process, (3) the morphological differentiation of axes and (4) the position (lateral vs. terminal) of reproductive structures. Although they correspond to basic morphological concepts, their associated terminology proved to be sometimes confused and led to incorrect interpetations. They were thus recently discussed and sometimes redefined (Caraglio and Barthélémy, 1997, and see below).
Growth process
The primary growth of a plant is the result of several processes that can be grouped into two distinct, but co-ordinated morphogenetic events: organogenesis and extension (Champagnat et al., 1986). The inception of new organs (organogenesis) results from the functioning of undifferentiated cells constituting the apical meristem (Fig. 1A). Located at the tip of a stem, this meristem forms, when in an active phase, small cell masses with different potentialities (Lyndon, 1988; Nougarède, 2001); these masses develop into embryonic leaves, then leaves on elongated stems. The insertion zone of a leaf on the stem is referred to as a node and the stem portion which separates two successive nodes is called the internode. According to species and phyllotaxis, one, two or more leaves may be inserted at one node and one to several, named supernumerary, buds (see Fig. 8) may develop at the axil of each individual leaf. A stem can thus be considered as a succession of internodes and the entity formed by a node, associated with its leaf (or leaves) and axillary bud(s) plus the subtending internode, represents the basic structural unit of the plant body commonly called the metamer or phytomer (White, 1979; Barlow, 1989). During growth, the superposition and repetition of this elementary entity builds up the leafy axis (Fig. 1B).
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Plant growth may be considered in several ways according to the kind of organ and/or level of organization concerned (growth of a leaf, a stem, a fruit, the whole plant, etc.). As we are dealing here with the topological edification of the stem and macroscopic aspects of plant growth, we will focus mainly on the extension process of the leafy axis or shoot and will neither detail organogenesis processes nor consider secondary (sensu Fahn, 1967) or radial growth.
Determinate vs. indeterminate growth (Fig. 2)
In many plant species, the apex may abscise or abort after some period of functioning (Garrison and Wetmore, 1961; Millington, 1963; Puntieri et al., 1998, 1999) or it may transform into a specialized structure (flower, inflorescence, spine, tendril, parenchymatous cells, etc.) lacking further extension capacity. In these cases, the axis is considered to have a determinate growth (Fig. 2A–C; Hallé et al., 1978; ‘definite extension’, Bell, 1991). By contrast, indeterminate growth (Hallé et al., 1978) or indefinite extension (Bell, 1991) refers to an axis on which apical meristem indefinitely maintains its growth potential (Fig. 2D). As the indefinite functioning of an apex is always limited at least by the limited life span of the plant it belongs to, this ultimate term is somewhat ‘theoretical’ and a misuse of the language (Guinochet, 1965). Nonetheless, this notion is useful and justified by the necessity to describe and name this phenomenon.
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Rhythmic vs. continuous growth
Hallé et al. (1978) distinguished shoots which have no marked endogenous cessation of extension (continuous growth) from shoots which have marked endogenous periodicity and cessation of extension (rhythmic growth; Hallé and Martin, 1968). Although organogenesis may be considered or known, these two growth patterns are generally more concerned with extension.
Continuous extension (Fig. 3A, B) is quite a rare phenomenon in the field and has generally been observed and described mostly in uniform equatorial climates or environments (mainly palm or mangrove trees; Venkatanarayana, 1957; Rees, 1964; Gill and Tomlinson, 1971) or for some herbs native to temperate (Bell, 1991) or tropical (Blanc, 2002) regions. In all these cases, plants exhibit a more or less constant production of leaves and/or shoots throughout the year. For the mangrove trees Rhizophora mangle (Gill and Tomlinson, 1971), growing in the subtropical climate of Florida, it was shown that the extension of each axis may have a fluctuating rate according to the seasonal climatic conditions, without ever being interrupted completely (Fig. 3B). In some cases, the endogenous nature of continuous extension may be ‘masked’ by fluctuating environmental conditions in the field and can be revealed experimentally by growing plants in favourable and constant conditions, as was demonstrated for several temperate Cupressaceae from the Southern Hemisphere (Grosfeld and Barthélémy, 2004). It has been shown that plants with continuous extension may also present a continuous production of new embryonic leaves, i.e. organogenesis (Gill and Tomlinson, 1971). As far as it has been documented, when extension is continuous the resulting stem is generally quite homogeneous and successive metamers and their constitutive elements are more or less of the same type and size along the elongated axis (Fig. 3A, B, right; Tomlinson and Gill, 1973; Hallé et al., 1978).
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Rhythmic extension of leafy axes is a far more frequent growth pattern in plants, regardless of their geographical origin, and is expressed by an alternation of periods of rest in meristem activity and periods of active shoot extension or ‘growth flushes’ (Fig. 3C). This rhythmic growth has been thoroughly studied by numerous authors (Alvim, 1964; Kozlowski, 1971; Hallé et al., 1978; Puntieri et al., 1998; Sabatier and Barthélémy, 1999).Hallé and Martin (1968), in their detailed study of the tropical tree Hevea brasiliensis, defined the ‘growth unit’ as the portion of an axis which develops during an uninterrupted period of extension. A growth unit is generally easy to identify on the elongated stem as the limit between two growth units is usually marked by a zone of short internodes and/or cataphylls (i.e. scale leaves) corresponding to the protective organs of the bud from which it derives (Fig. 4). Even if very common in rhythmically growing axes, this alternation of cataphylls and leaves (termed articulate growth by Tomlinson and Gill, 1973; Fig. 3C right, Fig. 4) may not be obvious in some species, and other morphological or macro-anatomical markers may sometimes be used in addition, for the a posteriori identification of a rhythmically elongating axis (Fig. 5).
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As with continuous growth, the identification of the endogenous nature of rhythmic growth, for plants naturally growing in seasonal climates, requires experimental verification in controlled, constant and favourable environmental conditions (Greathouse et al., 1971; Lavarenne, 1971; Payan, 1982; Parisot, 1985). Regardless, the rhythmic (or continuous) pattern of a shoot or axis growth must be checked by periodic measurement of its length. In practice, most often only the extension component of growth is known, such that some authors have proposed the use of the term ‘unit of extension’ (Gill and Tomlinson, 1971; Hallé et al., 1978) rather than growth unit, even though the two terms are synonymous. When organogenesis is known, it has been shown that the rhythmic extension of the stem may be combined either with a continuous (Bond, 1942) or more frequently, a rhythmic (Hallé and Martin, 1968; Gill, 1971; Puntieri et al., 2002a; Sabatier et al., 2003b) organogenesis pattern. In the latter case, it has been proposed that the ‘unit of morphogenesis’ is the axis portion corresponding to an uninterrupted phase of organogenesis (Hallé and Martin, 1968). Despite its relevance for the understanding of growth patterns in plants, the nature of the unit of morphogenesis is unknown in most cases partly owing to the long and tedious experimental work needed for its identification.
Preformation and neoformation
In the case of rhythmic growth, all the metamers and organs of the future elongated shoot may be present at an embryonic stage in a bud before the elongation of the shoot deriving from it; in this case the shoot is referred to as ‘preformed’ and its constitutive organs as ‘preformed organs’ or ‘preformation’ (Hallé et al., 1978; ‘early leaves’, Critchfield, 1960; ‘fixed growth’, Lanner, 1976). The duration of preformed organs at an embryonic stage in a bud may vary from several days or weeks (Hallé and Martin, 1968; Sabatier et al., 1995) to several years (Aydelotte and Diggle, 1997; Diggle, 1997; Meloche and Diggle, 2001). In other cases, more organs than those included at an embryonic stage in the bud are elongated: these supplementary, non-preformed elements are referred to as ‘neoformed organs’ (i.e. ‘neoformation’ sensu Hallé et al., 1978, or ‘late leaves’, Critchfield, 1960; ‘free growth’, Jablanczy, 1971; Lanner, 1976). As a consequence stems or shoots may comprise only preformed metamers (Critchfield, 1960; Rivals, 1965, 1966; Gill, 1971; Roloff, 1985; Sabatier et al., 1995; Nicolini, 1998; Puntieri et al., 2000, 2002a, b; Souza et al., 2000) or, more rarely, may be entirely neoformed (Borchert, 1969; El-Morsy, 1991). In many cases, a preformed part can be followed by a neoformed part and thus give rise to a mixed shoot (Critchfield, 1960; Hallé and Martin, 1968; Kozlowski, 1971; Nitta and Ohsawa, 1998; Puntieri et al., 2000, 2002b; Souza et al., 2000; Seleznyova et al., 2002; Costes et al., 2003; Gordon et al., 2006). As discussed in recent studies, the amount of preformation or the relative extent of preformation and neoformation in shoots may vary both between and within species according to external or internal parameters. For a number of tree species, preformation seems to be more relevant than neoformation in the mean number of organs developed by a shoot at a specific position within a tree's architecture (Remphrey and Davidson, 1994; Puntieri et al., 2000, 2002b; Souza et al., 2000). Neoformation responses within a specific position of a tree would be involved in the plastic response of trees to factors acting locally at the time of shoot extension (Remphrey and Powell, 1984; Gordon et al., 2006; Guédon et al., 2006).
Annual shoot (Fig. 6)
In rubber trees growing in equatorial conditions (Hallé and Martin, 1968), an axis with indeterminate growth forms a new growth unit about every 45 d and these successive units are morphologically identical (cf. Fig. 3C) so that the growth unit level itself is pertinent to describe the infrastructure of an axis and its morphological heterogeneity. In other tropical species, however, the timing of rhythmic extension during a whole calendar year is more complex. In Ryania speciosa var. subuliflora (Comte, 1993), for instance, the annual growth pattern corresponds to the extension of two growth units in a relatively short time, followed by a long resting phase, which again is followed by the rapid emission of a succession of two growth units. In some temperate species, shoot extension may occur in one, two or more successive events in a same growing season giving rise to an ‘annual shoot’ made up of one or a succession of several growth units or growth cycles (respectively monocyclism vs. polycyclism, i.e. Bugnon and Bugnon, 1951 or Lanner 1976, and see Caraglio and Barthélémy, 1997, for a critical and historical revision of these terms) occurring in a vegetative cycle (period between two marked seasons or two winters, Lanner, 1976). When several successive growth units are formed in the same annual vegetative cycle these growth units most often present distinctive features (Fig. 6); spring shoots and summer or additional shoots are frequently distinguished (Späth, 1912; Kozlowski, 1971; Cannell et al., 1976). In this situation, successive growth units produced in a same year are thus not identical and it is useful and pertinent to distinguish an annual-shoot level of organization.
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According to the number of constitutive growth units of an annual shoot and according to the indeterminate vs. determinate nature and to the relative extent of preformation and neoformation in each of the constitutive growth units, several combinations may exist for different species or even for a single species, depending on external and/or internal conditions (Lanner, 1971, 1976; de Reffye et al., 1991; Costes, 1993; Fontaine et al., 1999; Heuret et al., 2000, 2003, 2006; Puntieri et al., 2000; Isik et al., 2001).
Branching process
Although the architecture of some vascular plants consists only of a single vegetative axis during their whole life span, most display a more complex architecture consisting of several axes, one derived from another by a repetitive process known as branching.
Terminal vs. lateral branching
An apical meristem (McManus and Veit, 2002) or an initial apical cell (Gifford, 1983) can directly split and give rise to two or more new sibling axes, which results in dichotomy or polytomy, respectively (Emberger, 1960). Frequently encountered in ferns and mosses (Emberger, 1960), this terminal branching (Gatin, 1924) is rarely expressed in angiosperms (see for monocotyledons: Schoute, 1909; Tomlinson, 1971; Fisher, 1976; Tomlinson and Posluszny, 1977; and for dicotyledons: Nolan, 1969; Boke, 1976; Iwamoto et al., 2005). It is important to mention that this phenomenon is, as far as we know, not encountered within gymnosperms.
In other cases, the branching process relies on the delimitation of a zone of embryonic cells just aside the initiated leaf, i.e. the axillary meristem. This lateral branching process is the most common one among angiosperms and gymnosperms. The resulting lateral branch is characterized by the presence of one or two (in respectively monocotyledons or dicotyledons) prophylls: the first foliar organs of the lateral axis (see Fig. 7A, B for their particular location).
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and prophyll ß are mainly in opposite and lateral position with respect to the plan formed by the axillary leaf (L) and the parent axis (P) (Salvia guaranitica, A). In monocotyledons, the first leaf (prophyll In some plants, there are, at a single leaf axil, more than one axillary meristem, which are then called supernumerary or accessory buds (Sandt, 1925; Troll, 1937; Espagnac and Neuville, 1969; Altman and Goren, 1978; Bell, 1991; Fig. 8A, B). In this case, each individual lateral meristem may be identified by the position of its prophylls, which also allows the distinction between this situation and the development of condensed and more complex lateral branching systems (i.e. complexes of secondary buds, Hallé et al., 1978), where second-order lateral buds may be present in the axils of main lateral bud's prophylls (Fig. 8C).
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Immediate vs. delayed branching (Fig. 9)
Once initiated, an axillary meristem may remain dormant or can develop into a lateral axis. A lateral axis may elongate immediately after lateral meristem initiation or after a phase during which the lateral meristem remains inactive and very often protected in a lateral bud. These branching patterns are referred to, respectively, as immediate (i.e. ‘sylleptic’ sensu Hallé et al., 1978; Müller-Doblies and Weberling, 1984; Wu and Hinckley, 2001) or delayed (‘proleptic’ sensu Hallé et al., 1978; ‘prolepsis’, Bell, 1991) branching. The terms immediate vs delayed branching should be preferred to the more traditional ‘sylleptic’ vs. ‘proleptic’ branching (sensu Hallé et al., 1978) because of etymological and historical reasons, which have rendered the latter two terms ambiguous (see Caraglio and Barthélémy, 1997, for a critical review).
Morphologically, these two branching patterns may generally be identified a posteriori by the observation of the base of the lateral axis. Because of the immediate extension of lateral organs, branches with immediate development generally lack proximal cataphylls and present a relatively long most proximal internode termed a hypopodium (Fig. 9A; Tomlinson and Gill, 1973). Irrespective of the delay length, delayed branches present very short internodes and one or several cataphylls in their proximal portion, close to the point of insertion (Fig. 9B; Hallé et al., 1978). Thorough observation of the proximal part of lateral axes and a periodic observation and measurement of lateral meristem or bud size normally leaves no doubt as to the immediate or delayed nature of branching. In some cases, however, because lateral resting buds may be ‘hidden’, during the resting phase, in the axils of persistent basal foliar organs of the terminal bud (Guédès, 1975, 1980) or because lateral axes in an embryonic stage may already exist inside a resting bud (Champagnat, 1965; Roloff, 1985), the interpretation may be complicated or may lead to a misuse of the terminology (Caraglio and Barthélémy, 1997). Finally, in delayed branching it has been shown that the duration of the delay may be of several weeks to a year (Sabatier et al., 1995, 1998, 2003b; Puntieri et al., 1998; Heuret et al., 2003) and even several years (Fink, 1983; Nicolini et al., 2001).
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Monopodial vs. sympodial branching
Depending on the indeterminate or determinate growth pattern of an axis, its branching pattern may respectively be monopodial (Emberger, 1960; or ‘monopodic’, Sachs, 1874), or sympodial (Emberger, 1960; or ‘sympodic’, Sachs, 1874). In the latter case, one, two or more branches may develop after the death, abscission, abortion or transformation of the apex, and the resulting sympodial branching pattern be qualified respectively as mono-, di- or polychasial. In plant architecture, the concept of module (‘article’ in French) was defined for the first time by Prévost (1967) in her study of tropical Apocynaceae and then applied to ‘a leafy axis in which the entire sequence of differentiation is carried out from the initiation of the meristem that builds up the axis to the sexual differentiation of its apex’ (Hallé, 1986). Because of the various causes of determinate growth (see above), this definition is, however, restrictive and the term ‘module’ increasingly refers to the portion of an axis edified by a single terminal meristem, which corresponds also to a ‘sympodial unit’ as used by Bell (1991).
Involving one or more lateral axes, a sympodial branching system is very often three dimensional. In some cases, however, a sympode may imply a linear succession of ‘modules’ or ‘sympodial units’ forming a so-called ‘pseudomonopodium’ as termed by German mophologists (Troll, 1937; Rauh, 1939). The resulting rectilinear structure mimics an axis edified by a single meristem with indeterminate growth and, if reproduced on all axes, may give rise to a totally sympodial branching system that resembles a monopodial one (Caraglio and Edelin, 1990; Bell, 1991). As a consequence, a rectilinear stem may thus be composed of a succession of metamers or growth units or annual shoots all produced by a single meristem or by a linear succession of sympodial units or modules. In a broader sense and following Room et al. (1994), the term ‘leafy axis’ or ‘axis’ will identify not only a structure edified by a single meristem as initially considered by Hallé et al. (1978) but also a rectilinear stem, whatever its intrinsic mode of construction.
Branched system and branching order (Fig. 10)
The description of a branched system implies the use of a precise topological terminology. In plant architecture analysis it is usual to use ordinal numbers and to consider the main stem arising from seed as the order 1 axis (Fig. 10A; Hallé et al., 1978; Barthélémy et al., 1989, 1991) whereas the axes it gives rise to are referred to order 2 axes and so on. In a sympodial system, a rigorous use of this terminology will lead to the reference of the successive sympodial units as axis orders 1, 2, 3, etc. In order to be coherent with our broad axis definition (see above), each rectilinear succession of modules, even though not strictly edified by a single meristem, will be considered as an axis and will represent an ‘apparent branching order’ (Fig. 10A, C).
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Rhythmic vs. continuous or diffuse branching
Defined and used for the first time for plant architecture description, these terms contribute to the characterization and definition of architectural models (Hallé and Oldeman, 1970; Hallé et al., 1978) and take into account the topological distribution of sibling axes on a parent axis. Depending on whether all the axillary meristems of a stem develop into lateral axes, or whether lateral axes are grouped as distinct tiers with an obvious regular alternation of a succession of unbranched and branched nodes on the parent stem, branching is respectively referred to as continuous or rhythmic. In some cases, neither all nodes of a parent axis are associated with a lateral axis nor is there an obvious regular distribution of branches in tiers, and the branching pattern is then called ‘diffuse’. As revealed in Cupressaceae by qualitative observations (Courtot and Baillaud, 1961; Baillaud, 1999) and, in recent years by sophisticated mathematical methods (Guédon et al., 2001; Grosfeld, 2002; Heuret et al., 2002), a diffuse branching pattern may not mean an unorganized distribution of sibling shoots on a parent shoot but may indicate a predictable, precise and subtle branching organization.
Acrotonic vs. mesotonic or basitonic branching (Fig. 11)
In order to describe the positional preferential development of lateral axes on a vertical parent axis or shoot, Troll (1937) and Rauh (1939) distinguished three modalities that were grouped under the German expression ‘longitudinale Symmetrie’. Acrotony (Fig. 11A, B) is the prevalent development of lateral axes in the distal part of a parent axis or shoot, and depending on whether branching is monopodial or sympodial, Rauh (1939) and Champagnat (1947) termed it, respectively, ‘primary’ or ‘secondary’ acrotony. In the initial definition of acrotony, the parent axis was always longer than the sibling ones, but Bell (1991) used the term ‘acrotonic branching’ for the distal position of the largest lateral branch, independent of its size relative to parent stem. Basitony (Fig. 12) was at first (Troll, 1937) considered as the preferential development of lateral axes in the basal part of a vertical stem. Bell (1991) used the term ‘basitonic branching’ when the proximal branches grow larger than the distal ones. Finally, mesotony (Fig. 11C, D) is used for a privileged development of branches in the median part of a shoot or axis.
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Clearly included in the definition (Bell, 1991) or implicitly shown in the illustrations (Troll, 1937; Rauh, 1939), the topological lateral arrangement of branches along the parent axis is often associated with an increasing or decreasing gradient in length and/or vigour of the branches. As discussed by Caraglio and Barthélémy (1997), these two points must nevertheless be considered separately as the diversity of their expression in plants shows that there is neither automatic nor direct correlation between the privileged position and the relative vigour of lateral branches (compare Fig. 11A with Fig. 11B, or Fig. 11C with Fig. 11D). As all kinds of combinations may be found in the plant kingdom, we would prefer the terms acrotony, basitony and mesotony to be used only in reference to the privileged localization of branches on a parent shoot (respectively distal part, proximal part and median position) without reference to their relative vigour or length, which can be given in precise terms in addition.
Acrotony or basitony are frequently considered as two fundamental phenomena underlying, respectively, the ‘arborescent’ or ‘bushy’ growth habit (Troll, 1937; Rauh, 1939; Champagnat, 1947; Barnola and Crabbé, 1991). Nevertheless these authors refer mainly to the acrotonic branching of growth units or annual shoots in the arborescent case whereas they consider the proximal branching at the base of the whole individual when considering bushy plants. As discussed by Caraglio and Barthélémy (1997) either acrotonic or basitonic branching may characterize the growth units or shoots of either tree or bush, whereas basal sprouts may also be an adaptative strategy of some trees (Fig. 12). Therefore, these terms should be used only at the growth unit annual shoot or axis levels or, at least, the plant level of organization under consideration must be specified when using these terms.
Hypotony, epitony and amphitony (Fig. 13)
In order to describe the privileged arrangement of lateral axes on a horizontal, curved or slanted parent axis, Troll (1937) defined three modalities of so-called ‘laterale Symmetrie’.
According to this terminology the privileged development of branches on the upper, lateral or basal position of a parent axis is referred to, respectively, as epitony, amphitony or hypotony. Epitony is a very common process in many fruit trees (Costes et al., 2006) and in plants belonging to such architectural models as those of Champagnat, Troll or Mangenot (Hallé et al., 1978); it is also often associated with the survival of old branches in the canopy of old trees (Fig. 13C). Hypotony (Fig. 13A) is frequently marked by a privileged development of lateral axes in the curvature zone of a slanted branch whereas amphitony (Fig. 13B) is frequent on rectilinear horizontal or slightly slanted branches. Hypotony and amphitony may be combined in slanted and curved branches and their incidence in the expansion of lateral branch complexes is of the utmost importance in the crown architecture of many woody plants. Finally, it is noticeable that amphitony is a frequent feature in rectilinear branches whereas epitony and hypotony are characterized by the predominant development of lateral axes on the convex side of the curved, downwardly or upwardly orientated branches (Caraglio and Barthélémy, 1997; and compare Fig. 13A, B and C). As highly influenced by axis orientation, these phenomena are frequently combined with the previously described topological arrangement along axes (acrotony, basitony, mesotony) and these combinations have considerable relevance to bud fate according to their topological position and space orientation within a plant crown.
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Morphological differentiation of axes
The general orientation of a leafy axis and the spatial disposition of its leaves are of major importance in the growth strategy of a plant. Within a single plant, some of these axes are essential in plant skeleton edification; some are aerials whereas others may grow underground; some are involved in space exploration whereas others are more related to reproductive dissemination activities or in environment exploitation via photosynthesis. This axis polymorphism is frequent in plants and represents a true morphological differentiation related to meristem expression and activity (Hallé and Oldeman, 1970).
Orthotropy, plagiotropy and mixed axes (Fig. 14)
On most plants and more evidently in trees, two major types of axes may be distinguished according to their erect or horizontal general orientation. Orthotropy (Fig. 14A; Frank, 1868; Koriba, 1958) refers to axes whose general orientation is vertical and whose symmetry is radial, with leaves in a spiral, opposite or verticillate disposition, and associated lateral branches arranged in all spatial directions. Plagiotropic axes (Fig. 14B; Frank, 1868; Koriba, 1958) have a general horizontal to slanted orientation and a bilateral symmetry owing to leaves (distichous phyllotaxis) and branches being generally arranged in one plane.
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Therefore, both kinds of axes are defined not just by their orientation but rather by a set or ‘syndrome’ of features (Edelin, 1984). In addition, some axes may have intermediate features and/or secondary orientation of axes may sometimes occur thus complicating their exact characterization. In many plants, a single meristem may give rise to an axis with mixed properties. Sometimes an axis may have an orthotropic proximal portion and a plagiotropic distal end; the superposition of such ‘mixed axes’ is a distinctive feature of the trunk edification in some plants (Mangenot's architectural model for instance; Hallé and Oldeman, 1970). Other mixed axes may present the reverse configuration, i.e. a proximal plagiotropic portion followed by a distal orthotropic end. In such cases, the modules are formed by successive hypotonic branching, giving rise to horizontal branched systems named plagiotropy by apposition (Fig. 14C; Hallé et al., 1978; apposing growth of Koriba, 1958; apposition growth of Roux, 1968) or plagiotropy by substitution (Fig. 14D; Hallé et al., 1978; substituting growth of Koriba, 1958) depending on whether modules are of, respectively, indeterminate or determinate growth.
For a given species, all axes may be of the same kind or several axis types may coexist on the same individual. Different axis types may even coexist at the same foliar axil. On the main stem of Coffea trees for instance, the more distal axillary meristem develops in an immediate plagiotropic branch whereas a more proximal reserve (supernumerary) bud (Varossieau, 1940; Moens, 1963) in the same leaf axil may develop as a delayed orthotropic axis. The coexistence of buds with different fates on the same node leads to many questions regarding the physiological control and genetic determinism of plagiotropy (Tomlinson, 1986, 1987) and more generally branching differentiation.
Short vs. long axes (Fig. 15)
In the vegetative aerial part of most woody plants, orthotropy is generally associated with plant skeleton construction and the colonization or exploration of the vertical space, whereas plagiotropy is generally more concerned with exploration and exploitation of the horizontal space and reproductive functions (photosynthesis, flowering).
In many cases, axis differentiation is also related to axis size and very often long and short axes, respectively, specialized in environmental exploration and exploitation (Fig. 15A and B) may be identified in a plant species (Champagnat, 1965; Rivals, 1965, 1966; Kozlowski, 1971; Zimmerman and Brown, 1971). Here again the differentiation of axes and bud fate may be highly specialized and very different structures (i.e. flowers, inflorescences, spines, long axis, etc.) may be found in a single leaf axil and in a precise position, as is the case in several species (see Fig. 15C). In all these cases, however, differentiation of an axis may not be an irreversible process, and according to modifications of internal or external conditions or after architectural traumatism, reversion of axis differentiation is very often possible (see Fig. 15D–F), indicating that shoot differentiation and bud fate are controlled by a whole plant network of correlations (Champagnat, 1961; Nozeran et al., 1984; Greenwood, 1987, 1995) and environmental conditions.
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Position (terminal vs. lateral) of sexuality and reproductive organs
As architectural studies have historically focused mainly on the vegetative structure of the plant body, reproductive structures are considered as a whole and according to the impact they have on plant growth and branching. Because of their incidence on growth and branching, the lateral or terminal position of reproductive structures will be considered, i.e. whether they result from the transformation of a lateral or terminal meristem, respectively. Readers seeking more precise terminology and descriptions of the structure of reproductive organs or inflorescences in angiosperms should refer to more general (Bell, 1991) or dedicated synthetic works dealing with inflorescence typology or shoot typology according to the arrangement of reproductive or floral elements (Parkin, 1914; Pilger, 1921; Troll, 1957; Briggs and Johnson, 1979; Müller-Doblies and Weberling, 1984; Weberling, 1989; Claßen-Bockhoff, 2000, 2005).
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THE CONCEPT OF ARCHITECTURAL MODEL |
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For a tree species the growth pattern which determines the successive architectural phases is called its architectural model, or shorter, its model (Hallé and Oldeman, 1970). The architectural model is an inherent growth strategy that defines both the manner in which the plant elaborates its form and the resulting architecture. It expresses the nature and the sequence of activity of the endogenous morphogenetic processes of the organism, and corresponds to the fundamental growth programme on which the entire architecture is established. The identification of the architectural model of any given plant is based on the observation of the features belonging to the four major groups of simple morphological features presented above: (1) the growth pattern, i.e. determinate vs. indeterminate growth and rhythmic vs. continuous growth; (2) the branching pattern, i.e. terminal vs. lateral branching vs. no branching, monopodial vs. sympodial branching, rhythmic vs. continuous vs. diffuse branching, immediate vs. delayed branching; (3) the morphological differentiation of axes, i.e. orthotropic vs. plagiotropic vs. axes with mixed morphological and/or geometrical features (with plagiotropic and orthotropic portions); and (4) lateral vs. terminal flowering.
Each architectural model is defined by a particular combination of these simple morphological features and named after a well-known botanist (Fig. 16). Although the number of these combinations is theoretically very high, there are apparently only 23 architectural models found in nature. Each of these models applies equally to arborescent or herbaceous plants, from tropical or temperate regions, and which can belong to closely related or distant taxa.
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The reader will find detailed information on each architectural model in Hallé and Oldeman (1970) and Hallé et al. (1978).
Growth patterns defined by the architectural models are genetically determined. Only under extreme ecological conditions is their expression affected by the environment (Hallé, 1978; Barthélémy, 1986; Barthélémy et al., 1995, 1997b, 1999; Grosfeld et al., 1999; Grosfeld, 2002; Stecconi, 2006). Different models can be represented by plants belonging to closely related species (Edelin, 1977; Temple, 1977; Edelin and Hallé, 1985; Vester, 1999; Hallé, 2004). Architectural analysis also shows that some plants frequently exhibit morphological features that are apparently related to two or three models (Hallé and Ng, 1981; Edelin, 1977, 1984; Veillon, 1978, 1980; Grosfeld et al., 1999). These intermediate forms indicate that there is no real disjunction between the models. On the contrary, it must be considered that all architectures are theoretically possible and that there could be a gradual transition from one to another. Among this ‘architectural continuum’ (Edelin, 1977, 1981; Hallé et al., 1978), the models themselves represent the forms that are the most stable and the most frequent, i.e. the most probable biologically. As an architectural model is defined by few and simple morphological features, it gives only an idea of the elementary developmental pattern of a species. Nonetheless, this level of representation of the plant could be well adapted to describe the evolutionary pattern or phylogenetic or taxonomic distribution of plant architecture (Johnson, 2003; Hallé, 2004) and may help to unravel the ecological importance of these patterns (Foresta, 1983; Vester, 1997, 1999).
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THE ARCHITECTURAL UNIT |
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The architectural model represents the basic growth strategy of a plant, and this concept has allowed the definition of a typology of main plant growth strategies. Nevertheless, the characters used in its identification are far too general to describe the complete and precise architecture of a plant. For any given plant, the specific expression of its model has been called its ‘architectural unit’ (Barthélémy et al., 1989, 1991; origi