Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny

Abstract

Background 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.

Fig. 1.

Shoot apex (A) and stem (B) organization. Each leafy axis (B) ends in an apical meristem frequently protected in an apical bud (A). Each stem comprises a succession of metamers, i.e. the set composed by (1) one internode, (2) the node (i.e. insertion point of the leaves on a stem) located at its tip and (3) the corresponding one or several leaves and associated lateral buds (in grey on A; White, 1979; Caraglio and Barthélémy, 1997).

Fig. 2.

Determinate growth corresponds to an irreversible transformation of the apical meristem, which can be due to (A) apical flowering as in Nerium oleander, (B) parenchymatization (arrow) of the apical meristem as in Alstonia sp. or (C) apical death or abscission (‘X’) as in Castanea sativa. Indeterminate growth corresponds to permanent apical meristem functioning, as illustrated by the main stem of Picea excelsa (D).

Fig. 3.

Leaf extension rate in continuous (A and B) vs. rhythmic (C) growth and structure of the resulting stems (modified from Hallé et al., 1978). (A) Constant leaf extension in a theoretical case (i.e. several palm trees) and (B) fluctuations in the leaf extension rate of Rhizophora mangle correlated with climatic fluctuations. (C) Rhythmic cumulative rate of leaf extension in Hevea brasiliensis. G.U., growth unit; f, leaf; ca, cataphyll.

Fig. 4.

Morphological markers of rhythmic extension. Growth cessation phases (arrows) and delimitation of successive growth units (G.U.) as revealed a posteriori by an alternation of cataphylls (ca) and photosynthetic leaves (f) in Protea cynaroïdes (A) or their scars (Carya laciniosa, B, or Cycas pectinata, C).

Fig. 5.

Successive growth units may be delimited (arrows) only by more or less marked changes in leaf size (Virola michelii, A; Virola surinamensis, B; drawings from Edelin, 1993). In some cases the limit (arrow) between two growth units is indicated by a decrease in the pith diameter (Carapa procera, C; drawings from Edelin, 1993) and/or even by pith structure as in Juglans sp. (D). G.U., growth unit; ‘n’, ‘n + 1’, successive theoretical years of growth; p, plain pith; s, septate pith.

Fig. 6.

Stem extension may occur more than once during a same calendar year. The set of growth units produced in one year is then called an annual shoot (A.S.). In Quercus ilex (A) or Pinus halepensis (B) bicyclic shoots, the first growth unit (G.U.1) may produce reproductive organs whereas the second (G.U.2) is vegetative. On old stems, the presence of female cones or fruits on the first growth unit and the major development of branches borne on the second growth unit of such bicyclic annual shoots distinguishes these first and second growth units, respectively, as the a posteriori delimitation of successive annual shoots (B). ‘n-1’, ‘n’, ‘n + 1’, successive theoretical years of growth; solid white arrow, limit of an annual shoot; dashed white arrow, limit of a growth unit.

Fig. 7.

The leaf, or leaves, of the first (proximal) node of a lateral shoot (A) are referred to as prophylls. In dicotyledons prophyll α and prophyll β 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 α) is often bicarinate and shows a particular arrangement (unidentified Poaceae, B): it is located in adaxial position between the lateral shoot (A) and its parent axis (P).

Fig. 8.

Vertical succession of supernumerary (or accessory) buds in Juglans regia (A) and in Forsythia vulgaris (B). The arrangement of the prophylls (diagrams) distinguishes supernumerary buds from reduced branching systems as illustrated in Zelkova serrata (C). L, axillary leaf; Ls, leaf scar; P, parent axis; prophylls α and β or their scars, αs and βs, after abscission.

Fig. 9.

In the case of immediate branching (Juglans regia, A), the first internode is generally long and termed the hypopodium (h). Delayed branching refers to a system where lateral branching follows a resting phase of the lateral meristem during which it is frequently included in a bud. When elongated, such delayed branching lateral shoots frequently show a short first internode and proximal scale leaves or bud scale scars when abscissed (Platanus sp., B). x, apical mortality; α, prophyll alpha; αs, scar of abscissed prophyll alpha.

Fig. 10.

As a result of branching, sibling axes succeed topologically from a parent axis. This spatial succession is referred to as ‘branching order’ (BO). The first axis (branching order one, BO1) bears a lateral one (branching order 2, BO2) and so on as illustrated diagrammatically for a monopodial branching system (A). In a sympodial branching system, the branching order may increase rapidly (C). When successive sympodial units (each resulting from the functioning of a single meristem) are more or less in a rectilinear disposition (B), it can be considered that the general spatial direction of such a succession constitutes an ‘apparent branching order’ (AO) as in a monopodial system (pseudomonopodium sensu Troll, 1937). x, apical mortality; AOx, ‘apparent branching order’ number x.

Fig. 11.

Privileged repartition of sibling shoots on a vertical parent shoot or axis. Acrotony is the preferred development of lateral axes in the distal part of a parent axis or shoot (A and B). The topological lateral arrangement of branches along the parent axis may be associated with an increasing (Abies sp., A) or decreasing (Juglans nigra, B) gradient in length and/or vigour of the branches. Mesotony refers to a privileged development of branches in the median part of a shoot or axis. The topological lateral arrangement of branches along the parent axis may be associated with a distal to proximal increasing and then decreasing (Cedrus atlantica, C) or a decreasing (Alnus glutinosa, D) gradient in length and/or vigour of the branches. White arrows indicate the increasing gradient in length of branches. On the diagrams, the break represents the limit of an annual shoot.

Fig. 12.

Privileged repartition of sibling shoots on a vertical parent shoot or axis. Basitony is the privileged development of lateral axes in the basal part of a vertical stem or shoot. This may involve the whole plant level as for the shrubby plant Stenocereus thurberi (A) or the growth unit level only (Choysia ternatea, B). White arrow, limit of a growth unit. On the diagrams, the break is the limit of a growth unit.

Fig. 13.

Privileged repartition of sibling shoots on a slanted or horizontal parent shoot or axis. Hypotony refers to the privileged development of branches on a basal position on a parent axis (Opuntia fulgida, A). Mesotony refers to the privileged development of branches on a lateral position on a parent axis (branches of Abies sp. from above, B). Epitony refers to the privileged development of branches on upper positions on a parent axis (Juglans nigra, C). P, parent axis; M, privileged lateral branch.

Fig. 14.

Orthotropic axes are generally erect to vertical with a radial symmetry, bear large leaves and long lateral axes (Fraxinus oxyphylla, A). By contrast, horizontal axes tend to exhibit a bilateral symmetry frequently associated with a high reproductive and photosynthetic strategy: they represent plagiotropic axes (Azara microphylla, B). Particular kinds of plagiotropic axes correspond to an immediate hypotonic sympodial branching system of successive indeterminate (plagiotropy by apposition: unidentified Sapotaceae, C) or determinate (plagiotropy by substitution: Byrsonima densa, D) sympodial units.

Fig. 15.

Short shoots are characterized by short internodes and successive growth units (Prunus avium, A). They are frequently associated with lateral (A) or terminal (Cedrus atlantica, B) reproductive organs. Short shoot type may be linked to position in the leaf axil in the case of supernumerary buds (Gleditsia triacanthos, C). In some conditions a short shoot can dedifferentiate into a long shoot (Larix decidua, D; Malus domestica, E). Even the very specialized brachyblast of Pinus species (P. nigra, F) may transform into a long shoot after stem traumatism (white cross). White arrows indicate the transition between two successive growth units.

Fig. 16.

Some architectural models. Corner's model (A) concerns unbranched plants with lateral inflorescences. Leeuwenberg's model (B) consists of a sympodial succession of equivalent sympodial units, each of which is orthotropic and determinate in its growth. Rauh's model (C) is represented by numerous woody plants where growth and branching are rhythmic, all axes are monopodial and sexuality is lateral. Illustrations after Hallé and Oldeman (1970), Hallé et al. (1978) and Barthélémy (1991).

Fig. 17.

The architectural unit of Cedrus atlantica (Pinaceae) is composed of five axis categories (A1 to A5). (A) Diagrammatic representation of the tree (view in elevation) representing the relative position of main axis categories; (B) diagrammatic representation of a tier of branches (view from above); (C): diagram of a twig annual shoot bearing several short shoots. The break symbol indicates the limit between two successive annual shoots (from Sabatier and Barthélémy, 1999). The table summarizes the morphological features of all axis categories.

Fig. 18.

Category of axis vs. branching order. The relative arrangement of categories of axes (T, trunk; B, branch; S, short shoot) may (A, i.e. Araucaria araucana) or may not (B and C) be superposed to the notion of branching order, in either monopodial (B, i.e. Acer sp.) or sympodial (C, i.e. Platanus sp.; Caraglio and Edelin, 1990) branching pattern. x, apical mortality; BOn, branching order n; AOn, apparent branching order n.

Fig. 19.

Each category of axis (trunk, T; branch, B) results from the succession of shoots in a monopodial system (A, Acer sp., redrawn from Troll, 1937) or the succession of modules in sympodial trees (B, Ulmus sp., redrawn from Troll, 1937; dotted lines represent self shed branches; x, apical mortality) or herbs (C, Encyclia vespa, from Barthélémy, 1988; dotted sympodial units represent those that are naturally shed for the developmental stage diagrammatically represented).

Fig. 20.

Variation in crown physiognomy and architecture in relation to environmental conditions at the time of architectural unit expression in Araucaria araucana. (A) In forest stands, the mature tree expressing its architectural unit has a 15–20-m-high trunk which bears at its top a large conical crown composed of up to 20 tiers of living branches. (B) In full sun and with favourable soil and precipitation conditions, the tree has, at first cone production, a typical pyramidal crown. The trunk is 6–8 m high and most branches are alive. (C) In full sun and poor soil and precipitation conditions, the first production of cones may occur in a tree no more than 4 m high. The crown has a typical ‘umbrella form’ and most of the branches are alive (Grosfeld et al., 1999). Black arrows indicate terminal female cones.

Fig. 21.

Architectural types of Cupressus sempervirens observed in ‘fastigiated’ (A), ‘intermediate’ (B and C) and ‘horizontal’ (D) crown shape groups (from Barthélémy et al.,1999). Distinctive features of these architectural types are: the length of branches (compare A left and D), their straightness (A and B left) or straightening up (A and B right), their initial insertion angle (differences between D left and D right), homogeneity (A, B and D) or heterogeneity (C) of branch types within a single individual, the occurrence and importance of the reiteration process (A right and C). Black arrows indicate reiterated complexes.

Fig. 22.

Architectural sequence of development in Araucaria araucana (from Grosfeld, 2002). In this temperate South American species, the plant expresses step by step (A–D) its architectural unit composed of three axis categories (D). The following stages of development (E and F) are only marked by quantitative modifications, and the tree remains conform to its architectural unit, without any reiteration, up to the end of its life.

Fig. 23.

Opportunistic reiteration and structure of the reiterated complexes. (A) Opportunistic, ‘partial’ (P.R.) and ‘complete’ (C.R.) reiteration in an individual of Araucaria araucana (Araucariaceae; from Grosfeld et al., 1999). Diagrammatic representation of reiterated complexes (in black) according to their location on the tree in (B) Symphonia globulifera (from Barthélémy, 1988) and in (C) Isertia coccinea (from Barthélémy, 1988). All complete reiterated complexes result from the development of a previously dormant bud (delayed reiteration). They all duplicate the original sequence of differentiation of the original individual but the duplication is smaller and more ‘pauperized’ according to their insertion from the base of the trunk to the ‘periphery’ of the crown. At the top of the tree and in the most peripheral part of the crown, pauperization of the duplication is the highest and reiterated complexes all have a reduced and minimal specific structure (in the case of Symphonia globulifera, a small trunk bearing only one flowering tier of plagiotropic branches, and in the case of Isertia coccinea, a succession of small sympodial units only branched below the terminal inflorescence) named ‘Minimal Architectural Unit’ (M.A.U.) by Barthélémy (1988). (D) Opportunistic, ‘complete’ (C.R.) reiteration (dotted units) in old parts of a traumatically cut (x) sympodial herb (Encyclia vespa, Orchidaceae, from Barthélémy, 1988). Double arrows, roots.

Fig. 24.

(A) Total immediate reiteration (S.R.) expressed on the distal part of a branch of Araucaria araucana. (B) Successive immediate and partial reiterated complexes on a branch of Austrocedrus chilensis (from Grosfeld, 2002). A1, main stem; A'2, first order of reiteration of A2 category of axis; A''2, second order of reiteration.

Fig. 25.

(A) Damaged tree crown of an unidentified tropical tree comprising a part of the initial crown (C) and a set of reiterated complexes (C.R.) on the broken part (x). (B) Adaptive reiterated complexes (C.R.) can occur following local structural changes in the crown of an individual of Fraxinus excelsior (Barthélémy et al.,1997a) as caused by traumatism along the main stem (x); compare with Fig. 26.

Fig. 26.

Diagrammatic representation of the architectural sequence of development in Fraxinus excelsior (from Barthélémy et al.,1997a; highest category axes are not represented). The young plant expresses step by step (A and B) its architectural unit (in B) and then duplicates it automatically in the following stages of development (C and D) finally to give rise to a complex mature crown made of a succession of reiterated complexes (D).

Fig. 27.

Sequential (‘automatic’) reiteration and gradual trends in architectural, morphological and anatomical features according to stages of development. (A) Trends in leaf size and form for the main axis during the ontogeny of Artocarpus elasticus (from Edelin, 1984). (B) From left to right: trends in stem and leaf anatomy, in leaf and short shoot size and structure, in a main stem branching complexity (branching grade) and size (length of the latest G.U. in black and position of short shoots in dark grey on maximum expanded branching system in grey) and in architecture according to successive stages of development in Fagus sylvatica (after Nicolini, 1997; Nicolini and Chanson, 1999).

Fig. 28.

Diagrammatic representation of main levels of organization (construction units) and repetition phenomena (in italics or terms in boxes) in seed plants (synthesis from Barthélémy, 1991; Barthélémy et al.,1997a; Caraglio and Barthélémy, 1997). x, apical mortality.

Fig. 29.

Differentiation processes and levels of organization in seed plants. (A) Coordinate and related trends in leaf and internode structure and in size and nature of foliar axil products along the unique axis of a herbaceous tropical plant native to French Guyana: Noisettia longifolia (after Barthélémy, 1988). (B and C) Differentiation at the level of the growth unit (G.U.) and annual bicyclic shoot in the Mediterranean trees Pinus halepensis (B) and Quercus ilex (C, after Caraglio and Barthélémy, 1997, see also Fig. 6). In both cases, differentiation at the level of each growth unit is marked by the nature of foliar organs (cataphylls vs. photosynthetic leaves) or axillary products (dormant bud vs. lateral shoot or vs. reproductive organs) for G.U.1. For both species, at the bicyclic annual shoot level, differentiation between the two successive G.U.s (i.e. G.U.1 vs. G.U.2) is revealed by the presence of reproductive structures and lateral shoots on G.U.1 only and by differences in leaf size and structure according to their bearing G.U., i.e. G.U.1 vs. G.U.2. (D) Differentiation at the comprehensive level of the whole ontogeny of a plant is illustrated in the case of common walnut (Juglans regia, after Sabatier, 1999) by the architectural trend from young to mature tree (left to right) and by the associated annual shoot structure trends (diagrammatically represented here at each stage for the main stem and some lateral branches). Break symbol (=), winter growth stop; – or ∼, intra-annual growth stop or decrease in growth speed; o, terminal female flower.

Fig. 30.

Morphogenetic gradients and physiological age of meristems (after Barthélémy et al.,1997a). Theoretical and diagrammatic representation of the distribution of elementary botanical entities with similar characteristics (i.e. presenting the same ‘physiological age’ and represented by the same size and colour rectangle on the diagram) according to some main morphogenetic gradients very commonly observed in seed plants: for the initial structure and reiterated complexes four ‘branching orders’ (BO1–BO4), BO1 representing the main axis; ‘base effect’ is a gradient linked to the ‘establishment growth phase’ of any plant grown from seed; ‘acrotony’, with increasing acropetal gradient of vigour of lateral axes, is a common feature of the annual shoots and growth units of most rhythmically growing trees; ‘drift’ is a general feature linked with axis ageing; sequential ‘reiteration’, in this case, represented by the automatic duplication of the sequence of development and associated gradients of the main axis by another axis.

Fig. 31.

(A) Shape and size of successive leaves along a stem of a herbaceous Senecio sp. (redrawn from Baillaud and Courtot, 1955). (B) Organization of the two last successive annual shoots of the main stem of Cedrus atlantica during its life and (C) the corresponding global tree structure (from Sabatier and Barthélémy, 1995).

Fig. 32.

Diagrammatic representation of trends in the value of some morphological parameters according to annual shoot rank of successive annual shoots of branches borne on the same ontogenetical age parent shoots of the main stem of a set of 22-year-old dominant to co-dominant Pinus pinaster individuals grown on a same stand in the south-west of France (unpublished data; Coudurier et al., 1995; Heuret et al., 2006), where a is the mean annual shoot length (in percentage of maximum length), b is the percentage of polycyclic shoots, c is the percentage of branched shoots, and d is the percentage of shoots with male cones. For each shoot rank the particular combination of the value of the morphological parameters allows a strict characterization of the physiological age of meristem activity that produced it.

Fig. 33.

Diagrammatic representation of a theoretical plant whose elementary botanical entities produced by the meristems (for instance annual shoots, represented by rectangles) may encompass four different physiological ages (a–d). The ‘plant’ grows from seed in four steps (possible ontogenetic ages 1–4), each step corresponding to one year of growth (n – 3 to n). It is hypothetically represented as growing in ‘good’ environmental conditions (where the main stem expresses the four possible physiological ages successively and in relation to successive four ontogenetic ages and where branches fully express morphogenetic gradients as shown in Fig. 30: case ‘A’), or in suppressed condition (as for the growth of Araucaria araucana in Fig. 20; case ‘B’). Each entity is characterized by a trinom – where the first element represents ontogenetic age (1–4), the second element represents calendar age (n – 3 to n) and the third element represents physiological age (a–d) – that allows us to understand the structure of each entity in the whole architecture of the plant (represented in A and B 4 years after germination).