Leaf development, metamorphic heteroblasty and heterophylly in Berberis s. l.
Berberis s. l. (including Mahonia and Mahoberberis, Berberidaceae: Ranunculales) consists of approximately 400 species distributed in highland areas of the Americas and Tropical Africa, c. 200 spp. in China and 2 spp. in Europe (Mabberley, 2008). In South America, the genus is an important component of the high mountain flora (Camargo, 1966, 1981, 1983, 1991; Landrum, 1999). In temperate areas, such as northeast North America, New Zealand and the Malvinas Islands, some species of Berberis have become invasive (Ehrenfeld, 1997; Sliander & Klepeis, 1999; McAlpine & Jesson, 2008).
The branching system in Berberis s. str. consists of spiny long shoots and foliose short shoots (Figs. 1 and 2a-j). The common names ("holy thorn"; "una de gato" in Spanish) often refer to the usually dissected spines formed at the nodes of long shoots. The short shoots arise at the axils of bladeless variously dissected spines of the long shoots and have extremely short internodes and foliage leaves with entire, toothed, or spiny margins. That is the reason why some authors (e.g. Ernst, 1964:7)described the leaves of Berberis as "simple usually fascicled in the axil of a simple or branched cauline spine". The inflorescences develop at the apex of short shoots and do not arrest the growth of the long shoots (Fig. 2c, e-g, j). Accordingly, this branch system falls into Corner's architectural model (Halle et al., 1978).
Leaves in Berberidaceae. The family Berberidaceae (Ranunculales) consists of 15 genera and more than 650 species. Leaf morphology in the family is remarkably diverse (Fig. 1; Yischler, 1902; Schmidt, 1928; Troll, 1937-1943, Figs. 1352, 1353). The number of leaves per individual or aerial shoot varies from two (in e.g. Caulophyllum, Leontice, Podophyllum or Ranzania) to numerous (e.g. in Berberis; Fig. 2a-j). Leaves are sessile or subsessile (in most Berberis spp.) to long-petiolate (e.g. in Achlys and Jeffersonia). The lamina can be entire (e.g. the foliage leaves of Berberis s. str.; Fig. 2a-j) to variously compound (e.g. 2-3 pinnately compound in Nandina and odd-pinnately compound in Mahonia; Fig. 1j and 2k) or peltate (e.g. Diphylleia, Dysosma and Podophyllum; Fig. la). The leaf/leaflet lamina ranges from entire to highly dissected and often with spiny margins (e.g. Bongardia and Mahonia). Leaflets can be pulvinate (as in Nandina) or not. The leaf base is sometimes sheathing (e. g. in Leontice and Nandina) and stipulate (e.g. in Gymnospermium, with leaf-like and trifid stipules). However, the presence of stipules in the family has been controversial; for example, Lindley (1831) described the family as lacking stipules; conversely, Troll (1937-1943, his fig. 1640) showed that, at least in Berberis stipules are present in spiny, laminar, and transitional leaves, and Bell (1991, 2008) described the lateral arms of the spines as stipular.
Fossil leaves of Berberis and Mahonia have been described from the Miocene and Oligocene (Ramirez & Cevallos-Ferriz, 2000; Taylor et al., 2009). Ramirez and Cevallos-Ferriz (2000:257) stated that the "lack of detailed information on leaf architecture in Berberidaceae limits the evaluation of the taxonomic relationships that can be suggested between fossil and extant plants". Thus, interpreting leaf characters in a phylogenetic and paleobotanical context is challenging, because these characters greatly vary within most of the genera (Fig. 1).
Leaf variation is remarkable in Berberis s. l. (i. e. including Mahonia and Mahoberberis, with predominantly odd-pinnately compound leaves; Fig. 2), and leaf features have been extensively used in the systematics and family classification (Fedde, 1902; Schneider, 1905, 1908; Ahrendt, 1961; Camargo, 1960, 1966, 1981, 1983, 1991; Landrum, 1999). For example, Scheider (1905), followed by later authors such as Camargo (1960, 1966, 1981, 1983, 1991), divided the genus by the position of the articulation formed at the base of the lamina of the foliage leaves that form the short shoots. The presence of this articulation has led most authors (e.g. Lindley, 1831; Meacham, 1980; Cronquist, 1981; Takhtajan, 1997, among many others) to consider these leaves as unifoliolate.
The homology of both spiny and foliage leaves in Berberis has long been controversial. For example, Lindley (1831:30) stated that "(t)he spines of the common Berberry are a curious state of leaf, in which the parenchyma is displaced, and the ribs have become indurated. They, as well as all the simple leaves of ordinary appearance, are articulated with the petiole, and are therefore compound leaves reduced to a single foliole; whence the supposed genus Mahonia does not differ essentially from Berberis in foliage more than in fructification". Thus, the spines have been interpreted as: (a) as an odd-pinnately compound leaf in which each leaflet is reduced to a spine (Schmidt, 1928); (b) a dual organ in which the central spine would correspond to the lamina, and the lateral ones to the stipules (e.g., Bell, 1991, 2008); (c) as transformed branches in which the lateral spines would represent reduced leaves, and the central spine would represent an unfolded and reduced short shoot (Croizat, 1960); or (d) as outgrowth from single epidermal cells (Harvey-Gibson & Horsman, 1919). On the other hand, each typical foliage leaf along the short shoot (Fig. 2a, b, d-i) was alternatively considered by Ahrendt (1961:5)to correspond to a leaflet of a palmately compound leaf or homologous to each leaflet of a pinnately compound leaf of Mahonia (Fig. 2k). ("The whorl of Berberis leaves may be regarded as a pinnate leaf in which the leaflet internodes of the rachis have been eliminated, thus bringing leaflets, now regarded as simple leaves, into a cluster at the stem node ... Thus, the number of leaves, or the number of leaves and spines taken together, in each whorl at a Berberis stem node corresponds to the number of leaflets in the pinnate leaf of a Mahonia").
Heteroblasty versus Heterophylly. These two developmental processes have been described to occur in a broad spectrum of embryophytes, from bryophytes to many flowering plant families. In general, both processes exhibit changes in leaf morphology; if gradual, it has been described as a heteroblastic series by e.g. Bell (1991). The original definition of these developmental processes by Goebel (1900-1905) has been subject of different interpretations and elaborations (for a detailed review, see Zotz et al., 2011). Usually, heterophylly refers to different leaf forms on the same plant, whereas heteroblasty refers to the development of distinct types of juvenile and adult foliage. Cronk (2009:95) pointed out that heteroblasty is "a particular kind of heterophylly that is plant-age related rather than environmentally related". However, the environmental and the developmental factors can occur simultaneously, thus obscuring whether heterophylly is due to extrinsic or intrinsic factors. For example, in Populus (Salicaceae) heterophylly is plant-age and environmentally related, and "early" and "late" leaves along shoots of the same age can have different morphologies (Curtis & Lersten, 1978).
No clear-cut differences between heterophylly and heteroblasty are mentioned in most of the literature, and these two processes are described interchangeably (see e.g. Jones & Watson, 2001; Bums & Dawson, 2006), whether or not a time-related factor (detected by differences on leaf morphology among shoots of different order of ramification) is taking into account. Thus, gradual changes in leaf shape in species of, for example, the fern genus Matonia (Matoniaceae) are described as heteroblastic (Kato & Setoguchi, 1998) but they occur change along the same axis. Similar examples occur in Begonia (Kunze, 1986; McLellan, 1993) and in climbing plants such as the fern genera Lomagramma, Lygodium, and Teratophyllum, and members of the flowering plant genera Cucurbita (Cucurbitaceae), Ficus (Moraceae), Ipomoea (Convolvulaceae), Nepenthes (Nepenthaceae), Passiflora (Passifloraceae), Triphyophyllum (Dioncophyllaceae), Hoya (Apocynaceae), Marcgravia (Marcgraviaceae), Metrosideros (Myrtaceae), and Piper (Piperaceae), among others (Green et al., 1979; Lee & Richards, 1991; Jones, 1993).
Allsopp (1965) revised the following general traits that might be affected by the occurrence of heteroblasty in cormophytes: (1) changes in leaf morphology (size, shape), vegetative/reproductive phase), anatomy, juvenility, arrested organs, and differential growth; (2) changes in phyllotaxis; (3) changes in stem characteristics; (4) changes in the apical bud; (5) changes in growth habit and in physiological characteristics; and (6) reversion to juvenile forms in adult plants. The most frequent and well documented in the literature are the leaf phyllotaxis, e.g. in Eucalyptus (Myrtaceae) (Goebel, 1900-1905; Cameron, 1970; Wiltshire et al., 1998; Jaya et al., 2010); the dissection and overall shape of the lamina, e.g. from simple to compound in Fraxinus (Oleaceae) and Leea (Vitaceae) (Merrill, 1986; Gerrath & Lacroix, 1997); the leaf anatomy, unifaciality and morphogenesis, as occurs in Hakea (Proteaceae; Goebel, 1900-1905; Groom et al., 1994); and the petiole symmetry and blade: phyllode ratio, as occurs in e.g. the legume Acacia (Brodribb & Hill, 1993; Hansen, 1996; Gardner et al., 2008). Such changes have been considered as responses either to environmental conditions, particularly light or length of day (e.g. Ashby, 1948; Jones, 1995; Day, 1998; but see Gamage & Jesson, 2007), temperature (e.g. Winn, 1996), or seasonality (e.g. Eckenwalder, 1980); or to intrinsic factors, such as hormone gradients (e.g. Minorsky, 2003), fitness of the individual through enhancing photosynthesis and decreasing mechanical leaf damage and water loss (e.g. Winn, 1999; but see Darrow et al., 2002), and phase change from nonreproductive to reproductive stages (e.g. Wiltshire et al., 1998; Diggle, 1999; Jones, 1999; Poethig, 2003; Jaya et al., 2010). The ecophysiological factors associated with heterophylly and heteroblasty have been discussed by Allsopp (1965), Jones (2001), and Zotz et al. (2011), among others.
Based on studies in Syngonium (Araceae), Ray (1987) clearly described the so-called cyclic heterophylly as a differential development on distinct vegetative growth cycles; later, the same author (1990) refined this concept based on the examination of other Araceae, and described it as a "metamorphosis", which clearly differentiates first order from higher orders of development during leaf morphogenesis. It is important to underline that metamorphosis sensu Ray (1990) is fundamentally different from the "idealistic doctrine of metamorphosis" by von Goethe (1790), described especially in his chapter II "Ausbildung der Stengelblatter von Knotten zu Knotten" ("Development of stem leaves from node to node": our translation). The latter author stated his concept on metamorphosis on the basis of a series of expansion and compression processes of laminar organs (from cotyledons through carpels via eophylls, nomophylls, hypsophylls or bracts, sepals, petals, and stamens) along the same axis, which is essentially an anticipation of the concept of heterophylly. Ray's (1990) concept of plant metamorphosis is also different from the "real transformation" of leaves described by Goebel (1900-1905:6), which, according to Foster (1928) involves "the transformation of organ primordia, not mature organs" (Foster, 1928:136); that is, "direct genetic relationships to the foliage leaves on the shoot", a "Differentiation Theory" explained "entirely as an ontogenetic process" (Foster 1928:137). In order to avoid further confusion, we restrict here the concept of heteroblasty to the "metamorphic heteroblasty" sensu Ray (1987, 1990) and Zotz et al. (2011) as ontogenetic changes in leaf form among branches of different orders of ramification; that is, a "programmed ontogenetic change in shoot morphology" as described by Winn (1999:S113).
Heteroblasty versus Heterophylly in Berberidaceae. Although Goebel (1900-1905:429) mentioned that the leaves of the long shoots of Berberis are thorns, and that transitional stages "show that the leaf-lamina becomes gradually more deeply cut at the edge as it diminishes in breadth, whilst several of the marginal teeth, which are fewer in number than appear in the foliage leaves, develop considerably", he did not explicitly point out Berberis as an example of heteroblasty and/or heterophylly. Other Berberidaceae (e.g. Podophyllum peltatum) have been shown to be strongly heteroblastic (Holm, 1899; Jones & Watson, 2001) during the development of the leaf series, which consists of rhizome scales, bud scales, and a single or two foliage leaves in vegetative and reproductive shoots, respectively (Jones, 2001). Thus, our goals in the present paper are to examine the development of both long shoots and short shoots; to investigate the structural homology between the spines, the cataphylls, the simple leaves, and the pinnately-compound leaves present in Berberis s. l.; and to identify whether the observed changes correspond to the original definition of the term by Goebel (1900-1905), which implies substantial changes in the leaf form among different metamers during plant development. This form of shoot development was called metamorphic by Ray (1990), and redefined as metamorphic heteroblasty by Zotz et al. (2011).
Materials and Methods
Field and herbarium observations and conventional light and scanning microscopy were carried out in nine species of Berberis s.l. Young shoots of seven tropical Andean species of Berberis were collected in the Eastern Cordillera of Colombia, as follows: B. carupensis Camargo (Gonzalez 4435; Fig. 2j); B. glauca Kunth (Gonzalez 3782A); B. goudotii Triana & Planchon (Gonzalez 3781A; Fig. 20; B. huertasii Camargo (Gonzalez et al. 4330, 4421; Fig. 2g); B. petriruizii Camargo (Gonzalez & Pabon-Mora 4333; Fig. 2e); B. rigidifolia Kunth, (Gonzalez & Stevenson 3727); and B. samacana Camargo (Gonzalez 4069A). Three additional temperate species, B. dictyophylla Franch. (Pabon-Mora 262; Fig. 2h, i), B. thunbergii DC (Pabon-Mora 261; Fig. 2a-c), and Mahonia beali Pynaert (Pabon-Mora 265; Fig. 2k) were collected from cultivation in the New York City area. In all cases, young vegetative and reproductive shoots were fixed in 70% ethanol; voucher specimens were deposited at COL and NY.
For light microscopy, fixed material was dehydrated through an alcohol-toluene series in a Leica TP-1020 automatic tissue processor, and embedded in Paraplast X-tra (Fisher Healthcare, Houston, Texas, USA) using an AP 280 Microm (Thermo Fisher Scientific Inc. Waldorf, Germany) tissue embedding center. The samples were sectioned at 10-20 [micro]m with an AO Spencer 820 (GMI Inc. Minnesota, US) rotary microtome. Sections were stained with Johansen's safranin and 0.5% Astra Blue in 2% tartaric acid w/v in distilled water and mounted in Permount (Fisher Scientific, Pittsburgh, Pennsylvania, USA). Sections were viewed and digitally photographed with a Zeiss Axioplan compound microscope equipped with a Nikon DXM1200C digital camera with ACT (1) software.
For scanning electron microcopy studies, young shoots were dissected and dehydrated through an ethanol series and critical point dried using a Samdri 790 CPD. Material was mounted on aluminum stubs with adhesive tabs (Electron Microscopy Sciences), sputter coated with gold-palladium in a Hummer 6.2 sputter coater; and examined and photographed at 10 kV in a Jeol JSM-5410 LV Scanning Electron Microscope.
All the species of Berberis examined in this paper present a shoot system consisting of spiny long shoots and axillary short shoots, with a set of cataphylls at the base followed by foliage leaves (Figs. 2a-j, 3 and 4). Whereas long shoots are indeterminate, each short shoot terminates in a cymose inflorescence (Fig. 2c, e-g, j); thus, the shoot system in Berberis is pleonantic. Long shoots in tropical species (Fig. 2d g, j) grow and produce spiny leaves evenly throughout the year. Temperate species (Fig. 2a-c, h, i) grow seasonally and most of the elongation of the long shoots occurs during warm seasons. Mahonia differs from Berberis s. str. in that the long shoot/short shoot does not occur, and the flowering shoots do not develop foliage leaves but a set of two small cataphylls and a high number of spirally arranged bracts (Figs. 2k, 8 and 9).
Leaf Initiation, Morphogenesis and Histogenesis in Berberis
The initiation and morphogenesis of leaves in the species examined of Berberis follow similar patterns, therefore, hereafter descriptions alternate between B. glauca (Fig. 3) and B. thunbergii (Fig. 4).
Spines. Spines develop in a spiral arrangement on the long shoots (Figs. 3a, b and 4a-c). The initiation of the lateral arms becomes apparent from plastochrone three (P3) on (Fig. 3a, b), before the formation of the articulation above the leaf base (Fig. 3d f). Stipules form flanking the leaf base simultaneously with the epidermal differentiation of papillae (Figs. 3d g, i-l and 4d). The leaf base is massive and becomes sheathing, surrounding the axillary short shoots (Figs. 3e-m and 4a-d, j-n).
Spines are almost terete in cross section (Fig. 5b-e). One central vascular bundle enters the leaf base (Figs. 5b-d, 6g) and splits into two lateral traces that irrigate the stipules (Figs. 5b-h and 6a). The central bundle splits again immediately below the level of the articulation, which is particularly evident in the species with three or five spine arms (Fig. 5i). The adaxial and abaxial epidermis of the leaf base is formed by slightly rectangular cells with papillae and stomata (Fig. 7c). The mesophyll of the leaf base is formed of isodiametric parenchymatic cells that become collenchymatic at later stages (Fig. 5f-i). Cells flanking the vascular bundle become schlerenchymatic as the spine enlarges (Fig. 6h). Above the articulation, the epidermis is uniform adaxially and abaxially and is composed of large, transversally striate rectangular cells, lacking stomata and papillae (Figs. 5b-e, 6a, e, g and 7d). The young mesophyll cells are isodiametrical, densely packed and are organized in a four layered adaxial palisade and a 4-5 layered abaxial spongy mesophyll (Fig. 6g). At later stages, large areas of the mesophyll flanking the vascular bundle become schlerenchymatic (Fig. 6a).
The spines along the long shoots in the examined species of Berberis vary from single in B. thunbergii (Figs. 2a-c, 4a-d) to 3-5-furcate in B. glauca (Figs. 2d and 3d, g, i-l) and B. dictiophylla (Fig. 2h-i). However, the number of arms can also vary within the same species or even the same individual. The number of foliage leaves that form the short shoots vary between four and eight (Fig. 2a, b, d-j), and their margins can be entire in B. carupensis (Fig. 2j), B. thunbergii (Fig. 2a-c), and B. huertasii (Fig. 2g), and spinose in the remaining species (Fig. 2d-f, h, i). Mahonia lacks spines, but the cataphylls of the renewal shoots are conical, tuft, and possess an acute apex (Fig. 8e-j; see below).
Cataphylls. A set of two subopposite cataphylls initiate almost simultaneously on the short shoots (Figs. 3c-e and 4d-g). The cataphylls occupy a lateral position with respect to the axis of the long shoot. Cataphyll primordia are dome-shaped (Figs. 3c, d) but soon become triangular with a tapering apex (Figs. 3e-h and 4e-g, i, j). Most of the epidermal cells are papillose and are interspersed with few stomata, both adaxially and abaxially (Figs. 6b-t and 7a, b). No articulation was detected (Figs. 3f-m, 4g, i, m and 6b, c), which indicates that the cataphylls correspond only to the leaf base.
Cataphylls are triangular in cross section (Fig. 5b-e) and are irrigated by a single vascular bundle (Fig. 5b-i). The epidermis is uniform adaxially and abaxially composed of papillose cells (Fig. 5f-i). The young mesophyll is formed of uniform parenchymatic cells (Figs. 5b-i and 6b, c). At later stages large areas of the mesophyll flanking the vascular bundle become sclerenchymatic (Fig. 6a), similarly to the spines described above.
Foliage Leaves. Foliage leaves develop in spiral arrangement in a rapid series of 5-6 plastochrones before the apical meristem of the short shoot becomes reproductive (Figs. 3d-h, j, l and 4e-g, j-n). The articulation between the leaf base and the expanding lamina becomes evident by plastochrones 3-4 (Figs. 3f, g and 4j-l). The leaf base is massive as in the spiny leaves (Figs. 3h-m and 41-o). Stipules develop at the flanks of the leaf base simultaneously with the epidermal differentiation of papillae (Figs. 3h-m and 4m-o). The leaf base becomes sheathing, protecting the younger leaves and the apical meristem of the short shoot (Figs. 3im and 4l-o).
The leaf base is almost terete in cross section (Fig. 5b d, f). One central vascular bundle enters the leaf base (Fig. 5f, g). Immediately below the level of the articulation, the phloem of the massive main vascular bundle becomes packed in 3 5 discrete strands (Fig. 5g). This vascular bundle becomes the mid-vein of the lamina immediately above the articulation (Figs. 5h, i and 61), from which the secondary veins depart (Figs. 61).
The epidermis of the leaf base, both adaxial and abaxial, has papillose cells and stomata (Fig. 7e). The mesophyll of the leaf base is similar to that found in the base of the spine (Figs. 5g-i and 6i, j). Above the articulation, the epidermis is similar adaxially and abaxially, and it is formed by isodiametrical cells; stomata were observed only in the abaxial surface (Figs. 6k, 1 and 7f, g). The young mesophyll is organized in a single-layered adaxial palisade and a 5 to 6 layered abaxial spongy mesophyll (Fig. 6k). Sclerenchyma in laminar leaves is strongly reduced, compared to that present in the mesophyll of the spines (Figs. 5f-i and 6a, h, 1).
Leaf Initiation, Morphogenesis and Histogenesis in Mahonia
Cataphylls. A series of protective cataphylls are present in both the renewal and the short reproductive shoots of Mahonia (Figs. 8e-j and 9). As in Berberis, the cataphylls occupy a lateral position with respect to the axis of the long shoot. The young cataphylls of the renewal shoots are narrowly conical and spine-like (Fig. 8e-j). Each cataphyll is divided into two regions: a massive leaf base with two large stipules, and an imparipinnate compound lamina with 5-6 articulate leaflet pairs; the vestigial leaflets of the cataphylls remain appressed to the thick rachis and the terminal leaflet folds (Fig. 8e-j) so that macroscopically cataphylls have the appearance of single spines. The petiolar region is extremely reduced (Fig. 8e-h). The basal-most cataphyll protects younger cataphylls (Fig. 8e).
In addition to the vegetative short shoots, seasonally reproductive short shoots unfold axillary to the foliage leaves in Mahonia. The reproductive shoots also have a series of two to seven cataphylls; the two basal most cataphylls alternate to each other (Fig. 9a-c, f) and occupy a lateral position with respect to the main axis; cataphylls above them are spirally arranged and gradually become the subtending bracts of the inflorescence (Fig. 9c-f). All cataphylls and bracts are consistently simpler than those found in the vegetative branches, as they are reduced to the leaf base, and no stipules or vestigial leaflets are formed (Fig. 9).
Foliage Leaves. Foliage leaves develop in spiral arrangement in a rapid series of 4-5 plastochrons (Fig. 8a-c). There is no articulation between the leaf base and the expanding lamina (Fig. 8a-c). The lamina is compound and leaflet initiation occurs basipetally (Fig. 8a-d). The base of the leaflets and the rachis at the level of leaflet insertion become articulated in later stages (Figs. 1i and 2k). The leaf base is massive as in the cataphylls, but unlike Berberis, the epidermis of the leaf base is not papillose (Fig. 8a-c). The leaf base becomes sheathing, protecting the younger leaves and the apical meristem (Fig. 8a-c). Stipules are formed from the flank of the leaf base (Fig. 8ac). The spines along the margins of the foliage leaflets in Mahonia develop at later stages, during leaf expansion.
Leaf Homologs in Berberis s. l.
Our results regarding leaf initiation, morphogenesis and histogenesis show that each spine along the long shoots, either single or furcated, is a leaf homolog with the leaf base clearly differentiated from the laminar portion. No developmental evidence was found to support the hypothesis that each spine represents a modified branch, as invoked by Croizat (1960), or outgrowths "from single epidermal cells", as stated by Harvey-Gibson and Horsman (1919:504). Similar abrupt morphogenetic and anatomical changes between foliage, simple leaves, and trifurcated and spiny leaves co-occurring in the same plant are rare; for instance, they have been reported to occur in Hakea trifurcata R. Br. (Proteaceae). However, unlike Berberis, such abrupt leaf changes in Hakea occur along the same shoot, and appear to be strongly related to eco-physiological factors (Goebel, 1900-1905; Groom et al., 1994).
Occasionally, some species of Berberis s. str. (e.g.B. stapfiana C. K. Schneid., B. vulgaris L., and B. wilsoniae Hemsl.) show a gradual shift from spiny to laminar leaves (Masters, 1869; Tisehler, 1902; Troll, 1937-1943, his figs. 1639 and 1640, 1954, 1959; Rauh, 1950, his Fig. 96; Landrum, 1999), but when that occurs, such a shift is gradual, not drastic, and the resulting laminar leaf is different from the foliage leaves of the same individual.
Our results also indicate that, as in the foliage leaves of the long shoots, the two flanking stipules are formed directly from the leaf base, which supports the descriptions by Gluck (1919), Troll (1937-1943, 1954, 1959) and Rauh (1950), among others. Stipules in Berberis, Epimedium, Leontice and Mahonia are described as consisting of a basal ligular (Vaginalstipeln) portion more or less crowned by two or three small lateral processes ("Stipeln") by Gluck (1919). We have also demonstrated that the lateral arms of the furcated spines are not stipules, contrary to Bell's (1991) descriptions. In all species examined, the structure of the leaf base is more conservative, the lamina in the foliage leaves is more plastic, and the petiole often does not form. The stipulate leaf base is present in all leaf homologs of Berberis s. str. that is, the spiny leaves of the long shoots, the foliose leaves of the short shoots, and the cataphylls. However, the laminar portion is completely lacking in the cataphylls; thus, they are not arrested forms of adult foliage leaves, but are entirely formed by the leaf base. The lack of petioles in the foliage leaves of Berberis s. str. could be the result of progenesis caused by the developmental truncation due to early and rapid transition from vegetative to reproductive phase of the shoot apical meristem. Goebel (1900-1905) regarded the absence of a petiole as a common trait in cataphylls. The reduction of the cataphylls of the short shoots of Berberis and Mahonia are concordant to Foster's (1928) observations in a number of other plants such as Acer (Aceraceae)and Aesculus (Sapindaceae), in which the cataphylls appear to represent a modified development of the leaf base, whereas the petiolar portion is more labile.
According to our observations, the apical meristem of the short shoots form a rapid series of foliose leaves, each from independent leaf primordia, before forming the terminal inflorescence. The phase change of the apical meristem of the short shoots from vegetative to reproductive stands against Ahrendt's (1961) interpretation that each foliose leaf in these shoots represents a leaflet of a palmately compound leaf. Additionally, foliage pinnately-compound leaves of Mahonia (Fig. 8), and palmately-compound leaves in other members of the order Ranunculales (e.g. Lardizabalaceae; Sugiyama & Hara, 1988; Ranunculaceae; Pabon-Mora, 2012) clearly show that each compound leaf initiates from a single primordium, and that an early incepted terminal leaflet is always present, which clearly contradicts Ahrend's (1961) statement that a short shoot of Berberis is equivalent to a compound leaf.
We have shown that the cataphylls of the reproductive shoots of Mahonia are reduced and correspond to the sheathing basal portion of the leaf (Fig 9). This corroborates Foster's (1928:150) statement that the bud-scales in Mahonia "represent a modified development of the basal portion of the primordium with a concomitant "arrest" of the laminar region." The rapid arrest caused by the formation of the terminal inflorescences in the short shoots of Mahonia, could explain the extreme reduction of cataphylls and bracts only to the leaf base in the reproductive short shoots of Mahonia (Fig. 9) in a similar heterochronic process as that just mentioned for the reproductive short shoots of Berberis s. str. It is also consistent to the fact that the renewal shoots of Mahonia, which do not have constraints in the apical meristems, develop more complex cataphylls, formed of a leaf base, a short petiolar region, and a vestigial compound lamina (Fig. 8ej), corresponding to arrested but complete forms of adult foliage leaves in this genus. Thus, contrary to Ernst's (1964) statements, cataphylls of renewal shoots of Mahonia are not structurally comparable to those of Berberis, as they keep the compound nature of the foliage leaves in Mahonia, as it is clearly shown here (Fig. 8). Cataphylls conserving an arrested but clearly peltate and lobed lamina are known to occur also in Podophyllum peltatum (Holm, 1899, his Fig. 10a; Jones, 2001). This is a further example in which the external appearance of the scale-buds is not sufficient for assessing homology between them, as was predicted by Foster (1928:157: "On the contrary, it may be more correct to regard the external conformation of many scales as an example of homoplasv rather than of direct homology.)"
Plant Architecture, Heteroblasty and Heterophylly in Berberis s. l.
Differences in leaf morphology in Berberis s. l. falls into the original definition of heteroblasty given by Goebel (1900-1905), as in both lineages substantial changes in the leaf form occur among metamers of different orders of branching. Thus, leaf shape variation is a function of the order of shoots, which corresponds to the metamorphic shoot development sensu Ray (1990), described later as metamorphic heteroblasty by Zotz et al. (2011). Further heterophylly (defined here as the abrupt changes between leaves within the same shoot) occurs along short shoots of Berberis and Mahonia, as shown with the profound changes between the cataphylls and the foliage leaves in both taxa.
The metamorphic heteroblasty in Berberis is apparent in the plant from seedlings onwards. The two cotyledons have entire margins, the two pairs of eophylls ("primarblatter") have dentate margins, and above them, there is an abrupt change to trifid spiny leaves on the main axis. Seedlings and young plants of B. wilsoniae (Troll, 1937-1943:550, his fig. 424) and B. stapfiana (Troll, 1937 1943:647, his Fig. 507) already exhibit dramatic heteroblasty, with spiny leaves in the first order axis and laminar leaves on the growing second order short shoots. Although cotyledons and eophylls are expanded and photosynthetic (e.g. in B. bretschneideri Rehdel; B. vulgaris, and B. wilsoniae; Tischler, 1902; Rauh, 1950; Troll, 1954, 1959), the first leaves are already reduced to spiny, bladeless leaves. Thus, the transition between the eophylls and the spiny leaves, on one hand, and between the spines of the primary (long) shoot and the foliage leaves of the short shoots is drastic and occurs during the first branching onwards.
The long shoot/short shoot system is present in Berberis s. str. and Mahonia. Inflorescences in both lineages are formed terminally on the axillary short shoots, which have foliage leaves in Berberis s. str. but only cataphylls and bracts in Mahonia. A positional homology of these axillary short shoots between these two lineages was already proposed by Tischler (1902). The long shoot/short shoot ending in a terminal, monothelic inflorescence occur in all the tropical and temperate species of Berberis s. str. examined here, as well as in a number of other temperate species such as B. aggregata C. K. Schneid., B. aristata DC., B. beaniana C. K. Schneid., B. congestiflora Gay, B. darwinii Hook., B. dolichobotrys Fedde, B. julianae C. K. Schneid., B. thunbergii DC., and B. vulgaris L. (Tischler, 1902; Troll, 1937 1943, 1969). Occasionally in species such as B. candidula (Troll, 1969) the inflorescence is reduced to the terminal flower and one axillary flower.
Our study strongly suggests that such pleonantic, metameric heteroblasty in Berberis s. 1., is phylogeny-mediated and is not dependent upon environmental conditions. Similar shoot and leaf developmental processes were observed in both temperate and tropical species of Berberis s. str. No reversions to homoblasty occur in Berberis after mechanical, genetic or environmental modifications. Decapitation of the main axis in B. vulgaris and B. wilsoniae (Troll, 1954, 1959, 1937-1943) only affects the length of the intemodes of the short shoots, but has no effect on the spines or the shape of the foliage leaves. Additionally, the reported hybrid between B. vulgaris and M. aquifolia Ahrendt (B. x neubertii Hort. Ex Lem.; Beck, 1927) clearly retains the shoot system of Berberis over that of Mahonia; it produces spiny leaves in the long shoots and axillary simple foliage leaves born on short shoots. Foliage leaves also have a sheathing base and are articulated, suggesting that all of these characteristics are dominant in hybrids (Beck, 1927).
The metamorphic heteroblasty and concurrent heterophylly here documented in Berberis s. l. is different from that reported in Podophyllum. Heterophylly in P. peltatum occurs in an extremely programmed fashion year after year with respect to the development of rhizome scales, aerial shoot scales, and foliage leaves (Holm, 1899; Jones & Watson, 2001), but there is no difference in the developmental sequence of leaf homologs between the different shoot types, that is, rhizomes and aerial shoots, either vegetative or reproductive (Jones & Watson, 2001).
Eco-physiological variables, such as light, humidity, fire, grazing, nutrients, temperature, irradiance, photoperiod, among others have been directly or indirectly related as causal factors for heteroblasty and heterophylly (Allsopp, 1965; Lee & Richards, 1991; Winn, 1999; Zotz et al., 2011). However, none of these factors appear to have any effect on the metamorphic heteroblasty of Berberis, as both long and short shoots co-occur in the same individual, under the same environmental conditions. Both tropical and temperate species (exemplified by B. glauca and B. thunbergii, Figs. 3 and 4, respectively) examined here, show identical shoot and leaf developmental pathways. Even in the extreme temperature conditions of the paramos, species such as B. empetrifolia Lain. (Goebel, 1891; see his Table XII, Fig. 11) do not reduce the foliage leaves (a very common adaptation in paramo plants; F. Gonzalez, pers. obs.); instead, the leaves of this species become extremely involute as a strategy to tolerate sudden and continuous changes, all year round, in relative humidity, and temperature drop from 20 [degrees]C during the day to below 0 [degrees]C during the night.
Functional Implications of Heteroblasty in Berberis s. str.
The metamorphic heteroblasty of Berberis s. str. might be an efficient mechanism to improve fitness, as flowering occurs rapidly in fast growing, short shoots with expanded foliage leaves. Heterophylly might play a critical role for plant fitness (De Witt et al., 1998; Winn, 1999), as almost exclusively the foliage leaves of the short shoots, which are continuously produced and evenly distributed along the plant, carry out the photosynthetic functions. Thus, long shoots in Berberis could benefit the plant in promoting rapid and long-term growth and establishment due to the lack of apical constraint, as well as high stress tolerance, whereas the short shoots take upon the fast, efficient, and continuous photosynthetic rate, flowering, and seed set.
The spines of the long shoots might play a role in preventing predation, as it has been demonstrated in several spiny, heteroblastic species found mainly on islands (McGlone & Webb, 1981; Givnish et al., 1994; Bums & Dawson, 2006, 2009; among others).
In B. thunbergii, an invasive Japanese barberry, the presence of short shoots as a leaf phenology strategy increases photosynthetic capacity and leaf longevity (Xu et al., 2007).
Genetic Regulation of Leaf Morphogenesis in Model Organisms and Heteroblasty in Berberis
Genetic modules implicated in the regulation of leaf morphogenesis control five basic processes: (1) The acquisition of the abaxial-adaxial polarity; (2) the establishment of the three basic domains (dorsiventral, mediolateral and proximodistal); (3) the induction of blade outgrowth; (4) the maintenance of the domains during later growth; and (5) the generation of domain-specific tissues (Tsukaya, 2006; Efroni et al., 2010; Nakata et al., 2012). In this section we will review some of the genetic components that are known to regulate these processes in model organisms. In addition, we will highlight unique features of Berberis s. str. leaf development that make this a good candidate group to explore genetic mechanisms underlying heteroblasty in flowering plants.
In Arabidopsis numerous genes have been implicated in proper abaxial-adaxial patterning, these include ASYMMETRIC LEAVES1 (AS1), AS2, CLASS III HOMEODOMAIN-LEUCINE ZIPPER (HD-ZIPIII), FILAMENTOUS FLOWER (FIL)/YABBY,, and KANADI (KAN) (McConnell & Barton, 1998; Siegfried et al., 1999; McConnell et al., 2001; Emery et al., 2003; Eshed et al., 2004; Zgurski et al., 2005). Although the role of orthologs of these genes in non-model species is poorly known (McHale & Koning, 2004), at least PHANTASTICA (PHAN) in snapdragon and LePHAN in tomato, the orthologs of the Arabidopsis AS1, are key regulators of the adaxial domain in leaves. Loss of function of PHANTASTICA in phan and wiry mutants, result in radialized needle-like leaves, with abaxial identity, most likely as a result of the lack of leaf margin identity (Waites et al., 1998; Kim et al., 2003). On the other hand, alteration of the role of the HDZIPIII class genes, like in phb, phv and rev dominant mutants, results in abaxial to adaxial transfomation of lateral organs, often accompanied with ectopic axillary meristems (McConnell & Barton, 1998; McConnell et al., 2001; Prigge et al., 2005). Similarly, kan and fil yab3 double mutants in Arabidopsis show adaxialized lateral organs with altered vascular patterning (Sawa et al., 1999; Siegfried et al., 1999; Eshed et al., 2001, 2004; Mallory et al., 2004). Models for the development of leaf polarity support the idea of the homogenous expression of many of these factors in the unpolarized Plastochrone 0 (P0) leaf primordium, followed by the unequal distribution of abaxial vs. adaxial specific proteins via miRNA regulation, or negative regulation exerted by middle domain proteins dorsiventrally. These are the primary determinants of areas of marginal laminar growth (Eshed et al., 2001; Kerstetter et al., 2001; McConnell et al., 2001; Reinhart et al., 2002; Rhoades et al., 2002; Emery et al., 2003; Mallory et al., 2004; Pulido & Laufs, 2010; Nakata et al., 2012). Overall, accumulating data in Arabidopsis suggests a complex regulation of abaxial-adaxial identity, linked with marginal growth of lateral organs, proper vascular differentiation and axillary meristem development (Champagne & Sinha, 2004; Zgurski et al., 2005). In Berberis, leaf primordia shape in both leaf types is alike, suggesting that the early acquisition of abaxial-adaxial polarity and establishment of dorsiventral domains in spiny leaves in long shoots, and foliage leaves in short shoots, is controlled similarly. However, spiny leaves become nearly radial by P4-5 (Figs. 3a, b and 4a-c), suggesting that adaxial-abaxial patterning in the lamina is not maintained throughout spiny leaf development. Such nearly radial patterning in all arms that conform the spiny leaves (Figs. 3g, j, k, 1, 5b-e and 6a) suggests an atypical localization of adaxial-abaxial factors and the absence of a marginal meristem laminar growth in lateral organs in the long shoots, without altering vasculature or localization of the axillary meristems. On the contrary, cataphylls and foliage leaves developing in short shoots axillary to the spiny leaves, maintain typical adaxial-abaxial identity (Figs. 3h m, 4j-o and 6a, k, l), suggesting different genetic regulatory mechanisms controlling leaf morphogenesis in long and short shoots.
The molecular basis of proximal/distal differentiation in leaves involves the indirect role of AS1 and AS2 in Arabidopsis, ROUGH SHEATH2 (RS2) in maize and PHANTASTICA the snapdragon homolog, altogether known as ARP genes (Kidner & Timmermans, 2010). ARP genes are expressed at the site of leaf initiation and in young leaf primordia; later on, they promote distal identity, as shown by rs2 and phan mutants, which show blade cells adopting sheath-like or petiole (proximal) identity (Schneeberger et al., 1998; Waites et al., 1998; Tsiantis et al., 1999; Byrne et al., 2000; Zgurski et al., 2005; Katayama et al., 2010). Moreover, ARP genes antagonize WUSCHEL and Class 1 KNOTTED1-LIKE HOMEOBOX (KNOX1) genes (Waites et al., 1998; Timmermans et al., 1999; Ori et al., 2000; Venglat et al., 2002; Zgurski et al., 2005; Katayama et al., 2010), that promote meristem indeterminacy and maintain proximal cell division in leaf development after this has ceased in more distal areas (Byrne et al., 2000, 2002). All leaf types in Berberis s. str. engage a similar proximal-distal differentiation, having a massive leaf base with laminar growth and a distal lamina (Figs. 3h-m and 4j-o). This occurs in P5-6 in spiny leaves and in P3-4 in foliage leaves, suggesting that proximo-distal asymmetry is established similarly in lateral organs of long shoots and short shoots. However, cataphylls in Berberis s. str. and those found in the short inflorescences of Mahonia (Fig. 9), lack the distal lamina differentiation suggesting a truncation in distal identity due to the lack or premature cessation of cell division and/or the lack or down-regulation of distal identity gene homologs (potentially ARP orthologs) during cataphyll growth. It is worth noting that cataphylls lacking distal leaf identity have no defects in the abaxial-adaxial domains or in the regular histogenesis and morphogenesis typical of the leaf base (Figs. 3h-m, 4j-n, 5f-h and 9).
Once dorsiventral and proximodistal domains have been established, the induction of marginal growth and complexity (in compound leaves) begins. Genes controlling leaf complexity and leaf shape are relatively well known in flowering plants and most of them are factors involved in the meristematic maintenance of the shoot apex, that have been recruited in the regulation of leaf meristematic activity (reviewed in Champagne & Sinha, 2004; Efroni et al., 2010). The best-studied regulators of leaf complexity are the KNOX1 genes SHOOT MERISTEMLESS (STM) and its ortholog KNOTTED1 (Kn1) in maize, indispensable in maintaining proper shoot apical meristem (Long et al., 1996; Vollbrecht et al., 2000). The repression of KNOXI genes by ARP genes in the site of leaf initiation is a pre-requisite for the acquisition of determinacy in the leaf primordium (reviewed in Hay & Tsiantis, 2010). Once the leaf primordium has differentiated in the flank of the shoot apical meristem, KNOX1 genes remain down-regulated in species with simple leaves (Smith et al., 1992; Nishimura et al., 1998), or are subsequently up-regulated in species with compound leaves (Hareven et al., 1996; Bharathan et al., 2002). Complementary to the role of KNOX1 genes in promoting meristematic activity is the function of NO APICAL MERISTEM and CUP SHAPE COTYLEDON (NAM/CUC3) genes, which act as markers of leaf primordium boundaries and leaf dissection zones (Berger et al., 2009; Blein et al., 2008). It is thought that this regulatory module has been maintained across angiosperm diversification to directly shape leaf complexity and leaf shape (Berger et al., 2009; Blein et al., 2008). KNOX1 genes regulate leaf complexity in most angiosperms studied (reviewed in Hay & Tsiantis, 2010), with the exception of pea and Aquilegia where other genes have been co-opted to regulate leaflet formation and proper development. In pea (and close relatives within legumes; see Champagne et al., 2007), UN1FOLIATA (UN1), a LEAFY/FLORICAULA ortholog, regulates compound leaf development (Hofer et al., 1997), whereas, in Aquilegia (Ranunculaceae; Ranunculales), FRUITFULL, an APETALA1/FRUITFULL homolog, has been co-opted to promote leaf complexity (Pabon-Mora, 2012). In both cases, genes mostly known by their role as promoters of reproductive meristem identity, flower and fruit development have been recruited into the leaf morphogenesis genetic network. In Berberis s. str. spiny leaves can be simple (Fig. 2a-c and 4d, l, n, o) or furcated (Figs. 2d-j, 3d, g, i-l, 5b-e and 6a), whereas cataphylls and foliage leaves are always simple (Fig. 3g-m, 4j-o and 5f-i), suggesting once again that leaf complexity can be regulated differently in long and short shoots. Moreover, spiny leaves can produce up to 5 arms (leaflet homologs) while maintaining radial growth, suggesting that fractionation of the marginal meristem can occur in the absence of a clear dorsiventral domain. Finally, most species of Berberis s. l. possess compound foliage leaves (and compound cataphylls in Mahonia), suggesting that simple leaves and genetic mechanisms underlying simple leaf morphogenesis are derived in Berberis s str.
Heteroblasty in Berberis s. I. falls into the concept of a metamorphic shoot development, and it is phylogeny-mediated. This metamorphic heteroblasty is accompanied by heterophylly along the short shoots. The effect of heterophylly on the leaf base is minimal, but in the blade portion it is dramatic. The latter can become spiny or laminar, occasionally with gradual transitional forms. The heterochrony due to ontogenetic truncation caused by the formation of the terminal inflorescence at the apex of the short shoots could prevent the differentiation of the petiole in the foliage leaves.
The single to furcate spines are leaf homologs, and the lateral arms of the spines are not stipules. Stipules are formed in the flanks of the leaf base in all leaf homologs of Berberis s. l. (i. e. foliage leaves, spiny leaves, and cataphylls, except in the cataphylls of the flowering short shoots of Mahonia). A conspicuous articulation sharply delimits the leaf base from the laminar portion in both the foliage and the spiny leaves of Berberis s. str. Such articulation reflects the unifoliate condition of the leaves in Berberis. Foliage leaves can be unifoliolate as in the short shoots of Berberis s. str., or pinnately compound in Mahonia. Cataphylls are also affected by heteroblasty, as they are arrested in the form of pinnately compound cataphylls in the renewal shoots of Mahonia, or reduced to the leaf base (i. e. the laminar portion is completely absent) in the cataphylls of Berberis s. str, and those of the flowering shoots of Mahonia. Environmental factors are unlikely to be responsible for either the metamorphic heteroblasty or the heterophylly in Berberis s. str.
Thus, occurrence of metamorphic heteroblasty, heterophylly and (possibly) heterochrony in Berberis s. l., all phylogenetically fixed, makes this lineage an interesting one to explore in terms of genetic mechanisms that underlie such divergent leaf morphologies in a reiterative pattern in long and short shoots. The isolation and characterization of the expression patterns of the Berberis s.1. orthologs of the factors controlling abaxial-adaxial and proximal-distal differentiation, as well as genes involved in leaf complexity will shed light on the regulation and conservation of these genetic modules in a heteroblastic species.
Acknowledgments We thank D. W. Stevenson (The New York Botanical Garden) for inviting us to participate in the present issue of Botanical Review. We thank Barbara Ambrose for comments on the manuscript. We thank the Facultad de Ciencias, Universidad Nacional de Colombia, Bogota, and the staff of the Structural Laboratory, The New York Botanical Garden, for logistic support. We also thank J. Hennig, D. Basile, and M. Baxter (Lehmann College, City University of New York), for access to living collections and microscopy facilities.
Ahrendt, L. W. A. 1961. Berberis and Mahonia, a taxonomic revision. Botanical Journal of the Linnean Society 57: 1-410.
Allsopp, A. 1965. Heteroblastic development in connophytes. Pp 1172-1221. In: W. Ruhland (ed). Handbuch der Pflanzenphysiologie XV/1. Springer, Heidelberg.
Ashby, E. 1948. Studies in the morphogenesis of leaves. I. An essay on leaf shape. New Phytologist 47: 153-176.
Bharathan, G., T. E. Goliber, C. Moore, S. Kessler, T. Pham & N. R. Sinha. 2002. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296: 1858-1860.
Beck, P. V. 1927. Comparative anatomy of certain hybrid shrubs and their parents. The University of Kansas Science Bulletin 16: 367-396.
Bell, A. D. 1991. Plant Form. An illustrated guide to flowering plant morphology. Oxford University Press.
--. 2008. Plant Form. An illustrated guide to flowering plant morphology. Second edition. Timber Press.
Berger, Y., S. Harpaz-Saad, A. Brand, H. Melnik, N. Sirding, J. P. Alvarez, M. Zinder, A. Samaeh, Y. Eshed & N. Ori. 2009. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136: 823-832.
Blein, T., A. Pulido, A. Vialette-Guiraud, K. Nikovics, H. Morin, A. Hay, I. E. Johansen, M. Tsiantis & P. Laufs. 2008. A conserved molecular framework for compound leaf development. Science 322: 1835-1839.
Brodribb, T. & R. S. Hill. 1993. A physiological comparison of leaves and phyllodes in Acacia melanoxylon. Australian Journal of Botany 41: 293-305.
Burns, K. C. & J. W. Dawson. 2006. A morphological comparison of leaf heteroblasty between New Caledonia and New Zealand. New Zealand Journal of Botany 44: 387-396.
-- & --. 2009. Heteroblasty on Chatham Island: A comparison with New Zealand and New Caledonia. New Zealand Journal of Ecology 33: 156-163.
Byrne, M. E., R. Barley, M. Curtis, J. M. Arroyo, M. Dunham, A. Hudson & R. A. Martienssen. 2000. ASYMMETRIC LEAVES1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 104: 967-971.
--, J. Simorowski & R. A. Martienssen. 2002. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129: 1957-1965.
Camargo, L. A. 1960. A critical taxonomic study of 15 colombian species of Berberis. M. Sc. Thesis, Catholic University of America, Washington, D. C.
--. 1966. Especies nuevas del genero Berberis. Caldasia 9: 313-351.
--. 1981. Especies nuevas del genero Berberis. II. Caldasia 13: 203-222.
--. 1983. Especies nuevas del genero Berberis. III. Caldasia 13: 675-691.
--. 1991. Especies nuevas del genero Berberis. IV. Caldasia 16: 419-424.
Cameron, R. J. 1970 Light intensity and growth of Eucalyptus seedlings. I. Ontogenetic variation in E. fastigiata. Australian Journal of Botany 18: 29-43.
Champagne, C. & N. Sinha. 2004. Compound leaves: equal to the sum of their parts? Development 131: 4401-4412.
Champagne, C. E., T. E. Goliber, M. E Wojeiechowski, R. W. Mei, B. T. Townsley, K. Wang, M. M. Paz, R. Geeta & N. R. Sinha. 2007. Compound leaf development and evolution in the legumes. The Plant Cell 19: 3369-3378.
Croizat, L. 1960. Principia Botanica, or beginnings of botany. N. V. Drukkerij Salland Deventer, Netherlands. Cronk, Q. C. B. 2009. The molecular organography of plants. Oxford University Press, Oxford.
Cronquist, A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York.
Curtis, J. D. & N. L. Lersten. 1978. Heterophylly in Populus grandidentata (Salicaceae) with emphasis on resin glands and extrafloral nectarines. American Journal of Botany 65: 1003-1010.
Darrow, H. E., E Bannister, D. J. Burritt & P. E. Jameson. 2002. Are juvenile forms of New Zealand heteroblastic trees more resistant to water loss than their mature counterparts? New Zealand Journal of Botany 40: 313-325.
Day, J. D. 1998. Light conditions and the evolution of heteroblasty (and the divaricate form) in New Zealand. New Zealand Journal of Ecology 22: 43-54.
De Witt, T. J., A. Sih, & D. S. Wilson. 1998. Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution 13: 77-81.
Diggle, P. K. 1999. Heteroblasty and the evolution of flowering phenologies. International Journal of Plant Sciences 160($6): S123-S134.
Eckenwalder, J. E. 1980. Foliar heteromorphism in Populus (Salicaceae), a source of confusion in the taxonomy of Tertiary leaf remains. Systematic Botany 5: 366-383.
Efroni, I., Y. Eshed & E. Lifschitz. 2010. Morphogenesis of simple and compound leaves: a critical review. The Plant Cell 22: 1019-1032.
Ehrenfeld, J. G. 1997. Invasion of deciduous forest preserves in the New York metropolitan region by Japanese berberry (Berberis thunbepgii DC.). Journal of the Torrey Botanical Society 124:210 215.
Emery, J. E, S. K. Floyd, J. Alvarez, Y. Eshed, N. P. Hawker, A. Izhaki, S. F. Baum & J. L. Bowman. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Current Biology 13: 1768-1774.
Ernst, W. R. 1964. The genera of Berberidaceae, Lardizabalaceae and Menispermaceae in the southeastern United States. Journal of the Arnold Arboretum 45: 1-35.
Eshed, Y., S. E Baum, J. V. Perea & J. L. Bowman. 2001. Establishment of polarity in lateral organs of plants. Current Biology 11: 1251-1260.
--, A. Izhaki, S. F. Baum, S. K. Floyd & J. L. Bowman. 2004. Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131: 2997-3006.
Fedde, F. 1902. Versuch einer Monographie der Gattung Mahonia. Botanische Jahrbucher 31: 30-133.
Foster, A. 1928. Salient features of the problem of bud scale morphology. Biological Reviews 3: 123-164.
Gamage, H. K. & L. Jesson. 2007. Leaf heteroblasty is not an adaptation to shade: seedling anatomical and physiological responses to light. New Zealand Journal of Ecology 31: 245-254.
Gardner, S., A. Drinnan, E. Newbigin & P. Ladiges. 2008. Leaf ontogeny and morphology in Acacia Mill. (Mimosaceae). Muelleria 26: 43-50.
Gerrath, J. M. & C. R. Lacroix. 1997. Heteroblastic sequence and leaf development in Leea guineensis. International Journal of Plant Sciences 158: 747-756.
Givnish, T. J., K. J. Systma, J. F. Smith & W. J. Hahn. 1994. Thorn-like prickles and heterophylly in Cyanea--Adaptations to extinct avian browsers on Hawaii. Proceedings of the National Academy of Sciences, USA 91: 2810-2814.
Gluck, H. 1919. Pp 696. Blatt- und blutenmorphologische Studien. Eine morphologische Untersuchung uber die Stipulargebilde, uber die Intravaginalpapillen, uber die Blattscheide und uber die Bewertung der Blutenblattgebilde. Verlag von Gustav Fischer, Jena.
Goebel, K. 1891. Pp 1-50. Die Vegetation der venezuelanischen Paramos. Pflanzenbiologische Schilderungen, Vol. 2. N. G. Elwert'sche Verlagsbuchhandlung, Marburg.
--. 1900-1905. Organography of plants. Two volumes. Oxford University Press, Oxford.
von Goethe, J. W. 1790. Versuch, die Metamorphose der Pflanzen zu erlaren. Carl Wilhelm Ettinger, Gotha. Green, S., T. L. Green & Y. Heslop-Harrison. 1979. Seasonal heterophylly and leaf gland features in Triphyophyllum (Dioncophyllaceae), a new carnivorous plant genus. Botanical Journal of the Linnean Society 78:99-116.
Groom, P. K., B. B. Lamont & L. Kupsky. 1994. Contrasting morphology and ecophysiology of coocurring broad and terete leaves in Hakea trifurcata (Proteaceae). Australian Journal of Botany 42: 307-320.
Halle, E, R. A. A. Oldeman & E B. Tomlinson. 1978. Tropical trees and forests. An architectural analysis. Springer, New York.
Hansen, D. H. 1996. Establishment and persistence characteristics in juvenile leaves and phyllodes of Acacia koa (Leguminosae) in Hawaii. International Journal of Plant Sciences 157: 123-128.
Hareven, D., T. Gutfinger, A. Parnis, Y. Eshed & E. Lifschitz. 1996. The making of a compound leaf: Genetic manipulation of leaf architecture in tomato. Cell 84: 735-744.
Harvey-Gibson, R. J. & E. Horsman. 1919. The anatomy of stem of the Berberidaceae. Transactions of the Royal Society of Edinburgh 52: 501-515.
Hay, A. & M. Tsiantis. 2010. KNOX genes: Versatile regulators of plant development and diversity. Development 137: 3153-3165.
Hofer, J., L. Turner, R. Hellens, M. Ambrose, P. Mathews, A. Michael & N. Ellis. 1997 UNIFOLIATA regulates leaf and flower morphogenesis in pea. Current Biology 7: 581-587.
Holm, T. 1899. Podophyllum peltatum: A morphological study. Botanical Gazette 27:419-433.
Jaya, E., D. S. Kubien, P. E. Jameson & J. Clemens. 2010. Vegetative phase change and photosynthesis in Eucalyptus occidentalis: architectural simplification prolongs juvenile traits. Tree Physiology 30: 393-403.
Jones, C. S. 1993. Heterochrony and heteroblastic leaf development in two subspecies of Cucurbita argyrosperma (Cucurbitaceae). American Journal of Botany 80: 778-795.
--. 1995. Does shade prolong juvenile development? A morphological analysis of leaf shape changes in Cucurbita argyrosperma subsp, sororia (Cucurbitaceae). American Journal of Botany 82: 346-359.
--. 1999. An essay on juvenility, phase change, and heteroblasty in seed plants. International Journal of Plant Sciences 160: S105-S111.
--. 2001. The functional correlates of heteroblastic variation in leaves: changes in form and ecophysiology with whole plant ontogeny. Boletin de la Sociedad Argentina de Botanica 36: 171-184.
--, & M. A. Watson. 2001. Heteroblasty and preformation in mayapple, Podophyllum peltatum (Berberidaceae): Developmental flexibility and morphological constraint. American Journal of Botany 88: 1340-1358.
Katayama, N., S. Koi & M. Kato. 2010. Expression of SHOOT MERISTEMLESS, WUSHEL, and ASYMMETRIC LEAVES1 homologs in the shoots of Podostemaceae: implications for the evolution of novel shoot organogenesis. The Plant Cell 22: 2131-2140.
Kato, M. & H. Setoguchi. 1998. An rbcL-based phylogeny and heteroblastic leaf morphology of Matoniaceae. Systematic Botany 23: 391-400.
Kerstetter, R. A., K. Bollman, R. A. Tayler, K. Bomblies & R. S. Poethig. 2001. KANADI regulates organ polarity in Arabidopsis. Nature 411: 706-709.
Kidner, C. A. & M. C. P. Timmermans. 2010. Signaling sides: adaxial-abaxial patterning in leaves. In: M. C. P. Timmermans (ed). Plant Development. Elsevier, San Diego.
Kim, M., S. McCormick, M. C. P. Timmermans & N. Sinha. 2003. The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424: 438-443.
Kunze, H. 1986. Studien zur Blattmetamorphose. Beitraige zur Biologie der Pflanzen 61: 49-77.
Landrum, L. R. 1999. Revision of Berberis (Berberidaceae) in Chile and adjacent Southern Argentina. Annals of the Missouri Botanical Garden 86: 793-834.
Lee, D. W. & J. H. Richards. 1991. Heteroblastic development in vines. Pp 205-243. In: F. E. Putz & H. A. Mooney (eds). The Biology of Vines. Cambridge University Press, Cambridge.
Lindley, J. 183 I. An introduction to the natural system of botany; or, a systematic view of the organization, natural affinities, and geographical distribution of the whole vegetable kingdom. G. & C. & H. Carvill, New York.
Long, J. A., E. I. Moan, J. L Medfurd & M. K. Barton. 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66-69.
Mabberley, D. J. 2008. The plant book. Cambridge University Press, Cambridge.
Mallory, A. C., B. J. Reinhart, M. W. Jones-Rhoades, G. Tang, P. D. Zamore, M. K. Barton & D. P. Bartel. 2004. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5' region. EMBO J 23: 3356-3364.
Masters, M. T. 1869. Vegetable teratology. Ray Society, R. Hadwicke, London.
McAlpine, K. G. & L. K. Jesson. 2008. Linking seed dispersal, germination and seedling recruitment in the invasive species Berberis darwinii (Darwin's barberry). Plant Ecology 197: 119-129.
McConnell, J. R. & M. K. Barton. 1998. Leaf polarity and meristem formation in Arabidopsis. Development 125:2935-2942.
--, J. Emery, Y. Eshed, N. Bao, J. L. Bowman & M. K. Barton. 2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709-713.
McGlone, M. S. & C. J. Webb. 1981. Selective forces influencing the evolution of divaricating plants. New Zealand Journal of Ecology 4:20-28.
McHale, N. A. & R. E. Koning. 2004. MicroRNA- Directed cleavage of Nicotiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical meristems. The Plant Cell 16: 1730-1740.
MeLellan, T. 1993. The roles of heterochrony and heteroblasty in the diversification of leaf shapes in Begonia dregei (Begoniaceae). American Journal of Botany 80: 796-804.
Meacham, C. A. 1980. Phylogeny of the Berberidaceae with an evaluation of classifications. Systematic Botany 5:149-172.
Merrill, E. K. 1986. Heteroblastic seedlings of green ash. 1. Predictability of leaf form and primordial length. Canadian Journal of Botany 64:2645-2649.
Minorsky, P. V. 2003. The hot and the classic. Plant Physiology 133: 1671-1672.
Nakata, M., N. Matsumoto, R. Tsugeki, E. Rikirsch, T. Laux & K. Okada. 2012. Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. The Plant Cell 24: 519-535.
Nishimura, A., M. Tamaoki & M. Matsuoka. 1998. Expression pattern of KN-1 type tobacco homeobox genes. Plant Cell and Physiology 39: S60
Ori, N., Y. Eshed, G. Chuck, J. L. Bowman & S. Hake. 2000. Mechanisms that control Knox gene expression in Arabidopsis shoot. Development 125: 2935-2942.
Pabon-Mora, N. 2012. Functional evolution of the APETALAI/FRUITFULL gene lineage. PhD. Dissertation, The City University of New York, NY.
Poethig, R. S. 2003. Phase change and the regulation of developmental timing in plants. Science 301: 334-336.
Prigge, M. J., D. Otsuga, J. M. Alonso, J. R. Ecker, G. N. Drew & S. E. Clark. 2005. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. The Plant Cell 17: 61-76.
Pulido, A. & P. Laufs. 2010. Co-ordination of developmental processes by small RNAs during leaf development. Journal of Experimental Botany 61 : 1277-1291.
Ramirez, J. L. & S. R. S. Cevallos-Ferriz. 2000. Leaves of Berberidaceae (Berberis and Mahonia) from Oligocene sediments, near Tepexi de Rodriguez, Puebla. Review of Palaeobotany and Palynology ll0: 247-257.
Rauh, W. 1950. Morphologie der Nutzpflanzen. Quelle & Meyer, Heidelberg.
Ray, T. S. 1987. Cyclic heterophylly in Syngonium (Araceae). American Journal of Botany 74: 16-26.
--. 1990. Metamorphosis in the Araceae. American Journal of Botany 77: 1599-1609.
Reinhart, B. J., E. G. Weinstein, M. W. Rhoades, B. Barrel & D. P. Bartel. 2002. MicroRNAs in plants. Genes and Development 16: 1616-1626.
Rhoades, M. W., B. J. Reinhart, L. P. Lim, C. B. Burge, B. Barrel & D. P. Bartel. 2002. Prediction of plant microRNA targets. Cell 110: 513-520.
Sawa, S., K. Watanahe, K. Goto, E. Kanaya, E. H. Morita & K. Okada. 1999. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with zinc finger and HMG-related domains. Genes and Development 13: 1079-1088.
Schmidt, E. 1928. Untersuchungen uber Berberidaceen. Beihefte zum Botanischen Centralblatt 45: 329-396.
Schneeberger, R., M. Tsiantis, M. Freeling & J. A. Langdale. 1998. The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125:2857-2865.
Schneider, C. K. 1905. Die Gattung Berberis (Euberberis). Vorarbeiten fur eine Monographie. Bulletin del Herbier Boissier, ser. 2, 5: 33-48, 133-148, 391-403, 449-464, 655-670, 800-831.
--. 1908. Weitere Beitrage zur Kenntnis der Gattung Berberis (Euberberis). Bulletin del Herbier Boissier, ser. 2, 8:192-204, 258-266.
Siegfried, K. R., Y. Eshed, S. F. Baum, D. Otsuga, G. N. Drews & J. L. Bowman. 1999. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126: 4117-4128.
Sliander, J. A. & D. M. Klepeis. 1999. The invasion ecology of Japanese barberry (Berberis thunbergii) in the New England landscape. Biological Invasions 1: 189-201.
Smith, L. G., Greene, B., Veit, B. and Hake, S. 1992. A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116:21-30.
Sugiyama, M. & N. Hara. 1988. Comparative study on early ontogeny of coumpound leaves in Lardizabalaceae. American Journal of Botany 75: 1598-1605.
Takhtajan, A. L. 1997. Diversity and classification of flowering plants. Columbia University Press, New York.
Taylor, T. N., E. L. Taylor & M. Krings. 2009. Paleobotany, the biology and evolution of fossil plants. Academic Press, New York.
Timmermans, M. C. P., A. Hudson, P. W. Becraft & T. Nelson. 1999. ROUGH SHEATH2: a Myb protein that represses Knox homeobox genes in maize lateral organ primordia. Science 284:151 153.
Tischler, G. 1902. Die Berberidaceen und Podophyllaceen. Versuch einer morphologisch-biologischen Monographie. Botanische Jahrbucher 31: 596-727.
Troll, W. 1937-1943. Vergleichende Morphologie der hoheren Pflanzen. Band 1 (1-3). Gebruder Bomtraeger, Berlin.
--. 1954. Praktische Einfuhrung in die Pflanzenmorphologie. Gustav Fischer, Jena.
--. 1959. Allgemeine Botanik. Ferdinand Enke, Stuttgart.
--. 1969. Die Infloreszenzen. Typologie und Stellung im Aufbau des Vegetationskorpers. Vol. 2, part 1. Gustav Fischer, Stuttgart.
Tsiantis, M., R. Schneeberger, J. F. Golz, M. Freeling & J. A. Langdale. 1999. The maize rough sheath2 gene and leaf development in monocot and dicot plants. Science 284: 154-156.
Tsukaya, H. 2006. Mechanism of leaf-shape determination. Annual Review in Plant Biology 57: 477-496.
Venglat, S. P., T. Dumonceaux, K. Rozwadowki, L. Parnell, V. Babic, W. Keller, R. Martienssen, G. Selvaraj & R. Datla. 2002. The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proceedings of the National Academy of Sciences USA 99: 4730-4735.
Vollbrecht, E., L. Reiser & S. Hake. 2000. Shoot meristem size is dependent on inbred background and presence of the of the maize homeobox gene, knotted1. Development 127: 3161-3172.
Waites, R., H. R. N. Selvadurai, I. R. Oliver & A. Hudson. 1998. The phantastica gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93: 779-789.
Wang, W., A.-M. Lu, Y. Ren, M. E. Endress & Z.-D. Chen. 2009. Phylogeny and classification of Ranunculales: Evidence from four molecular loci and morphological data. Perspectives in Plant Ecology, Evolution and Systematics 11: 81-110.
Wiltshire, R. J. E., J. B. Reid & B. M. Potts. 1998. Genetic control of reproductive and vegetative phase change in the Eucalyptus risdonii-E, tenuiramis complex. Australian Journal of Botany 46: 45-63.
Winn, A. A. 1996. The contribution of programmed developmental change and phenotypic plasticity to within-individual variation in leaf traits in Dicerandra linearifolia. Journal of Evolutionary Biology 9:737-752.
--. 1999. The functional significance and fitness consequences of the heterophylly. International Journal of Plant Sciences 160(6 Suppl.): S113-S121.
Xu, C.-Y., K. L. Griffin & W. S. E Schuster. 2007. Leafphenology and seasonal variation of photosynthesis of invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern United States deciduous forest. Oecologia 154:11-21.
Zgurski, J. M., R. Sharma, D. A. Bolokosi & E. A. Schultz. 2005. Asymmetric auxin response precedes asymmetric growth and differentiation of asymmetric leaf 1 and asymmetric leaf 2 Arabidopsis leaves. The Plant Cell 17: 77-91.
Zotz, G., K. Wilhelm & A. Becker. 2011. Heteroblasty--A review. Botanical Review 77: 109-151.
Natalia Pabon-Mora (1),(3),(4) * Favio Gonzalez (2)
(1) The New York Botanical Garden, Bronx, NY 10458, USA
(2) Instituto de Ciencias Naturales, Universidad Nacional de Colombia, AA 7495 Bogota., Colombia
(3) Present Address: Instituto de Biologia, Universidad de Antioquia, AA 1226 Medellin, Colombia
(4) Author for Correspondence; e-mail: firstname.lastname@example.org
Published online: 10 October 2012
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|Author:||Pabon-Mora, Natalia; Gonzalez, Favio|
|Publication:||The Botanical Review|
|Date:||Dec 1, 2012|
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