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Anatomy and Morphology |
2Instituto de Ciencias Naturales, Universidad Nacional, Ap. Ae. 7495, Bogotá, Colombia; and 3Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK
Received for publication March 15, 2001. Accepted for publication June 26, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Aristolochiaceae • Chloranthaceae • cymes • Lactoris • leaf ontogeny • magnoliids • monocotyledons • Piperaceae • Piperales • sympodial growth
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). It belongs in the magnoliid clade, which includes Piperales, Magnoliales, Laurales, Winterales, and possibly Chloranthaceae and monocotyledons, although the relationships of these taxa are still unresolved (APG, 1998
; Qiu et al., 2000
; Soltis et al., 2000
). Morphological treatments have variously linked Lactoris with Magnoliales (Cronquist, 1981
; Lammers, Stuessy, and Silva, 1986
), Laurales (Takhtajan, 1980
; also Annonales suborder Laurineae; Thorne, 1974
), or Piperales (Saururaceae and Piperaceae; e.g., Bentham and Hooker, 1880
; Hallier, 1903
; McLaughlin, 1933
; Meeuse, 1972
; Burger, 1977
; Carlquist, 1990
). Recent molecular data place it firmly in Piperales, together with Aristolochiaceae, Piperaceae, and Saururaceae (e.g., Qiu et al., 1999, 2000
), although relationships with other magnoliids (including monocotyledons and Chloranthaceae) remain equivocal. More controversially, however, molecular data have indicated a close relationship between Aristolochiaceae and Lactoridaceae, placing Lactoris as sister to (e.g., Neinhuis, Borsch, and Hilu, 1999
) or even nested within (e.g., Qiu et al., 1999, 2000
) Aristolochiaceae.
Many investigations have sought additional data to explore these putative relationships. These include studies on vegetative anatomy (McLaughlin, 1933
; Lemesle, 1953
; Carlquist, 1990
), ultrastructure (Behnke, 1988
; Hennig et al., 1994
), floral development and morphology (Tucker and Douglas, 1996
), reproductive biology (Skottsberg, 1928
; Bernardello et al., 1999
), pollen morphology including fossil pollen (Erdtman, 1952
; Carlquist, 1964
; Zavada and Taylor, 1986
; Zavada and Benson, 1987
; Sampson, 1995
; Macphail, Partridge, and Truswell, 1999
; González, Rudall, and Furness, in press
), embryology and karyomorphology (Bouman, 1971
; Tobe et al., 1993
), gynoecium and fruit development (Meeuse, 1971
; Melikian and Brobov, 1999
), allozyme and DNA variation (Brauner, Crawford, and Stuessy, 1992
; Crawford et al., 1994
), and phytochemistry (Crawford, Stuessy, and Silva, 1986
). However, two morphological traits of Lactoris that have been overlooked for detailed investigation are the branching pattern (including the position of the flower/inflorescence) and stipule development, the latter briefly commented on by Weberling (1970)
. These characters have been variously scored for Lactoridaceae in several cladistic analyses (e.g., Dahlgren and Bremer, 1985
; Donoghue and Doyle, 1989
; Loconte and Stevenson, 1991
; Stevenson and Loconte, 1995
; Tucker and Douglas, 1996
). This paper describes inflorescence structure and stipule development in Lactoridaceae and compares them with those of other Piperales (Piperaceae, Saururaceae, and Aristolochiaceae), in the context of systematic relationships within the order.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Material was fixed in formalin acetic alcohol (FAA) and stored in 70% ethanol. For scanning electron microscope (SEM) examination, apical meristems and axillary buds were carefully dissected in 90% ethanol, then dehydrated in an absolute ethanol : acetone series (90% ethanol, 30 min; absolute ethanol, 30 min; absolute ethanol : acetone in proportions 50 : 50, 10 min; and finally two steps of acetone, 10 min each). Dehydrated material was then critical-point-dried using a Balzer CPD 020 (Balzer Union, Furstentum, Liechtenstein), mounted onto SEM stubs on double-sided sellotape, coated with gold using an Emscope SC 500 sputter coater (Emscope, Ashford, UK), and examined using a Cambridge 240 SEM (Cambridge Instruments, Cambridge, UK). For light microscope observations of Lactoris, apical portions were sectioned using standard methods of Paraplast embedding and serial sectioning (6–12.5 µm thickness) with a Reichert Jung 2040 rotary microtome. Sections were stained in safranin and Alcian blue and mounted in DPX (distyrene, the plasticizer tricresyl phosphate, and xylene). Photomicrographs were taken using a Leitz Diaplan photomicroscope (Leitz, Germany).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. There is one bud in each leaf axil. The axillary buds from the proximal leaves of the main branches become vegetative renewal shoots, whereas those from the distal leaves become partial inflorescences (Figs. 1 and 3). Both the vegetative shoots and the partial inflorescences have a single, adaxial prophyll (Figs. 1, 3, 13, and 14).
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) that run along the sides of the internode (Figs. 1–3, 13, and 25–27).
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), i.e., a branch that ends in a terminal flower and has axillary partial inflorescences that, in turn, end in terminal flowers.
Each partial inflorescence consists of a prophyll and a terminal flower, between which a second-order flower and its corresponding prophyll are formed (Figs. 3 and 29–33). A third-order flower sometimes develops. The partial inflorescences are rhipidia, as the two or more flowers on each partial inflorescence have a distichous structure, and the flowers follow a zigzag pattern. The prophyll corresponding to the second- or third-order flower within each partial inflorescence is often reduced to its stipular portion (Fig. 14). Furthermore, each prophyll is opposite the median perianth part of its corresponding flower (Figs. 2, 3, and 14), following prophyllate aestivation (as defined by Weberling, 1989
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, not monopodial, as described by Kubitzki (1993)
. This is a significant observation in terms of magnoliid evolution, since the sympodial habit is an important feature of monocotyledons and also occurs in the basal clades of Aristolochiaceae (Saruma, Asarum, and some species of Thottea and Aristolochia; see González, 1999a, b
), many Piperaceae, most Saururaceae, and Chloranthaceae. It may therefore prove to be a synapomorphy (or partial synapomorphy) for these groups, which are also linked by other morphological characters, although this hypothesis requires rigorous testing in a revised morphological cladistic analysis. The terminal flower in Lactoris has been overlooked in previous descriptions, although it was figured by several authors, such as Muñoz-Pizarro (1966)
, Takhtajan (1969)
, Bernardello et al. (1999)
, and Tucker and Douglas (1996)
.
Leaf structure
This investigation has also demonstrated that the ochrea-like structure of Lactoris is closely connected to the leaf base; it is not a median or ligular stipule formed by a cross meristem ("Transversalwulst") as in many magnoliids and monocots (reviewed by Rudall and Buzgo, in press
), but rather a structure formed by the fusion of two lateral stipules. This conclusion is further supported by the bifid or bilobed apex of the so-called ligule at maturity. This interpretation is in agreement with Carlquist (1964)
, who described the "wings" as "extensions of [the] stipules." It contradicts Lemesle's (1955)
statement that stipules of Lactoris "are completely independent from the leaf base but fused to it."
Stipules are lateral appendages of the leaf base. They are present in at least some Saururaceae (Saururus in Figs. 15–16; Houttuynia in Fig. 18), some Piperaceae, and some other magnoliids, including Magnoliaceae. In Chloranthus, the leaf base resembles that of Saururaceae, but the leaves are opposite rather than alternate, and the sheath is formed by two fused opposing leaf bases (Figs. 19 and 20). The stipules in Chloranthus are modified, but there is a ligular projection between them. There is striking similarity in stipule morphology and development between Lactoris and members of the families Piperaceae and Saururaceae (see also Glück, 1919
; Roth, 1949
; Weberling, 1970
), demonstrated by Roth's (1949)
illustration of Houttuynia. This observation contradicts Carlquist's (1964)
view that the stipules of Lactoris are probably not indicative of relationship with other stipulate plants. Stipules in Piperaceae and Saururaceae form a ligule-like structure on the adaxial side of the leaf base (i.e., the vaginal lobe, the ochrea-like stipule, or the intrapetiolar stipule of some authors) and a sheath that fuses on the opposite side of the leaf (Fig. 17; see also Ponzo, 1934
; Bharathan, 1996
). At least in Saururaceae, the ligule-like structure is bifid at the apex (Fig. 18), which indicates that it is formed from the fusion of two lateral stipule primordia, as in Lactoris. On the other hand, in all members of Aristolochiaceae the leaf base is sheathing but stipules are entirely lacking (Figs. 21–23), presumably representing a reversal for the family. Stipules are relatively rare in monocots, but although it is commonly believed that dicot stipules and monocot ligules have different development origins, there is some evidence from ontogeny (e.g., Roth, 1949
) and developmental genetics (Mooney and Freeling, 1997
) that this is not the case. The morphology of the leaf tip in Lactoris (Figs. 8, 10) is worth noting in this context, as it closely resembles the precursor tip ("Vorläuferspitze") of many monocotyledons, and may be homologous with the upper leaf zone ("Oberblatt") (reviewed by Rudall and Buzgo, in press
).
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and Bernardello et al. (1999)
also observed. Cymose partial inflorescences (rhipidia) are therefore possibly synapomorphic for Lactoris and the Aristolochiaceae. Inflorescences of Lactoris have previously been described in various ways. Engler (1887)
and Skottsberg (1928)
noted the formation of 1–4 flowered axillary monochasia. Bentham and Hooker (1880)
, Muñoz-Pizarro (1966)
, and Lammers, Stuessy, and Silva (1986)
described the presence of solitary flowers, but they also observed that two or three flowers can occur together. Kubitzki (1993)
stated that "what is called inflorescence is a raceme-like structure that represents a brachyblast producing 1 to 4 leaves each with one axillary flower." Stevenson and Loconte (1995)
and Tucker and Douglas (1996)
both coded solitary flowers for Lactoris. Despite this, both their analyses have the cyme as an alternative character state. Tucker and Douglas (1996)
mentioned that the position of the inflorescence is axillary and that each flower is in the axil of a bract, but that basal bracts of the inflorescence are absent. Stuessy et al. (1998)
accordingly interpreted inflorescences in Lactoris as raceme-like structures, with single flowers subtended by leaves. However, our observations show that the inflorescences occupy the terminal portions as well as the axils of the branches, that the flowers are opposite to bracts, and that there is a basal bract (a prophyll) on each partial inflorescence. Saururaceae and most Piperaceae also have terminal inflorescences and sympodial growth.
Doyle and Endress (2000)
stated that prophylls in Lactoris are paired and lateral and that rhipidia in Annonaceae and Aristolochiaceae are "assumed to be derived from solitary." Our data indicate the opposite, i.e., that there is a single, adaxial prophyll in Lactoris and that rhipidia (or cymes of any kind) are plesiomorphic in Aristolochiaceae and Lactoridaceae, or at least in Aristolochiaceae.
Relationships within magnoliids
A placement for Lactoris within the order Piperales seems highly likely; both molecular evidence (e.g., Qiu et al., 1999, 2000
) and several morphological characters, including presence of stipules and sympodial growth, are consistent with this position. In a series of insightful papers on comparative wood anatomy in magnoliids, Carlquist (1990, 1992, 1993)
and Carlquist, Dauer, and Nishimra (1995)
demonstrated a potential suite of synapomorphies for Piperales (Lactoris, Piperaceae, Saururaceae, and Aristolochiaceae), including simple perforations, fiber-tracheids, scanty vasicentric axial parenchyma, and predominantly upright ray cells. Many of these characters are also shared with Chloranthaceae. Wood anatomy of Lactoridaceae is "virtually identical to that of Piperaceae" (Carlquist, 1990
: 1499). Within Saururaceae, vascular cambial activity is at best vestigial in Saururus and Houttuynia (as in monocotyledons), but in Anemopsis wood anatomy is highly comparable with that of other Piperales. Igersheim and Endress (1998)
noted that "special similarities with monocots are more prominent in the Aristolochiales [i.e., Aristolochiaceae and Lactoris] than in other paleoherbs," citing trimerous flowers as an example. This statement is also true for other Piperales (Saururaceae and Piperaceae), and relationships between the four families of Piperales and other magnoliids, especially monocots and Chloranthaceae, require further exploration.
Relationships within Piperales
Although combined analyses of molecular data (e.g., Graham and Olmstead, 2000
; Qiu et al., 2000)
have indicated the monophyly of the order Piperales, the phylogenetic position of Lactoris within Piperales remains equivocal from both the standpoint of molecular and morphological data.
Duvall (2000)
assessed phylogenetic placements of Lactoris using analyses of molecular data from different gene loci. He found that placements varied with different loci, from sister to Piperales, sister to Aristolochiaceae, to being nested within Aristolochiaceae (sister to Aristolochia). Graham and Olmstead (2000)
presented an analysis of basal angiosperms using 17 chloroplast genes but with limited taxon sampling: Piperales were represented by only Asarum (Aristolochiaceae), Lactoris, and Saururus. They found that a combined analysis of sequence, indel, and intron data from all 17 chloroplast genes resolved Lactoris and Saururus as sister taxa with 89% bootstrap support. In contrast, their combined analysis using only data from atpB, ndhF and rbcL genes, resolved Asarum and Lactoris as a sister pair with 74% bootstrap support. Lactoris occupies a long branch with respect to both number of substitutions and number of indel events, indicating that its position is still uncertain, in common with the somewhat inconsistent placements of several other basal angiosperms, including Chloranthus, Ceratophyllum, and even Acorus. On the other hand, the combined five-gene analyses of Qiu et al. (1999, 2000)
, which included three other genera of Aristolochiaceae (Aristolochia, Saruma, and Thottea), placed Lactoris as sister to Aristolochia plus Thottea, and these three genera as sister to Asarum plus Saruma. All these genera were in turn sister to Piperaceae plus Saururaceae.
Endress (1994)
listed several morphological characters in favor of a close relationship between Lactoridaceae and Aristolochiaceae: presence of tepals, anthers strongly extrorse with a broad connective and almost sessile, stamens basally fused with the gynoecium, placenta linear, ovules anatropous, inflorescences with few, noncondensed flowers, one adaxial prophyll per flower, and pollen monosulcate. However, most of these characters are symplesiomorphies of the whole order Piperales, and therefore not indicative of relationships within the order. For example, adaxial prophylls and monosulcate pollen are commonly present in other Piperales, including Piperaceae and Saururaceae, and indeed in many other magnoliids. Linear placentae and anatropous ovules are also common in other magnoliids. Furthermore, although in Aristolochia stamens are basally fused with the gynoecium in Saruma, Asarum, and Thottea, which represent the probable basalmost clades of Aristolochiaceae (González, 1999a
), stamens are entirely free from the gynoecium. In contrast, in some Saururaceae stamens are fused with the gynoecium.
Perhaps the best morphological evidence for a sister group relationship between Lactoridaceae and Aristolochiaceae is the cymose inflorescence; otherwise, there are few consistent morphological synapomorphies between these taxa. A trimerous perianth links Lactoridaceae and Aristolochiaceae but is also found in monocotyledons. On the other hand, there are also strong links between Lactoridaceae and Saururaceae; for example, both Houttuynia and Lactoris have tenuinucellate ovules (Igersheim and Endress, 1998
; F. González and P. J. Rudall, unpublished data), a condition that is rare in other magnoliids. Development and morphology of stipules link Lactoris with Piperaceae and Saururaceae, although presence of stipules may be symplesiomorphic, with absence of stipules in Aristolochiaceae as a derived condition. No single character can independently test relationships. A revised morphological cladistic analysis, possibly combined with molecular data, may help to resolve this conundrum. This requires more comparative data on other taxa and will be the subject of future investigation.
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FOOTNOTES |
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4 Author for reprint requests: (fgonzg{at}ciencias.unal.edu.co
).
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