| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Structure and Development |
2Universidade Estadual de Campinas, Instituto de Biologia, Departamento de Botânica, Caixa Postal 6109, CEP 13083-970, Campinas, SP, Brazil; 3Department of Biology (Ecology, Evolution and Marine Biology), University of California, Santa Barbara, California 93106 USA
Received for publication October 23, 2001. Accepted for publication May 2, 2002.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: Exostyles • flower • Harleyodendron • Lecointea • Leguminosae • ontogeny • Papilionoideae • Zollernia
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Doyle, 1995
; Herendeen, 1995
; Doyle et al., 1997
, 2000
; Ireland, Pennington, and Preston, 2000
; Pennington et al., 2000
, 2001
) suggest that the tribe Swartzieae is polyphyletic and that some genera of this tribe are more closely related to Sophoreae pro parte than to other Swartzieae. These studies also support the basal position of tribes Swartzieae and Sophoreae pro parte in subfamily Papilionoideae. One group of Swartzieae sensu lato (s.l.) was designated as the Lecointea group by Polhill (1994)
, and it was resolved as a monophyletic clade by Herendeen (1995)
. Recently, however, Ireland, Pennington, and Preston (2000)
suggested that the Lecointea clade sensu Herendeen (1995)
is paraphyletic. The Lecointea clade ("lecointeoid" sensu Ireland, Pennington, and Preston, 2000
) retains Holocalyx, Lecointea, Zollernia with sophoroid Uribea, while a "vataireoid" clade combines Exostyles and Harleyodendron with sophoroid genera Sweetia, Luetzelburgia, and Vataireopsis.
The radially symmetrical flowers in some Dalbergieae, Sophoreae, and Swartzieae have been thought to be primitive among Papilionoideae, but Pennington et al. (2000)
suggested that they should be considered independent reversals and that at least nine such reversals from the papilionoid state have occurred.
Herendeen (1995)
, studying the phylogeny of the tribe Swartzieae (sensu Polhill, 1981
), verified two distinct groups of Swartzieae: the Swartzia clade including Swartzia, Aldina, Bocoa, Candolleodendron, Baphiopsis, Mildbraediodendron, and Cordyla plus the Sophoroid genera Baphia, Baphiastrum, Leucomphalos, Airyantha, Bowringia, and Dalhousiea, and the Lecointea clade including Exostyles, Harleyodendron, Holocalyx, Lecointea, and Zollernia. Herendeen asserted that these latter five taxa are more closely related to certain genera of Sophoreae s.l. such as Ateleia, Castanospermum, Luetzelburgia, and Myroxylon, than to the other genera of Swartzieae.
Floral ontogeny has been studied in other Swartzieae sensu Polhill (1994)
(on Ateleia, Tucker [1990
]; on Swartzia, Tucker [1987
]; Tucker [unpublished data] on Swartzia, Cyathostegia, Baphiopsis, Mildbraediodendron) and Sophoreae sensu Polhill (1994)
(Tucker, 1993
, 1994
, 2002
). None of the Lecointea clade sensu Herendeen (1995)
has been available for floral ontogenetic study until now. Ontogenetic features, such as presence of a ring meristem, have proved significant systematically, so it is important to study taxa of the Lecointea clade to provide additional significant evidence bearing on its evolutionary relationships to other groups of Swartzieae and Sophoreae.
The first and third authors have studied the taxonomy of Exostyles (unpublished data), and Zollernia (Mansano and Tozzi, 1999a
, b
) and are currently carrying out molecular studies on the group.
The taxa of the Lecointea clade sensu Herendeen (1995)
have a nonpapilionoid flower with five petals and ten stamens, but the flowers show considerable variation in other respects: radial symmetry in most taxa but zygomorphy in Zollernia; a hypanthium present in Exostyles, Holocalyx, and Lecointea but missing in the other two; a persistent, entire calyx tube in Lecointea, compared to irregular splitting and reflexing of calyx lobes in the other taxa. To determine the basis for morphological variation, this study will compare flower development among taxa of the Lecointea clade sensu Herendeen (1995)
. Four genera will be studied: Exostyles, Harleyodendron, Lecointea, and Zollernia. The material of Holocalyx is not sufficient for a complete ontogenetic series; more work is planned on it when material can be obtained. Major aims will include determining whether morphological and developmental evidence support monophyly of this group of taxa or whether their separation into distinct clades is warranted.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
The four species studied include Exostyles venusta Schott: Mansano 55, Brazil, Espírito Santo, Linhares, Reserva Florestal da Companhia Vale do Rio Doce; Harleyodendron unifoliolatum R. S. Cowan: Mansano 63, Brazil, Bahia, Una, Reserva Biológica de Una; Lecointea hatschbachii Barneby: Mansano 167, Brazil, Paraná, Adrianópolis, km. 15 da Estrada Turnas do Paraná—Adrinópolis; and Zollernia ilicifolia (Brongn.) Vogel: Mansano 50, Brazil, São Paulo, Campinas, Campus da UNICAMP. One species of each was considered representative because floral development in a genus usually does not vary significantly among species (see Tucker [1994
], which compares development of several species of Sophora). Identifications were made by the first author. Vouchers have been deposited in herbaria at CEPEC, CVRD, MBM, and UEC (Holmgren, Holmgren, and Barnet, 1990
). Liquid-preserved collections are held by the first author.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
), Venezuela and the Guianas. Zollernia ilicifolia Maximil. & Nees and Z. magnifica A. M. de Carvalho & R. C. Barneby were studied, but only Z. ilicifolia is described (Fig. 1A) since they are essentially alike in development. The paniculate racemes are positioned at the tips of the branches and have small, acutely tipped bracts (Fig. 2) subtending the flowers. Paired bracteoles persist at the base of each flower at the distal end of the short pedicel. Additional flower buds are initiated in the axils of the bracteoles below individual flowers, and order of opening of flowers is not strictly acropetal. Each flower (Fig. 1A) is 20–25 mm long, and its longitudinal axis is perpendicular to the pedicel. It has a short, zygomorphic calyx tube, which is tubular and encloses the bud as a sheath, with the tip arched adaxially. At anthesis the calyx splits irregularly and the tips reflex and then abscise, leaving a circular scar. Of the five petals, the vexillum is broader and outside the others. The petals are imbricate in bud. At anthesis the median adaxial and two lateral petals reflex, while the two keel petals enclose the stamens and gynoecium (Fig. 1A). The flower has 9–13 free stamens, varying in number on an individual inflorescence. The anthers are uniform, linear, basifixed with longitudinal dehiscence and with very short filaments. The gynoecium has an elongate stipe and an elongate cylindrical ovary. The style is short and subulate with a small, obliquely terminal stigma (Hutchinson, 1964
).
|
|
Before petal initiation the floral apex is convex and pentagonal (Figs. 8 and 11). The petal initiation is simultaneous (Fig. 12), and the carpel primordium is initiated at the same time (Figs. 12 and 13) as a central mound (in contrast to the low-convex apex in Fig. 11).
The two whorls of stamens overlap in time of initiation almost completely. In Fig. 13 two antepetalous and two antesepalous stamen primordia have initiated. In Figs. 15 and 16 one can see that, despite the antepetalous stamens beginning initiation first, they are the last whorl to be completed. The antesepalous stamen primordia are larger than the antepetalous ones. The abaxial stamens initiate first in each whorl (Figs. 13–15). After all stamens have initiated, the antesepalous ones are larger and well defined while the antepetalous ones are smaller and still show a size difference between the abaxial and adaxial primordia.
Organ development in Zollernia ilicifolia
At midstage of development all of the organs have initiated and organs within each whorl are equal in size (Figs. 17 and 18). Bracteoles become trichome-covered but do not surround the flower bud (Fig. 10). The sepal lobes become subequal, acute-tipped, and valvate at midstage (Fig. 10), when they close over the summit of the flower. The lobes remain free in 1–2-mm buds, but later the tips are lightly coherent, perhaps by interlocking hairs. The calyx tube, the continuous region below the level of the sepal lobes, elongates by intercalary growth; it is 0.5 mm long in a 1 mm long bud, 2.5 mm long in a 3 mm long bud, and 5.5 mm long in a 6 mm long bud. The calyx becomes zygomorphic in the 6-mm bud as the tip curves to one side (not shown).
|
The carpel is at first a convex dome (Figs. 17 and 18). The carpel cleft begins adaxially (Figs. 19 and 20) and deepens gradually (Fig. 21). The carpel margins are appressed early (Figs. 21–23) and become fused. In many flowers one margin grows more than the other so that the cleft is not exactly in the median plane (not shown). In shape the carpel becomes tapered slightly at the base (Figs. 26 and 27). Trichomes start to form after carpel fusion (Figs. 22 and 23) and later become abundant (Figs. 26 and 27). At maturity the gynoecium (Fig. 31) is about 12–14 mm long, has an elongate stipe, a long cylindrical ovary, an elongate style that is upturned distally, and a punctiform stigma (Figs. 31 and 32).
Stamen primordia are uniform in size in each whorl (Figs. 19 and 20). Most flowers have five stamens in each whorl, but some flowers have as many as 13, with eight in the outer stamen whorl (not shown). The antesepalous stamen primordia heighten first, before the others (Figs. 21 and 24). Anther differentiation begins by a height of about 340 µm, when the bases become narrowed to form the filaments. The microsporangia begin to differentiate at the same time (Fig. 22). Median and lateral grooves become visible in the anthers at a height of about 800 µm (Fig. 26) at the same time that hair formation begins on the anthers.
The antepetalous stamen primordia start to enlarge (Fig. 22) at the same time that anther formation is beginning in the antesepalous whorl. Anthers and filaments start to differentiate in the antepetalous stamen primordia, and they develop marginal trichomes (Figs. 25 and 28) by a height of about 460 µm. At anthesis, the stamens are uniform, with the anthers far exceeding the filaments in length (Figs. 30 and 31).
2. Harleyodendron unifoliolatum R. S. Cowan
Organography
Harleyodendron is a monotypic genus; H. unifoliolatum R. S. Cowan is a small tree of Bahia, Brazil (Cowan, 1979
, 1981
; Lewis, 1987
). The racemose inflorescences contain about 20 flowers in a helical arrangement but clustered toward the inflorescence tip. Individual flower buds are globose, radially symmetrical, and about 20 mm high on a short pedicel before anthesis. Bracteoles are represented by two small wartlike protuberances near the base of the pedicel. The calyx tube is tubular in bud; at anthesis the lobes split into four or five segments and reflex (Fig. 1B). The five petals are broadly ovate and tapered basally, imbricate in bud and flared outward at anthesis (Fig. 1B). The perianth is about 22–30 mm wide at anthesis. The ten uniform stamens have elongate basifixed anthers held together in a domelike structure by interlocking hairs on the sides of the anthers (Fig. 1B). The stamen filaments are very short and are free. The gynoecium has a short broad stipe, a short cylindrical ovary, an elongate style that often is slightly angled, and a punctiform stigma. There is no hypanthium.
Organogeny in Harleyodendron
The flower buds are initiated singly in axils of bracts produced in helical order in the raceme (not shown). The floral apex is broader transversally than sagittally (Fig. 33). Two bracteoles are initiated on the floral apex in succession (Figs. 34 and 35). The first sepal primordium is initiated abaxially and medianly (Fig. 35). These figures also show an adaxial ridge (Figs. 35 and 36) that is not a primordium but rather a compression mark. Two lateral sepal primordia and one adaxial sepal primordium are initiated next (Figs. 36 and 37). The fifth sepal initiates soon thereafter (not shown). A shallow ridge in Fig. 37 suggests the inception of a calyx tube, although later stages do not show it.
|
|
Another way of describing development would be that there are five petal-stamen common primordia. The primordia in Figs. 39–41 are relatively broad and each may later subdivide into a petal and an antepetalous stamen (Figs. 42, 45, and 46). In support of this interpretation, the petal primordia in Fig. 49 appear as shoulders on the antepetalous stamen primordia and are not distinct. In some flowers all petals and stamens are raised on a common base (Figs. 47 and 49), but this common base is not visible in all flowers or in later stages. The petal primordia later become distinct mounds (Fig. 50).
Organ development in Harleyodendron
Bracts and bracteoles remain minute as the flower buds enlarge. The bracteoles are sessile in a 4 mm high bud and appear later as wart-like protuberances on the pedicel below the bud (Fig. 1B). The five sepal primordia converge over the rest of the flower, but thereafter most growth consists of the calyx cup growing by intercalary growth as an enlarging, closed cylinder. The sepal lobe tips are not visible in buds 4 mm high or larger. The flower buds reach a height of about 13 mm with a pedicel approximately equal in length, before the bud opens.
Petal primordia start to grow marginally at a height of about 220 µm (Fig. 52). They arch upward and inward over the other organs of the flower (Fig. 53). When the petals are about 1.3 mm high they become erect and gradually overtop the other organs. The petals are nearly in contact but do not overlap at this time. The petals begin to overlap at the margins when they are about 1.3 mm high (Figs. 53–56), and the bud is about 4 mm high. The overlap increases to produce an imbricate corolla.
By midstage the antesepalous stamens are larger than the antepetalous ones (Figs. 50 and 52). All the stamens in a whorl are the same size. The antesepalous stamen primordia start to differentiate by distal enlargement (Fig. 52). The stages of microsporangial formation are not included, but the median adaxial grooves are visible in Fig. 54 (at arrow). The anthers elongate greatly and become falcate, but the filaments remain short with a flared base (Figs. 59 and 60). Trichomes become abundant on the sides of the anthers (Fig. 58), causing them to adhere as a dome-shaped cap at anthesis (Fig. 1B).
The carpel primordium heightens and develops a style and stigma (Figs. 55 and 57). The ovary becomes covered by dense trichomes while the style remains glabrous (Fig. 60). Neither hypanthium nor stipe forms. The ovary contains more than 20 ovules in two rows (Fig. 61). The stigma is punctiform and the suture remains open at the tip (Fig. 62). Some functionally male flowers were seen with a highly reduced gynoecium.
3. Exostyles venusta Schott ex Spreng
Organography
Exostyles includes four species (one of which is undescribed) of small trees native to Brazil (Mansano, 1997
). Exostyles venusta has short, lax, axillary racemes of rose, magenta, or purple flowers. Each flower is pedicellate and up to 3 cm long; two tiny bracteoles persist on the pedicel near the flower base. The calyx tube is elongate-turbinate (Fig. 1C; Hutchinson, 1964
) and encloses the bud as a sheath. At anthesis the calyx splits into two or three segments which reflex and curl revolutely (Fig. 1C).
The five petals remain erect and imbricate; each has a claw and an ovate limb (Fig. 87). Although Herendeen (1995)
reports that the uppermost (vexillary) petal is innermost, we found petal aestivation to vary considerably. Of ten flowers examined, seven had the vexillary petal innermost, in two it was outermost, and in one the vexillary petal overlapped a lateral petal on one side and was itself overlapped on the other side. Altogether, we found six different aestivation patterns among the ten flowers examined.
|
Organogeny in Exostyles
The racemes have helical order of bracts and flowers. The floral apex first initiates a pair of bracteoles laterally and approximately at the same time (Figs. 63 and 64). Sepal initiation is unidirectional, beginning with the first sepal primordium initiating medianly on the abaxial side (Fig. 65). The next two sepal primordia are initiated laterally, closely adjacent to the first sepal (Fig. 66), and the last two sepals are initiated adaxially, one slightly ahead of the other in time (Fig. 67). The post-sepal floral apex is pentagonal with five radiating ridges (Fig. 68) from sepals appressing it.
|
Antepetalous stamen primordia are the next organs to be initiated, centripetal to each of the petal primordia (Fig. 70, at arrowheads). They start on the abaxial side and initiate in unidirectional order (Fig. 70). The carpel primordium next is initiated centrally on the floral apex (Figs. 71 and 72) while the antepetalous stamen primordia become more evident. In side view (Fig. 72) the antepetalous stamen primordia are clearly visible, while there is only a suggestion of an antesepalous primordium (at arrowhead, Fig. 72).
The antesepalous stamen primordia overlap in time of initiation with the antepetalous stamen primordia. In Figs. 73 and 74, all of the antepetalous stamen primordia have initiated and are larger than any of the antesepalous ones. The antesepalous stamen primordia initiate in bidirectional order (Figs. 73, 74, and 76): the two laterals appear to initiate first, followed by the median abaxial one and the adaxial pair (Figs. 74 and 75).
The carpel is at first a convex dome (Figs. 71–74) and gradually becomes flattened on the adaxial side (Fig. 76). An adaxial cleft is first visible in Fig. 77, concurrently with initiation of the last antesepalous stamen primordia.
Organ development in Exostyles
Bracts and bracteoles become narrowly linear and stiff, with spiny margins. The sepal lobes enlarge and converge over the rest of the flower by midstage. Thereafter, most of calyx enlargement takes place in the calyx tube, the cylindrical region of intercalary growth below the lobes that raises the lobes upward. The lobes grow but little, from a length of about 400 µm in a 1 mm long bud to about 500 µm in a 5 mm long bud (not illustrated).
Petal primordia remain short and undifferentiated when about 100 µm high (Figs. 79 and 81) while the stamens and carpel are enlarging and starting to differentiate. The petals start to grow marginally at a height of about 350 µm and elongate to a length of about 1–1.2 mm, still not touching one another, in a bud 5 mm high. They are still widely separated from each other at a height of 1–1.2 mm long. The margins start to approach one another at a petal height of 2.2–3.0 mm (Figs. 82 and 86) in a bud 7 mm high. By a height of 2.7 mm (Figs. 87 and 88) the petals overlap one another at their margins and taper basally as a short claw. The overlap increases as the petals enlarge.
Although the antepetalous stamens initiate before the antesepalous ones, all are approximately equal in size by midstage (Figs. 77–79). As they start to elongate, the antepetalous stamens are higher than the antesepalous ones (Fig. 81). Microsporangial development appears to occur concurrently in stamens of both whorls (Figs. 82, 84, and 85). The stamen primordia arch inward in both, and sporangium formation is not easily seen from the outside (Fig. 82). The stamens of the two whorls differ somewhat in shape at least at some stages; the antepetalous ones are truncate terminally, while the antesepalous ones are acutely tipped (Fig. 86). Median dorsal and lateral grooves are present in stamens of both whorls at about the same time (Figs. 82, 84, and 85). In the mature flowers the anthers are very long and the filaments are relatively short (Fig. 86). The tips of the anther connectives become acutely tapered (Figs. 87 and 89). The anthers are glabrous and flare outward as the bud begins to open (Fig. 88).
As the carpel primordium enlarges, one margin may grow more than the other (Fig. 80) so that the cleft becomes slightly obliquely oriented. The carpel margins in some flower buds remain open while ovule initiation begins (Figs. 82 and 83). The carpel at this time is about 575 µm in height. By a height of about 800 µm, the carpellary margins become appressed and then fused (Fig. 85). The gynoecium enlarges as a straight, narrow cylinder (Fig. 89), with a stipe (Fig. 89) and a punctiform stigma (Fig. 90). The gynoecium is attached centrally at the base of a short hypanthium (Fig. 89).
4. Lecointea hatschbachii R. C. Barneby
Organography
Lecointea includes six species of trees native to South America (Barneby, 1992
). We studied material of Lecointea hatschbachii. The inflorescences are small racemes of 9–15 flowers. A raceme may produce a flower-bearing branch near its base, or several racemes may be clustered at adjacent nodes. Each flower (Fig. 1D) is about 8 mm long, with the campanulate calyx tube to 4 mm long. In bud the calyx tube encloses the rest of the flower. In a mature flower there are 4–5 calyx lobes. The five petals (Fig. 1D) are erect, imbricate in bud, clawed, inconspicuous, and early deciduous. One, the vexillary or uppermost petal, is broader than the others and overlaps the lateral petals. The 9–10 stamens are uniform, free, long-exserted, with small, longitudinally dehiscing, basifixed anthers (Fig. 1D). The ovary is stipitate, with a straight or slightly curved stout style exserted in bud and a small obliquely terminal stigma (personal observation).
Organogeny in Lecointea
The floral apex is wide transversally and narrow sagittally before bracteole initiation (Fig. 91). Two bracteoles are initiated on the apex (Fig. 92). The first sepal primordium is initiated abaxially but not medianly (Figs. 93, 94). The second sepal primordium is initiated beside the first (Fig. 94). In some flowers there appear to be two sepal primordia rather than three on the abaxial side (Fig. 95). The other three sepal primordia are then initiated laterally and on the adaxial side (Figs. 95 and 96). The flower of Lecointea in Fig. 95 has six sepals; the abaxial sepal is replaced by two sepals that initiate successively. Six sepals (instead of five) were occasionally found in Lecointea. Of 12 flowers examined, eight had five sepals, three had four, and just one had six sepals. So, we can consider the six-sepaled condition rare in Lecointea. Altogether, we found three different numbers of sepals among the 12 flowers examined, in spite of five sepals being the most common number. Sepal positions are atypical for a papilionoid in that the adaxial sepal in a five-sepalate flower is not median (Fig. 96).
|
|
The antesepalous stamens overlap in time of initiation with the antepetalous stamens. The first antesepalous stamen primordia are lateral (one in Fig. 102, two in Fig. 103, and five in Fig. 104). Organ initiation is bidirectional with the median abaxial and two adaxial antesepalous stamens initiating last (Fig. 105). The stamen primordia differ in size immediately after all are initiated (Figs. 106 and 107). Total stamen number at anthesis varies (7–13) from flower to flower (not shown).
Organ development in Lecointea
Sepal lobes elongate and converge over the rest of the flower by midstage. The calyx tube, the cylindrical region below the sepal lobes, starts to elongate by intercalary growth and encloses the bud as a sheath by the time it is 1.5 mm high. The lobes remain about 500 µm high from this stage onward while the calyx tube enlarges greatly in the pre-anthetic bud (Fig. 117) to about 5.5 mm high. At anthesis the calyx cup is flaring with short broad lobes and is tomentose externally (Fig. 118).
The petals remain short and undifferentiated (Figs. 108–112) while the other organs heighten and begin differentiation. The petals start marginal growth at a height of about 275 µm (Figs. 113 and 114). The petals increase further in height to about 1 mm high in a bud 3.7 mm high (Fig. 115), but still do not overlap. The petal margins meet and overlap at a height of 2 mm, when the bud is 5.5 mm high.
The antesepalous stamen primordia start to elongate first (Figs. 111 and 112). Dorsal grooves become visible (Figs. 111 and 112). Anthers and filaments are distinguishable at a height of about 600 µm (Fig. 113). Trichome formation begins near the anther tips at the same time in both antesepalous and antepetalous anthers. Anthers are basifixed, although the microsporangia extend down below the point of the filament attachment (Fig. 115). In an open flower the filaments have elongated greatly (Fig. 1D).
The antepetalous stamens start to elongate later (Fig. 112) than the antesepalous stamens but become equal in length and degree of differentiation by a high of about 500 µm (Fig. 113). Hair formation begins concurrently in both stamen whorls and increases in both to the same degree (Figs. 114–116).
The carpel cleft closes at the same time that hair formation starts on the carpel primordium (Fig. 112). A gynoecium covered with trichomes is seen in Fig. 117. The gynoecium at maturity has a stipe, a trichome-covered ovary, an elongate style, and a punctiform stigma (Figs. 119 and 120). The gynoecium is central in the short hypanthium in the mature flower (Fig. 119).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
the first sepal is abaxial, followed by two laterals and lastly two adaxial sepals (as in all papilionoids investigated so far). The flower then has a single median abaxial sepal and two on the adaxial side. It is possible that Harleyodendron unifoliolatum and Lecointea hatschbachii have common primordia on which petals and antepetalous stamens are initiated. In the other lecointeoid taxa (as in most papilionoids studied) petal primordia are initiated separately from the antepetalous stamen primordia.
Also unusual is the pattern of stamen initiation. In Zollernia ilicifolia, Exostyles venusta, and Lecointea hatschbachii, the antepetalous stamen primordia start to initiate earlier than the antesepalous ones. In Harleyodendron unifoliolatum members of the antesepalous stamen whorl start to initiate before the antepetalous whorl.
Petal aestivation is unstable among several taxa of the Lecointea group (Table 1). Most papilionoid flowers have descending cochlear aestivation, in sharp contrast to most caesalpinioids that have ascending cochlear aestivation. Systematists have occasionally noted exceptions to these generalizations: Cadia (Sophoreae; van der Maesen, 1970
) and Exostyles (Swartzieae s.l.; Pennington et al., 2000
). Both genera have petal aestivation varying from flower to flower. In our studies, we have also found variable petal aestivation in Exostyles venusta, Harleyodendron unifoliolatum, and Lecointea hatschbachii.
The carpel margins in some flower buds of Exostyles remain open while ovule initiation begins. The latter sequence is uncommon in legumes (Tucker and Kantz, 2001
).
Unusual developmental features
The flowers of the Lecointea clade sensu Herendeen (1995)
are relatively unspecialized, with a calyx undivided in bud, the full complement of floral organs (about 21), and little or no fusion among parts (except by interlocking anther hairs as in Harleyodendron). We have examined scanning electron micrographs of Exostyles venusta, Harleyodendron unifoliolatum, Holocalyx glaziovii, Lecointea hatschbachii, and Zollernia ilicifolia. Most have radial symmetry except Zollernia, in which zygomorphy is achieved by changes late in development: two petals remain erect and cradle the stamens and gynoecium, while the other three petals are reflexed. The flowers are also laterally inclined. Zygomorphy among most Papilionoideae is expressed earlier than this during floral development, as soon as all organs have been initiated (in Sophoreae [Tucker, 1993
, 1994
], Vicieae [Tucker, 1989
], and Psoraleeae [Tucker and Stirton, 1991
]).
Stamen initiation is unidirectional in each stamen whorl (except bidirectional in the antesepalous whorl in Exostyles and Lecointea) and starts on the abaxial side of the bud in all. The stamens of both whorls later become equalized in size and intercalated into a single whorl at anthesis. This is the first report of antepetalous stamens initiating before the antesepalous ones in legumes, so it may provide synapomorphies to substantiate the close affinity among the taxa of the Lecointea clade.
Late-stage developmental changes
In late floral development, several changes occur to distinguish the lecointeoid taxa (Table 1). Sepal lobes reflex in Exostyles, Harleyodendron, and Zollernia, but remain erect in the other taxa (Table 1). Shifts in relative growth of the receptacle produce a hypanthium in Exostyles venusta, Holocalyx glaziovii, and Lecointea hatschbachii, but this shift does not occur in the other taxa. The carpel base elongates as a stipe in all except Harleyodendron; the gynoecium is centrally attached on the receptacle in all (in contrast to adaxial attachment in many Caesalpinioideae). Trichomes form along the sides of the anthers in Harleyodendron, holding the anthers together as a domelike cylinder quite unlike most legume flowers. Trichomes also form laterally on anthers in Lecointea and Zollernia but do not hold them together at anthesis. In Lecointea they are concentrated at the anther tips. Stamen trichomes in most other papilionoid legumes are rare on anthers and tend to be located around the base of the filaments. Trichomes on the anther tips are also found on many species of Indigofera (Gwilym Lewis, Royal Botanic Gardens, Kew, UK, personal communication) and on anthers of species of Bauhinia and Senna (Tucker, 1996
).
Comparisons among the Lecointeoid group, Sophoreae, and Swartzieae
As the relationships in Swartzieae and Sophoreae are currently in a state of flux, it is worthwhile to review developmental similarities and differences that might help to understand the alignment of the Lecointea clade sensu Herendeen (1995)
with other subgroups of these two tribes. Floral ontogenies are available for several taxa of Sophoreae (Castanospermum and Myroxylon, Tucker [1993
]; Sophora, Tucker [1994
]), Cadia, Tucker (2002)
and several taxa of Swartzieae (Ateleia herbert-smithii, Tucker [1990
]; Baphiopsis, Bobgunnia, Cyathostegia, Mildbraediodendron, and Swartzia, Tucker [unpublished data]).
The presence of a ring meristem is an important character state among certain Swartzieae s.l. (in Ateleia, Swartzia, Cyathostegia, and Mildbraediodendron). This structure functions in stamen initiation and is usually associated with proliferation in stamen number (although most Ateleia have only ten stamens). No sign of a ring meristem was found among the Lecointea group taxa.
Presence of common petal-stamen primordia in some of the Lecointea group is unique so far among legumes (although not uncommon in some other plant families). Initiation of stamens and petals in Pisum sativum (Tucker, 1989
) included common primordia. There are strong supports in morphology and in DNA data to consider this shared feature as a convergence.
The Lecointea group of Herendeen (1995)
shares with Sophoreae s.l. the 21 floral organs per flower, little or no cellular fusion among organs, uniform petal and stamen morphology within each whorl, and largely unidirectional order of initiation in floral whorls. Molecular data (Ireland, Pennington, and Preston, 2000
) have shown that the earlier concept of the Lecointea clade (Herendeen, 1995
) needs to be redefined. The phylogeny of basal Papilionoideae is still unclear in many clades, but with more and more genes being sequenced relationships appear more stable. Floral ontogeny can provide valuable information to complement molecular data in cladistic analysis.
Cowan (1981)
placed Exostyles, Harleyodendron, Lecointea, and Zollernia in Swartzieae, one of the most basal papilionoid tribes (Polhill, 1994
; Doyle et al., 1997
; Pennington et al., 2001
), and placed Holocalyx in tribe Sophoreae, also near the base among papilionoids (Pennington et al., 2000
). The Lecointea group of papilionoid genera as proposed by Herendeen (1995)
was based on morphological evidence and was considered monophyletic at that time. It includes Exostyles, Harleyodendron, Holocalyx, Lecointea, and Zollernia and is sister to a clade including several genera of woody Sophoreae. More recent phylogenetic analyses based on molecular data (Ireland, Pennington, and Preston, 2000
; Pennington et al., 2001
) placed Harleyodendron and Exostyles (with several taxa of Sophoreae) in the Vataireoid clade, and Holocalyx, Lecointea, and Zollernia in a clade with Uribea of the Sophoreae. According to Pennington et al. the Lecointea clade sensu Herendeen (1995)
is not a natural group, but we have used this name for convenience and because we have found that the four taxa share a significant assemblage of ontogenetic features.
Despite the work of Pennington et al. (2001)
, relationships among the taxa of basal Papilionoideae (such as Zollernia and Lecointea) with the other genera are still unclear. Harleyodendron, Exostyles, Sweetia, Luetzelburgia, Vatairea, and Vataireopsis are resolved together in the vataireoid clade with a high bootstrap value, but Zollernia and Lecointea are not included in this clade in spite of ontogenetic and other similarities. Our ontogenetic data give us good evidence for thinking that more molecular analyses may support the close phylogenetic relationships of Zollernia and Lecointea with the vataireoid clade of Pennington et al. (2001)
.
The four taxa studied here have many character states in common, including some unique ones such as antepetalous stamens initiating first in Exostyles and Lecointea, yet they are placed in two different clades in Pennington's analysis. This conflict suggests that more basal Papilionoideae genera have to be studied to help us to understand the origin and evolutionary relationships of the five genera of the Lecointea clade and the significance of the unusual ontogenetic character states that they share.
|
FOOTNOTES |
|---|
4 Current address: Botanical Garden, Rio de Janeiro, Brazil (vmansano{at}hotmail.com )
5 Author for reprint requests (tucker{at}lifesci.ucsb.edu
)
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Carvalho A. M. R. C. Barneby 1993 The genus Zollernia (Fabaceae: Swartzieae) in Brazil. Brittonia 45: 208-212[CrossRef][ISI]
Cowan R. S. 1979 Harleyodendron, a new genus of Leguminosae (Swartzieae). Brittonia 31: 72-78[CrossRef][ISI]
Cowan R. S. 1981 Swartzieae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, Part 1, 209–212. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Doyle J. J. 1995 DNA data and legume phylogeny: a progress report. In M. D. Crisp and J. J. Doyle [eds.], Advances in legume systematics, Part 7, Phylogeny, 11–30. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Doyle J. J. J. A. Chappill C. D. Bailey T. Kajita 2000 Towards a comprehensive phylogeny of legumes: evidence from rbcL sequences and non-molecular data. In P. S. Herendeen and A. Bruneau [eds.], Advances in legume systematics, Part 9, 1–20. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Doyle J. J. J. L. Doyle J. A. Ballenger E. E. Dickson T. Kajita H. Ohashi 1997 A phylogeny of the chloroplast gene rbcL in the Leguminosae: taxonomic correlations and insights into the evolution of nodulation. American Journal of Botany 84: 541-554[Abstract]
Herendeen P. S. 1995 Phylogenetic relationships of the tribe Swartzieae. In M. D. Crisp and J. J. Doyle [eds.], Advances in legume systematics, Part 7, Phylogeny, 123–132. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Holmgren P. K. N. H. Holmgren L. C. Barnet [eds.] 1990 Index Herbariorum, Part 1: the herbaria of the world, 8th ed. New York Botanical Garden, Bronx, New York, USA
Hutchinson J. 1964 The genera of flowering plants (Angiospermae), vol. 1, Dicotyledones. Oxford University Press, Oxford, UK
Ireland H. R. T. Pennington J. Preston 2000 Molecular systematics of the Swartzieae. In P. S. Herendeen and A. Bruneau [eds.], Advances in legume systematics, Part 9, 217–231. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Lewis G. P. 1987 Legumes of Bahia. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Mansano V. F. 1997 Estudos taxonômicos da tribo Swartzieae (DC.) Benth. (Leguminosae-Papilionoideae) no Sudeste do Brasil. Master's thesis, State University of Campinas, Brazil
Mansano V. F. A. M. G. A. Tozzi 1999a The taxonomy of some Swartzieae (Leguminosae, subfam. Papilionoideae) from southeastern Brazil. Brittonia 51: 149-158[CrossRef][ISI]
Mansano V. F. A. M. G. A. Tozzi 1999b Distribuição geográfica, ambiente preferencial e centros de diversidade dos membros da tribo Swartzieae na região sudeste do Brasil. Revista Brasileira de Botânica 22: 249-257
Pennington R. T. B. B. Klitgaard H. Ireland M. Lavin 2000 New insights into floral evolution of basal papilionoids from molecular phylogenies. In P. S. Herendeen and A. Bruneau [eds.], Advances in legume systematics, Part 9, 233–248. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Pennington R. T. M. Lavin H. Ireland B. Klitgaard J. Preston J. Hu 2001 Phylogenetic relationships of basal papilionoid legumes based upon sequences of chloroplast trnL intron. Systematic Botany 26: 537-556[ISI]
Polhill R. M. 1981 Papilionoideae. In R. M. Polhill and P. H. Raven [eds.], Advances in legume systematics, Part 1, 1–26. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Polhill R. M. 1994 Complete synopsis of legume genera. In F. A. Bisby, J. Buckingham, and J. B. Harborne [eds.], Phytochemical dictionary of the Leguminosae 1, xlix–liv. Chapman and Hall, New York, New York, USA
Tucker S. C. 1987 Stamen proliferation in Swartzia macrosema, a legume considered transitional between subfamilies Caesalpinioideae and Papilionoideae. American Journal of Botany 74: 627 (Abstract)
Tucker S. C. 1989 Overlapping organ initiation and common primordia in flowers of Pisum sativum (Leguminosae: Papilionoideae). American Journal of Botany 76: 714-729[CrossRef][ISI]
Tucker S. C. 1990 Loss of floral organs in Ateleia (Leguminosae: Papilionoideae: Sophoreae). American Journal of Botany 77: 750-761[CrossRef][ISI]
Tucker S. C. 1993 Floral ontogeny in Sophoreae (Leguminosae: Papilionoideae). 1. Myroxylon (Myroxylon group) and Castanospermum (Angylocalyx group). American Journal of Botany 80: 65-75
Tucker S. C. 1994 Floral ontogeny in Sophoreae (Leguminosae: Papilionoideae). II. Sophora (Sophora group). American Journal of Botany 81: 368-380[CrossRef][ISI]
Tucker S. C. 1996 Stamen structure and development in legumes, with emphasis on poricidal stamens of Caesalpinioid tribe Cassieae. In W. G. D'Arcy and R. C. Keating [eds.], The anther: form, function, and phylogeny, 236–254. Cambridge University Press, Cambridge, UK
Tucker S. C. 2002 Floral ontogeny in Sophoreae (Leguminosae: Papilionoideae). III. Cadia purpurea with radial symmetry and random petal aestivation. American Journal of Botany 89: 748-757
