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Plant Physiol, March 2003, Vol. 131, pp. 911-926
UPDATE ON FLORAL DEVELOPMENT
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INTRODUCTION |
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 TOP
 INTRODUCTION
 SUBFAMILY CAESALPINIOIDEAE
SUBFAMILY MIMOSOIDEAE
SUBFAMILY PAPILIONOIDEAE
WHAT CAN WE LEARN...
LITERATURE CITED
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Species of flowering plants are most reliably identified by their flowers, the sexually reproductive organs. A flower is similar to a vegetative short shoot (lacking appreciable internodes) that bears four kinds of laterally attached organs in successive whorls: sepals, petals, stamens, and carpels. Significant floral distinctions among plant families include symmetry, whether organs are organized in whorls or helically, number of parts per whorl, carpel position relative to the surrounding organs, fusion among organs within a whorl or between different whorls, and whether both male and female organs are present in the same flower.
A flower, like a vegetative shoot, has a terminal floral apical meristem that initiates organs laterally, usually in acropetal succession (although exceptions are common in some taxa): sepals first, followed by petals, stamens, and carpels. Because each flower lives for a very short time, the floral apical meristem is determinate, meaning that it ceases activity after a certain number of organs have initiated. Vegetative apical meristems, in contrast, are usually indeterminate, continuing to initiate new organs, such as leaves, indefinitely.
In this Update, I will focus on flowers of the plant family
Fabaceae. This family comprises three large subfamilies:
Caesalpinioideae, Mimosoideae, and Papilionoideae. Although the family
is widely accepted as monophyletic (Chappill, 1995
;
Doyle, 1995; Doyle et al., 2000), these
subfamilies differ greatly in floral symmetry. Fabaceae is a large
family (about 700 genera and about 18,000 species), and is nearly
ubiquitous over temperate and tropical parts of the world
(Polhill and Raven, 1981). Many agronomically important
plants are members of this family. The information base is huge, and
the taxa are relatively easy to obtain.
Most legume flowers share a pentamerous ground plan with five sepals,
five petals, two whorls of five stamens each, and a single carpel, or
21 organs in all. Members of each of the four whorls alternate with
those of the preceding whorl. The single carpel at the center of the
flower is superior in position; i.e. its base is attached at the same
level as those of the sepals, petals, and stamens. The carpel
differentiates as a gynoecium with ovary, style, and stigma, and
eventually forms a pod-like fruit. Although most people think of
papilionoid-type flowers (or flag flowers; Fig.
1A, F) as representative of legumes, many legume taxa differ markedly from this type of flower (Fig. 1, B-E;
Tucker, 1987a).
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Superimposed upon this basic floral ground plan are prominent differences among the three legume subfamilies. These include differences in flower position in the inflorescence, floral symmetry, sepal and petal aestivation, fusion, loss or increase of floral organ number, heterogeneous organs within a whorl, unisexual flowers, etc. Ontogenetic differences among the subfamilies are of particular interest.
With this background in mind, I will describe the details of floral
development in each subfamily of legumes. These details are necessary
as a foundation for molecular studies on legume flower development
and organ identity relative to the ABC model (Meyerowitz
et al., 1991; Irish, 1999; Jack,
2001).
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SUBFAMILY CAESALPINIOIDEAE |
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TOP
INTRODUCTION
SUBFAMILY CAESALPINIOIDEAE
SUBFAMILY MIMOSOIDEAE
SUBFAMILY PAPILIONOIDEAE
WHAT CAN WE LEARN...
LITERATURE CITED
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The subfamily Caesalpinioideae encompasses 170 genera and about
3,000 species. It has a basal position in phylogenetic schemes (Doyle, 1995; Doyle et al., 2000;
Bruneau et al., 2001) and is highly diverse in floral
form and ontogeny. It is currently divided into four or five tribes:
Cercideae, Caesalpinieae, Cassieae, and Detarieae, with Macrolobieae
(derived from within Detarieae) recently gaining acceptance.
Inflorescences
Caesalpinioid inflorescences are usually racemes or panicles,
although solitary flowers and cymes occur more often than in either of
the other subfamilies. A raceme, as in Senna didymobotrya (Fres.) Irwin & Barn. (Fig. 2A; Tucker,
1996), is the most common kind of inflorescence among legumes. Racemes,
together with panicles, spikes, and some umbels, have a terminal apical
meristem that grows indeterminately and initiates bracts (modified
leaves) in acropetal succession along the inflorescence axis. A single
floral bud is initiated in the axil of each bract. A pair of bracteoles (reduced leafy organs) is usually produced below each flower. Developmental differences distinguish variations on the raceme, e.g. a
spike has flowers that lack pedicels and are crowded along the axis
without appreciable internodes, and a panicle has second order branches
along the first order axis. Racemes of caesalpinioids (Fig. 2A) show
successive, acropetal initiation and development among the flowers. In
other words, each inflorescence includes flowers of many ages, with the
oldest at the bottom and the younger ones above.
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A cymose inflorescence (Fig. 2B, Chamaecrista nictitans L. Moensch) has determinate growth, with a terminal flower forming first,
followed by younger flowers in the axils of two bracteoles that are
located below the terminal flower. Because every flower in a cyme has
bracteoles, the pattern of successive flower initiation in bracteole
axils can be repeated indefinitely. Cymes are found in Dialium
guineense Willd. (Tucker, 1998), Gleditsia
triacanthos (Tucker, 1991), and Poeppigia
procera Presl. (Kantz, 1996) among caesalpinioids.
Solitary flowers, each subtended by a foliage leaf, occur in the
caesalpinioid Petalostylis labicheoides R. Br.
(Tucker, 1998).
Symmetry
Floral symmetry among Caesalpinioideae is highly variable,
reflecting the fact that the subfamily is basal and polyphyletic, based
on molecular phylogenies (Doyle, 1995; Doyle et
al., 2000). Most caesalpinioid flowers are radially symmetrical
through midstage of development, when all organs have formed but have
not yet differentiated. In radial symmetry (Fig. 2C), an object can be
bisected along any radius to produce two halves that are mirror images.
Radial symmetry persists to anthesis in most taxa of tribe
Caesalpinieae, e.g. Gleditsia triacanthos (Tucker,
1991), and in selected members of the other tribes, e.g.
Ceratonia siliqua (Tucker, 1992) in tribe
Cassieae, and many tropical taxa of tribe Detarieae such as
Saraca declinata (Fig. 1C; Tucker, 2002b,
2000c). However, some caesalpinioids such as redbud
(Fig. 1A) have flowers that become moderately to strongly zygomorphic
at anthesis (Tucker, 2002a) and show convergence with
subfamily Papilionoideae in their papilionoid type of flower. Strongly
zygomorphic but non-papilionoid flowers occur in many other tropical
woody caesalpinioids such as detarioids Paramacrolobium
caeruleum (Taub.) J. Léon. (Fig. 1B) and
Gilbertiodendron klainei (Pierre and Pellegr.) Léon. (Fig. 2D), in which the standard petal is very large, but the other
petals are absent or reduced in size (Tucker, 2000a,
2002d). The flower of Amherstia nobilis Wall.
(Fig. 1E), another caesalpinioid in tribe Detarieae, is also strongly
zygomorphic but nonpapilionoid, having just three petals. Some
caesalpinioid flowers are asymmetric, such as Labichea
lanceolata Benth. (Fig. 1D) in tribe Cassieae.
Organ Positions
The positions of floral organs differ among the subfamilies. In Caesalpinioideae, the whorls of sepals, petals, and the two whorls of stamens are each pentamerous and alternating. The sepal in the median sagittal plane (the vertical median) is on the abaxial or lower side of the flower (Fig. 2, A, H, and I). Because organs of each whorl alternate around the circumference of the flower, the median sagittal petal (the standard petal) initiates on the adaxial or upper side (Fig. 2E). This positional arrangement of caesalpinioids is shared by papilionoids but differs in mimosoids.
Number of Organs
Most legume flowers consistently have 21 floral organs in
alternating whorls: five sepals, five petals, 10 stamens in two whorls
of five, and a single carpel. However, many caesalpinioid taxa have
undergone complete loss of some organs, so that there are examples of
missing sepals, petals, or stamens (Tucker, 1988c). Entire whorls may be missing, as in the inner stamen whorl of Labichea lanceolata (Figs. 1D and
3E; Tucker, 1998) and S. declinata (Figs. 1C and 3D; Tucker, 2000b), or only one petal and
one sepal may be initiated as in Monopetalanthus durandii F. Hallé & Normand (Fig. 3A; Tucker, 2000a). Developmental
mechanisms have evolved for increase or decrease in organ number among
caesalpinioids. Is their ontogeny abbreviated as well, or is ontogeny
normal but with subsequent suppression of organs?
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Reductions in the number of organs initiated are seen in some examples.
The only organs initiated in L. lanceolata (Figs. 1D and 3E)
are five sepals, four petals, two stamens, and a carpel, whereas
Saraca declinata initiates five sepals, a carpel, and four
petal primordia that are converted to stamens (Figs. 1C and 3D). Far
more commonly, legumes apparently lack some floral organs after
initiating all 21 organs; some are suppressed after initiation and fail
to develop. The caesalpinioid genus Bauhinia includes many
species showing suppression of some of the petals and stamens. The
number of functional stamens per flower varies among species: one, two,
three, five, nine, or 10. B. divaricata (Fig. 3F), for example, has two large petals (several are rudimentary) and one stamen.
The other nine stamens are initiated but remain small, sterile, and
form a toothed collar around the ovary (Tucker, 1987a, 1988b).
Increase in the number of organs is not simply achieved in development
of a highly synorganized flower with a set number of organs in a set
number of whorls. (Synorganization is the spatial and functional
integrated connection of organs to form a functional apparatus;
definition after Endress [1994].) Some legumes have evolved novel kinds of meristems such as ring meristems (Fig. 3A),
common primordia, or additional whorls, by which extra organs are added
to the basic ground plan. A ring meristem, a circular ridge on which
numerous stamens (up to 200) may be initiated, is a regular feature of
ontogeny in several tropical tree genera of caesalpinioids including
Monopetalanthus durandii (Fig. 3A; Tucker,
2000a).
Organogenesis
An ontogenetic series of organ initiation is shown in Figure 2
(G-L) in the caesalpinioid redbud. Bracteoles (Fig. 2G) are first
initiated, then the first sepal (Fig. 2H), then the rest of the five
helically initiated sepals and the first two petals (Fig. 2I). Petal
initiation begins on the abaxial side of the flower and continues
unidirectionally toward the adaxial side. The next stage shows all five
petals plus the first three outer stamens (Fig. 2J); then the inner
stamens initiate (Fig. 2K). Each of the two stamen whorls also show
unidirectional order of initiation. A midstage view has all organs
present (Fig. 2L) before enlargement and differentiation begin
(Tucker, 2002a).
Caesalpinioids share some features of floral ontogeny with mimosoids
(e.g. helical calyx in some taxa) and some with papilionoids (e.g.
having the median sagittal petal on the upper or adaxial side of the
flower, and unidirectional order in some taxa). Among Caesalpinioid
taxa, organogenesis varies greatly. One finds every possible
combination of helical and unidirectional organogenesis among whorls
(Table I), from completely helical (in
Gleditsia triacanthos) to completely unidirectional (in 17 taxa, mostly species of Caesalpinia (Kantz,
1996), and in several species of Bauhinia
(Tucker, 1988b). Completely unidirectional order is the same as that prevailing in the papilionoid subfamily. This pattern is
considered the most specialized one among legumes. It is interesting to
find the most derived type of organogenesis represented in three of the
caesalpinioid tribes: Caesalpinieae, Cercideae, and Detarieae. The
caesalpinioid tribe Cassieae has especially diverse development, with
every combination of organogenesis except for uniformly unidirectional
(Table I), the only tribe that lacks any known taxa that are
consistently unidirectional. This tribe includes some of the most
unusual patterns involving bidirectional or erratic order, as well as
reduced or missing whorls (Table I). Interestingly, Cassieae is
polyphyletic and includes at least three distinct groups of taxa
(Doyle, 1995; Doyle et al., 2000), which
have evolved developmental sequences different from those of the other
tribes.
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Other combinations of organogenesis found rarely among caesalpinioid
taxa include several with bidirectional or erratic order in some whorls
(Table I). In a few, the number of organs per whorl is so reduced that
order cannot be determined. Only one sepal and one petal are initiated
in flowers of Aphanocalyx djumaensis (de Willd.) J. Léon. and Monopetalanthus durandii (Fig. 3A;
Tucker, 2000a). Only two stamens are initiated in
Labichea lanceolata (Figs. 1D and 3E) and Dialium
guineense (Tucker, 1998), and they are in anomalous
positions that make order of initiation difficult to compare with other taxa.
Unisexuality
Reduction in organ number results in unisexual flowers among some
Caesalpinioideae such as Gleditsia triacanthos and
Bauhinia malabarica Roxb. All flowers of G. triacanthos (Tucker, 1991; Fig. 3I) are initially
bisexual, initiating both stamens and carpels, but reproductive organs
are suppressed selectively to produce either male or female flowers
(Fig. 3, J and K). Three floral morphs (male, female, and bisexual) are
found in B. malabarica (Tucker, 1988b) and
Ceratonia siliqua (Tucker, 1992). In many other caesalpinioid legumes such as other species of
Bauhinia (Tucker, 1988b) and
Saraca (Tucker, 2000b), bisexual flowers are the rule, but occasional flowers are functionally male; the gynoecium is suppressed and nonfunctional.
How is unisexuality brought about developmentally? All floral buds are bisexual at first in caesalpinioid legumes examined, developing both stamen and carpel primordia. Late in development either the stamens or the carpel become suppressed in flowers, so that they are functionally unisexual. Pollen fails to form in the anthers of female flowers; the gynoecium in male flowers may contain ovules but the gynoecium remains much smaller than usual and the style and stigma do not develop normally.
Petal Aestivation
As the petal primordia enlarge and broaden, their margins overlap. The pattern of petal aestivation (or overlapping) distinguishes the three legume subfamilies. The petals of caesalpinioid flowers become imbricate in a pattern called ascending cochleate; the keel margins overlap the adjacent margins of the wings, and wing margins overlap the adjacent margins of the standard or vexillum petal (Fig. 2F, redbud).
Organ Differentiation and Specialization
Differentiation of floral organs occurs late in their development.
Developmentally, organs in the same whorl are initially alike, and will
develop alike in radially symmetrical flowers (predominant in tribe
Caesalpinieae; Kantz, 1996). Floral specializations are
rather few in this tribe, according to Kantz (1996).
Uniform whorls also can be found in some radially symmetrical taxa of tribe Detarieae [e.g. Fig. 2C, Isoberlinia angolensis
(Benth.) Hoyle & Brenan].
In many other caesalpinioids, however, same-whorl organs
differentiate as dissimilar structures, especially in flowers with zygomorphic symmetry. How do these dissimilarities arise in
development? Three petal morphs are seen in the flower of
Amherstia nobilis (Fig. 3G; Tucker, 2000c),
and only three functional stamens. Although uniform stamens per flower
predominate, exceptions with heterogeneous stamens can be found. Two
dissimilar stamens occur in the flower of Labichea
lanceolata (Figs. 1D and 3E), a flower that is asymmetrical. Bauhinia divaricata (Fig. 3F) has one large functional
stamen and nine suppressed stamen rudiments. Stamen diversification is even more noticeable in Senna pendula (Humb. & Bonpl.
ex Willd.) Irwin & Barneby, in which the 10 stamens include
four different morphs (Fig. 3H, with stamen types labeled as A1-A4;
Tucker, 1996). S. pendula flowers are
zygomorphic and dorsiventrally heteromorphic, having two large
pollinating stamens (A1) with curved anthers and terminal pores; four
intermediate "fodder" stamens (A2) with straight anthers; a median
adaxial stamen (A3) with a longer filament, and three short staminodia
(A4) with coiled or arched nonfunctional anthers. Flowers of
Senna spp. are adapted for "buzz" pollination by large
bees. An ontogenetic study of this species shows that the stamen
primordia are alike in each whorl up until late stages, when the two
lateral abaxial stamens of the inner whorl enlarge ahead of the others
of both whorls, and each stamen type differentiates uniquely.
Specialized features of floral organs, such as these stamens, commonly
are expressed very late in ontogeny.
Organ Fusion
Fusions occur among caesalpinioid floral organs. Fusions are of two kinds: edge-to-edge fusion and fusion that results from intercalary growth. The first type of fusion may be either temporary or permanent, whereas the second is usually permanent. Edge-to-edge fusion is exemplified by sepal and petal margins that may fuse temporarily in bud and then split open as the flower expands and opens. Carpel margins also fuse by appression of the edges, cells interlocking, and subsequent cell division. The carpel margins are permanently fused in this way during seed development, although anatomical mechanisms of the developing fruit may later lead to separation along the suture.
Fusion also occurs by intercalary growth. Many caesalpinioid flowers
appear to have only four sepals, because the two adaxial sepals fuse to
appear as one (Fig. 3, B and C, Brownea latifolia Jacq.;
Tucker, 2000c). The sepal primordia initiate separately, but intercalary growth of the receptacle below the bases of two adjacent sepal primordia creates the appearance of a single organ. Intercalary growth also occurs in the receptacle below the ring of 10 stamens in some caesalpinioids, raising the stamens on a tubular sheath
(Tucker, 2002c, 2002d).
Comparisons of Caesalpinioid Tribes
The subfamily Caesalpinioideae is basal in phylogenetic schemes
(Doyle, 1995; Doyle et al., 2000;
Bruneau et al., 2001) and is highly diverse in floral
form and ontogeny. The number of tribes continues to be controversial,
with current opinions including four or five: Cercideae, Caesalpinieae,
Cassieae, and Detarieae; Macrolobieae is segregated from the latter in
some views (Bruneau et al., 2001).
Only one (Cercideae) of the tribes of Caesalpinioideae appears to be
monophyletic (Bruneau et al., 2001). The flowers are generally showy, with zygomorphic symmetry. Several species of two of
its genera (Bauhinia and Cercis) have been
studied developmentally (Tucker, 1984b,
1988b, 2002a), but the other three are
poorly known.
Members of tribe Caesalpinieae (Polhill and Raven, 1981;
Kantz, 1996) are characterized by simple floral
organization, primarily radial symmetry and lack of specializations.
These unspecialized floral features may be considered plesiomorphic
(primitive shared) character states. Floral ontogeny is relatively
uniform among Caesalpinieae (Table I; Tucker, 1984b,
1991; Kantz, 1996). Specializations are
rather few and minor in this tribe, according to Kantz
(1996). Recent molecular-based phylogenetic analyses
(Doyle, 1995; Doyle et al., 2000;
Bruneau et al., 2001) suggest that tribe Caesalpinieae is not monophyletic. Aggregations of taxa having unspecialized flowers,
such as Caesalpinieae, lack the shared, specialized character states
that indicate close relationship by convention in cladistic analysis.
Tribe Cassieae is not monophyletic, including at least three
disparate lineages, according to molecular-based phylogenetic analyses
(Doyle, 1995; Doyle et al., 2000). The
great developmental diversity in floral form, with every combination of
organogenesis except for uniformly unidirectional (Table I), supports
this lack of close relationship among members of tribe Cassieae.
Specializations among caesalpinioids include heterogeneous androecial
whorls and adaptations for "buzz" pollination in the
Cassia group (Tucker, 1996), and unisexuality
and complete loss of petals in Ceratonia siliqua
(Tucker, 1992).
Tribe Detarieae sensu lato (here including Macrolobieae) is
both the largest (84 genera, 50% of the total in the subfamily Caesalpinioideae) and the least well-known tribe of caesalpinioids. Floral structure is diverse, with numerous specializations including suppression of some organs after initiation (Tucker,
2000c, 2001, 2002c,
2002d), nearly complete loss of sepals and/or petals
(Tucker, 2000a), and homeotic conversion of petal
primordia into stamens in Saraca declinata (Figs. 1C and 3D;
Tucker, 2000b). The molecular-based phylogenetic
analysis by Bruneau et al. (2001) shows two major clades, Macrolobieae and Detarieae sensu stricto. The Macrolobieae clade appears monophyletic and derived from within the diverse tribe
Detarieae sensu stricto.
In the last 10 years, concerted efforts have been made to investigate
many aspects of the Detarieae tribe. Molecular evidence suggests the non-monophyly of Detarieae (Bruneau et al.,
2001), although some groups within it are monophyletic.
Developmental floral evidence is complex and is not altogether
congruent with molecular results.
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SUBFAMILY MIMOSOIDEAE |
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TOP
INTRODUCTION
SUBFAMILY CAESALPINIOIDEAE
SUBFAMILY MIMOSOIDEAE
SUBFAMILY PAPILIONOIDEAE
WHAT CAN WE LEARN...
LITERATURE CITED
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Mimosoideae includes 65 genera and about 3,000 species. There is
general agreement that the Mimosoideae subfamily is a monophyletic group arising from among the caesalpinioids, based upon both
morphological (Chappill, 1995) and molecular evidence
(Doyle et al., 2000; Luckow et al.,
2000). Although its flowers are radially symmetrical and appear
unspecialized, the group as a whole is derived. The subfamily includes
four tribes: Mimoseae, Acacieae, Ingeae, and Parkieae.
Inflorescences
Mimosoid flowers are usually aggregated in a raceme (Fig.
4A, Mimora strigillosa T. & G.) or a paniculate inflorescence (Tucker, 1987a). The taxa examined
share an unusual developmental feature: synchronous development of the
flowers in any one inflorescence. As in racemes of the other
subfamilies, these undergo acropetal, successive order of flower
initiation, but each floral bud pauses after its initiation until all
are initiated in that inflorescence. Then, all flowers undergo
synchronized initiation of sepals, then petals, and so on. As a result,
all flowers will be at the same stage of development in an individual
inflorescence. Synchronous development in mimosoid inflorescences
contrasts with the successive development found in inflorescences of
the other two subfamilies.
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Symmetry
Flowers are radially symmetrical in nearly all taxa in the mimosoid subfamily (Fig. 4F). Radially symmetrical mimosoid flowers usually have four or five organs in each whorl, and all members of a whorl are alike.
Organ Positions
Flowers of Mimosoideae differ as a group from other legumes in
organ position (Tucker, 1987a, 1988a;
Ramirez-Doménech, 1989; Derstine and
Tucker, 1991). In pentamerous taxa of Mimosoideae, the sepal in
the median sagittal plane is on the adaxial or upper side (Fig. 4, B
and C; Neptunia pubescens Benth.). In Caesalpinioideae and
Papilionoideae, the sagittal plane sepal is on the abaxial or lower
side (Fig. 2, H and I). This difference in the architecture of the
flower between Mimosoideae and the other two subfamilies is a major
developmental difference, and one in which there are unlikely to be
intermediate states or exceptions. It is difficult to see an adaptive
value for either of these states in themselves, but an advantage may
lie in associated or derivative characters. The lack of a petal in the
median adaxial position in mimosoids may suppress in some way the
tendency toward zygomorphy that prevails among papilionoids and many caesalpinioids.
Number of Organs
Mimosoid flowers are either tetramerous or pentamerous. Flowers of
tribes Mimoseae and Parkieae have eight or 10 stamens in two whorls. In
tribes Acacieae and Ingeae (Fig. 4I, Calliandra houstoniana
Standley), stamens are numerous. The genus Acacia in
Acacieae includes numerous multistaminate species, i.e. Acacia myrtifolia Willd., with as many as 500 stamens per flower. Stamens proliferate on "common primordia" in Acacia baileyana F. Muell. (Derstine and Tucker, 1991). Common primordia are
apical meristem sectors below each of the first five stamen
primordia, on which additional stamens are initiated, giving a total of
30 or more per flower. Most mimosoids have a single carpel per flower,
although some taxa of Ingeae have multicarpellate flowers.
Reduction in organ number is uncommon among mimosoids, except for some taxa with only one whorl of four or five stamens, rather than two whorls. Unisexual flowers also have reduced numbers of organs at anthesis, although generally the reduction results from failure of either stamens or carpel to enlarge.
Organogenesis
The flowers of mimosoid taxa nearly all show simultaneous initiation of each whorl (Fig. 4, B-F, Neptunia pubescens). The only exception is that sepals may be either simultaneous or helical, depending on the taxon. Members of each whorl alternate with those of the previous whorl. Among Mimosoideae, developmental innovations such as ring meristems and common primordia produce numerous additional organs beyond the 21 found in flowers of most Caesalpinioideae and Papilionoideae. Large numbers of stamens per flower are initiated on ring meristems or common primordia in tribes Acacieae and Ingeae (Fig. 4I, Calliandra houstoniana).
Unisexuality
Unisexual flowers are quite common among mimosoids, particularly
andromonoecy (Kalin Arroyo, 1981). Three sexual floral
morphs (male, female, and neuter) occur in each inflorescence in
Neptunia pubescens (Tucker, 1988a) and in
species of the tropical, bat-pollinated tree genus Parkia
(Polhill and Raven, 1981, and refs. therein).
Petal Aestivation
Mimosoid petal aestivation is predominantly valvate (meeting edge-to-edge), without overlap (Fig. 4G, N. pubescens). This pattern contrasts with imbricate (overlapping) petal aestivation in the other two subfamilies.
Organ Differentiation and Specialization
Organs are all alike in each whorl in mimosoid flowers, unlike many caesalpinioids. Within-whorl organs all develop similarly. Organ specializations among mimosoids include unisexual flowers in Parkia spp. and some Mimoseae, glandular-tipped anthers in Parkieae and some Mimoseae, a fused staminal tube in Ingeae, and polyad pollen grains in Acacieae and Ingeae.
Organ Fusion
Fusions among organs, either temporary or permanent, are prevalent among mimosoids. Temporary edge-to-edge fusions most commonly involve sepals or petals (Fig. 4G). Permanent fusions occur occasionally in the calyx through intercalary growth (Fig. 4H, Shrankia microphylla [Dryander] MacBride), and commonly among stamen filaments (Fig. 4I, C. houstoniana) in tribe Ingeae as the result of intercalary growth. Stamens are initiated individually, but intercalary growth occurs in the receptacle below their bases so that all the stamens are raised on a ring and appear fused (Fig. 4I).
Comparison among Tribes
Traditionally, the four tribes of Mimosoideae differ on morphological bases. Stamen number distinguishes Mimoseae and Parkieae (eight or 10 stamens per flower; Fig. 4, E and F) from the other two tribes, Acacieae and Ingeae (both with numerous stamens). The latter two are distinguished by free stamens in Acacieae versus fused stamens in Ingeae. The Mimoseae have valvate sepals, whereas the Parkieae have imbricate sepals.
Recent molecular-based analyses by Luckow et al.(2000,
2002) suggest that none of the four mimosoid tribes is
monophyletic. Mimoseae is basal and paraphyletic, with taxa of the
other tribes derived from within it. Parkia, the major genus
in tribe Parkieae, is nested within tribe Mimoseae. Acacieae and Ingeae
are each polyphyletic; Acacia subgenus Acacia
forms one monophyletic clade, whereas the remainder of the huge genus
Acacia, together with Ingeae, forms a second clade.
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SUBFAMILY PAPILIONOIDEAE |
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TOP
INTRODUCTION
SUBFAMILY CAESALPINIOIDEAE
SUBFAMILY MIMOSOIDEAE
SUBFAMILY PAPILIONOIDEAE
WHAT CAN WE LEARN...
LITERATURE CITED
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Papilionoideae is the largest of the three subfamilies, with 30 tribes, 455 genera, and about 12,000 species. It is a specialized monophyletic group that is derived from within the caesalpinioid subfamily, based on morphological (Chappill, 1995) and
molecular evidence (Doyle, 1995; Doyle et al.,
2000). Most taxa have the familiar "papilionoid" flower
form (Fig. 1F), although there are exceptions in tribes Sophoreae and Swartzieae.
Inflorescences
Inflorescences of Papilionoideae are usually racemes or panicles.
In a raceme of Lupinus affinis Agardh (Fig.
5A; Tucker, 1984a), the apical meristem
initiates bracts in acropetal succession, and a floral bud develops in
the axil of each bract. The number of flowers per raceme depends on how
long the apical meristem is active. The flowers in racemes are
initiated in succession and develop in succession, as in
Caesalpinioideae. Hence, an individual inflorescence contains flowers
of many different ages, the oldest at the bottom, and younger ones
above.
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Two other kinds of inflorescences occur among Papilionoideae:
pseudoracemes and cymes (rarely). Pseudoraceme inflorescences (Tucker, 1987b) have evolved in five tribes of
Papilionoideae: Abreae, Desmodieae, Millettieae, Psoraleeae, and
Phaseoleae. All of these tribes are currently grouped in the
"phaseoloid" clade based on molecular evidence (for summary, see
Doyle et al., 2000). Pseudoracemes (Fig. 5B) differ from
racemes in that two to several flowers are initiated in each bract axil
rather than just one as in a raceme. The cluster of flowers at each
node is called a fascicle. The order of initiation among flowers at a
node (Fig. 5B, Psoralea macrostachys DC) shows the fascicle
to be a short shoot topped by a second order inflorescence apical
meristem. This meristem initiates flowers in a bilaterally symmetrical
order: a single abaxial flower, then two lateral flowers, another
median abaxial, then two more laterals. The number of flowers per
fascicle depends on the duration of the axillary inflorescence apex of the short shoot, which ceases activity after initiating the few flowers
in the fascicle. No flowers are initiated adaxially (toward the first
order axis) on the short shoot (Tucker, 1987b;
Tucker and Stirton, 1991). The short shoot in a
pseudoraceme can be distinguished from a cyme in that every flower is
bract subtended in a pseudoraceme.
Symmetry
Most Papilionoideae (in 28 of 30 tribes) have specialized
zygomorphic flowers with papilionaceous features that
result from surprisingly uniform ontogenies. Papilionoid flowers, such
as Lupinus succulentus Dougl. (Fig. 1F) and
Erythrina herbacea (Fig. 6, B
and C), are typical examples of zygomorphic symmetry (Tucker, 1987a).
Each flower has three petal forms: a single standard petal (or
vexillum), two wing petals, and two keel petals (Fig. 5F, Genista
tinctoria). The petals are alike, however, throughout much of
their development (Fig. 5D), and only differentiate late in ontogeny
(Figs. 1F and 5F). Other expressions of zygomorphy also are manifested
at late stages, e.g. upturning of the style and stamens, the horizontal
positioning of the entire flower, differential elongation of sepal
lobes, and formation of one or two "windows" or fenestrae into the
nectar-containing filament tube (Fig. 6G, Erythrina caffra
Thunb.). Zygomorphy expressed late in floral development is very
common, especially among papilionoid taxa.
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Two papilionoid tribes, Sophoreae and Swartzieae, include exceptions to
the rest of the subfamily in floral form and uniform ontogeny. These
exceptions include (in some but not all taxa) radial symmetry
(Pennington et al., 2000; Tucker, 2002b;
Mansano et al., 2002), non-papilionaceous corollas,
complete loss of some petal primordia, atypical petal aestivation,
polystemony (resulting from an innovative developmental feature, the
ring meristem), and lack of stamen fusion. Representing taxa with
radial symmetry, Cadia purpurea Forsk. (Fig. 5E;
Tucker, 2002b) in tribe Sophoreae has a uniform calyx,
corolla, and androecium. Representing zygomorphic but nonpapilionoid
symmetry is Swartzia (Fig. 5, G and H) in tribe Swartzieae,
which has a completely fused calyx, a single petal, and multiple
stamens of two size classes. The order of initiation of organs in
Swartzieae also diverges from that of all other papilionoids.
Organ Positions
Papilionoid flowers are pentamerous, with members of each whorl alternating with those of adjacent whorls. The basic ground plan has the median sagittal sepal on the lower or abaxial side, and the median sagittal petal on the upper or adaxial side. This arrangement is similar to that of Caesalpinioideae, but contrasts with that of Mimosoideae, in which the median sagittal sepal is on the upper or adaxial side.
Number of Organs
Most taxa of Papilionoideae have a full complement of organs: pentamerous alternating whorls of sepals, petals, two stamen whorls, and the single carpel. Where organs appear to be fewer, ontogeny shows that all are initiated but that some organs are subsequently suppressed during development.
Loss and increase in floral organ number are rare among papilionoids,
but both occur in one tribe, Swartzieae, a group of tropical trees. In
Swartzia, the corolla is reduced to one petal (Fig. 5, G,
S. sericea Vogeli-Zuber; and H, S. aureosericea Cowan) or absent altogether. Numerous stamens
(20-200) are initiated on a ring meristem, a circular ridge that is an
innovation in ontogeny in Swartzia (e.g. Fig. 5G;
Tucker, 1988c).
Organogenesis
In most Papilionoideae, all floral organs are
initiated in a unidirectional successive order in each whorl starting
on the abaxial side (next to the subtending bract). The ontogenetic
series of papilionoids resembles that shown in Figure 2, G through L, for a caesalpinioid, except that all whorls have unidirectional order
in papilionoids. Timing of one whorl may overlap with that of the next
among some papilionoids. For example, stamens commonly start to
initiate before the last petals have been initiated. An extreme example
is in garden pea (Fig. 5C; Tucker, 1989;
Ferrándiz et al., 1999), in which petal and stamen
whorls as well as the carpel overlap in their time of initiation. This
flower also is unusual in having "common primordia," ephemeral
meristems that each initiate two or three individual primordia.
The pattern of organogenesis differs in papilionoid tribe Swartzieae,
which has a ring meristem on which numerous stamen primordia are
initiated (Fig. 5, G and H, species of Swartzia;
Tucker, 1988c). This genus also is exceptional in having
either a single petal initiated, or no petals. Most species have a
single carpel but a few have several carpels, a rare condition among legumes.
Unisexuality
Unisexual flowers are rare among papilionoids, but Ateleia
herbert-smithii Pitt. in tribe Swartzieae (Tucker,
1990, and refs. therein) is dioecious, with male and female
flowers on different trees. It is wind-pollinated, a rare feature among
legumes. All flowers of A. herbert-smithii initiate both
stamens and carpels. Later in development, stamen or carpel development
is suppressed, resulting in female or male flowers. Male sterility
occurs in some cultivated species of Vigna,
Lathyrus, and Lupinus (Kalin Arroyo,
1981).
Petal Aestivation
Papilionoid petal aestivation is expressed as imbricate in a pattern called descending cochleate, in which the standard petal margins overlap the adjacent wing margins, which overlap the adjacent keel margins (Fig. 5F, Genista tinctoria). This pattern contrasts with that of caesalpinioids (ascending cochleate, Fig. 2F) and mimosoids (valvate, Fig. 4G; no overlap). The pattern of overlap among petals is an easy way to distinguish the legume subfamilies. These distinctions in petal aestivation among subfamilies are stable and are presumably highly canalized. How do these differences arise in development?
A few taxa in Papilionoideae have a random pattern of petal
aestivation, e.g. Cadia purpurea (Fig. 5E) in tribe
Sophoreae, and three taxa of the Lecointea group
(Mansano et al., 2002), with currently uncertain
affinity (Pennington et al., 2000), but closely related
to Sophoreae. The basis for this aberrant petal aestivation appears to
be that all petal margins in C. purpurea grow straight
outward like the vexillar or standard petal in most papilionoids. In
papilionoid corollas with descending cochleate aestivation, overlapping
petal margins grow essentially straight outward, whereas those that
will be overlapped curve inward, due to slightly greater cell
enlargement abaxially than adaxially (for details, see Tucker,
2002b). In C. purpurea, chance determines which
petal overlaps another. Taxa with random aestivation such as C. purpurea provide an opportunity to determine the basis for genetic
control of the prevailing descending cochleate petal aestivation among
Papilionoideae and the ascending cochleate aestivation among Caesalpinioideae.
Organ Differentiation and Specialization
Specializations among papilionoid flowers include different types of inflorescences, some asymmetry, elaborations of petals and stamens, heterogeneous whorls, and fusions among petals and among stamens. Same-whorl organs often differentiate as dissimilar morphs, especially in papilionoid flowers with zygomorphic symmetry. How do these dissimilarities arise in development, and at what stage do they first appear? In the papilionoid Erythrina herbacea, petal primordia are uniform in size up through midstage, when size differences first become evident (Fig. 6A). The standard or vexillum petal (at arrowhead in Fig. 6A) is slightly taller than the wing and keel petals at midstage. In late stages, the petals have taken on different shapes, symmetries, and degree of fusion. The standard or vexillum petal enlarges greatly and envelops the rest of the flower, but remains bilaterally symmetrical (Fig. 6, B and C). The two wing and two keel petals remain small and have each become asymmetrical. The two keel petals have attenuate tips, and their adjacent margins become fused (Fig. 6, B and C). At anthesis in E. herbacea, only the standard petal, 3 to 5 cm long, is visible; it wraps around the other petals that are 0.5 to 1.3 cm long. These changes in petal size and form are expressions of zygomorphy and are manifested late in development of the flower.
Petals of other papilionoids may show additional changes in form: auricles, transverse ridges, folds, pegs, and corresponding pits that interlock petals together, even though they may not be physically fused. Papilionoid petals may have elaborate pouches, knobs, ridges, and other elaborations. An example is shown in the inflated fused keel petals of Indigofera heteranthera Wall. (Fig. 6D) that also have spurs. In many papilionoids, the knobs and pits between adjacent petals interlock to form a tube-like corolla that encloses the stamens, gynoecium, and nectary, thereby restricting the type of pollinator and controlling its path of entry to pollen and nectar.
Organ Fusion
Fusions are especially common among floral organs of papilionoids. Although all floral organs are initiated singly, many show fusion at anthesis. Examples include an enclosing calyx in bud, fused keel petals, fused carpel margins that form the ovary locule, and the fused stamen tube. How do these fusions occur during development, and what adaptive advantages do they provide?
First, both edge-to-edge fusions and intercalary growth fusions occur,
as described for the other two subfamilies. Sepal, petal, and carpel
margins fuse by appression of the edges, interlocking between epidermal
cells, and (often) subsequent cell division (Tucker,
1987a). Edge-to-edge fusions between keel petals are common
among papilionoids (Fig. 6, B and C, E. herbacea; and D, I. heterantha), and these fusions generally persist during
the short life of the petals. Keel enclosure of the stamens and
gynoecium is one of the mechanisms that restricts the type of
pollinator and its activity to species-faithful insects. Carpellary
marginal fusion usually involves cell division and enlargement that
obscure the line of contact and is permanent until fruit ripening.
Permanent fusion due to intercalary growth is responsible for the
fused stamen sheaths of papilionoids (Tucker, 1987a).
Ten stamen primordia are initiated in two successive, alternating whorls of five (Fig. 5D, Genista tinctoria). They become
reoriented into a single whorl as the receptacle enlarges, and their
filaments then become fused into a tube (Fig. 6E), with the anthers and upper parts of filaments free. This fusion occurs by elongation in the
receptacle below the bases of the stamens, so that they are raised up
on a cylindrical or tubular base. The stamen primordia themselves
do not undergo fusion. Papilionoid filament tubes are of
three kinds: monadelphous, diadelphous, and pseudomonadelphous. In the
monadelphous type (Lupinus affinis Agardh, Fig. 6E), the cylinder includes all 10 stamens and is closed; in the diadelphous type
(Robinia hispida, Fig. 6F), only nine stamens are fused and one is free. The free stamen is always the median adaxial one, and its
separate base permits insect access to the nectary between the carpel
and stamen bases.
A diadelphous androecium may undergo a further elaboration during
ontogeny to form the third type, a pseudomonadelphous cylinder (Erythrina caffra, Fig. 6G; Tucker, 1987a).
Edge-to-edge fusions occur between the free stamen filament and the
sides of the adjacent filament tube, so that it becomes a continuous
tube. Fusion is not complete, however, at the base of the filaments. In
fact, two "holes" or fenestrae enlarge at these points, which
facilitate entry of a bee's proboscis into the area of the nectary.
Thus, this androecium is called pseudomonadelphous because it mimics a
monadelphous androecium, but results from a different ontogeny. The
stamen tube characterizes papilionaceous floral form and restricts or
controls pollinator behavior. The stamen tube has evolved via at least
three different ontogenetic pathways among papilionoid legumes.
Selective fusion, by intercalary growth in the receptacle and/or by edge-to-edge fusion, thus determines the type of androecium in papilionoids. Some papilionoids such as those in tribes Sophoreae and Swartzieae generally lack fusion among stamens, and are adapted to different kinds of pollinators.
Comparison among Papilionoid Tribes
Much more molecular systematic work has been done on
Papilionoideae than on either of the other two subfamilies. Only a
brief summary of current opinion about relationships can be offered here. Several major monophyletic groups or clades appear consistent among Papilionoideae, based on molecular evidence (for summary, see
Doyle, 1995; Doyle et al., 2000). A
"genistoid" clade includes tribes Genisteae, Thermopsideae,
Crotalarieae, Podalyrieae, and Sophoreae pr. p. An
"aeschynomenoid" group includes tribes Aeschynomeneae, Adesmieae,
Desmodieae pr. p., and Dalbergieae pr. p. The "galegoid" clade
(Hologalegina) is the largest papilionoid clade and is comprised of
most of the temperate herbaceous tribes (Carmichaelieae, Cicereae, Coronilleae, Galegeae, Hedysareae, Loteae, Trifolieae, and Vicieae). A
"phaseoloid" clade includes tribes Desmodieae pr. p., Indigofereae, Millettieae, Phaseoleae, and Psoraleeae. Two Australian tribes, Mirbelieae and Bossieae, form a clade. Several other small tribes remain unresolved as to their relationships. Neither Swartzieae nor
Sophoreae, the two anomalous tribes with non-papilionoid flowers, is
monophyletic. Their status is currently in flux, as discussed by
Pennington et al. (2000).
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WHAT CAN WE LEARN FROM LEGUME FLORAL ONTOGENY? |
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TOP
INTRODUCTION
SUBFAMILY CAESALPINIOIDEAE
SUBFAMILY MIMOSOIDEAE
SUBFAMILY PAPILIONOIDEAE
WHAT CAN WE LEARN...
LITERATURE CITED
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Does Legume Flower Development Follow the ABC Model?
The successive and overlapping order of organ initiation in some
legume flowers is intriguing developmentally because of its conflict
with prevailing interpretations of hypotheses concerning timing of
determination of organ identity. The ABC model hypothesis of floral
organ identity (Meyerowitz et al., 1991; Irish,
1999; Jack, 2001) applies to flowers such as
Arabidopsis, in which all organs of a whorl initiate simultaneously,
the order of initiation is sepals, petals, stamens, and carpels, and
where whorls do not overlap in time of initiation. It proposes that
certain sets of genes or gene combinations act in the floral apex in
succession, determining the type of organ being initiated. "A"
alone produces sepals, "A" + "B" produces petals, "B" + "C" produces stamens, and "C" alone produces carpels. This
hypothesis applies only to organ identity determination and the order
in which whorls occur in the flower and does not explain timing within
whorls or location of organs within the whorl. It does not
satisfactorily explain a system in which more than one type of organ is
being initiated at the same time, such as that in papilionoid and
caesalpinioid legumes that have overlapping whorls. The ABC model also
does not explain the concurrent initiation of the carpel at the same time as petals or stamens, which is usual in legumes. I know of no
legume in which the carpel is initiated last, after all stamens are
present. In several respects, legume flowers fail to conform to the ABC model.
An intriguing array of mutant genes that control various aspects
of normal floral ontogeny in legumes have been discovered. Genes
control the transition from inflorescence to flower, as well as
affecting floral organ expression (Singer et al., 1999; Hirsch et al., 2002; Taylor et al.,
2002). Organ initiation in pea involves common primordia, an
extra step inserted during ontogeny. Each common primordium initiates
two or three individual organ primordia (Tucker, 1989).
Ferrándiz et al. (1999) examined floral identity
genes as well as mutations of A, B, and C classes in pea. They
concluded that A, B, and C factors specify organ identity in common
primordia as well as in organ primordia, although these factors do not
control floral determinacy or organ number unlike some of the gene
homologs in Arabidopsis and Antirrhinum spp. Common
primordia are quite rare among legumes and probably represent an
evolutionary specialization. Most other papilionoid legumes (e.g.
Lupinus affinis, Tucker, 1984a,
1984b; Melilotus alba, Hirsch et al.,
2002) share an unusually uniform pattern of organogenesis and
initiate organs directly without a common-primordial stage. This
contrast in pattern of organ initiation offers an opportunity to
compare control of floral organ initiation with and without the stage
involving common primordia.
Although research on the ABC model has concentrated on two angiosperms
(Arabidopsis and Antirrhinum majus) belonging to the eudicots (the most highly derived group of dicotyledons), 17 basal angiosperms have recently been investigated for the B class genes that
control petal and stamen identity (Kramer and Irish,
2000). Many of these basal or lower dicots have only one
perianth whorl (tepals), which have long been thought to be derived
from modified leaves, in contrast to petals of higher dicots, which are
considered to be evolved from stamens. The basal angiosperms and lower
dicots have PISTILLATA and a form of the
APETALA gene (PaleoAP3) expressed in the tepals,
although the timing and degree of expression varied considerably among
the basal taxa.
What Does Comparison of Floral Ontogenies of Numerous Related Taxa Tell Us about Evolution in Legumes?
Unspecialized floral structure, used as a basis for systematic
relatedness in several groups of Fabaceae, appears deceptive in several
cases. For instance, simple floral organization and lack of floral
specializations characterize members of tribe Caesalpinieae of
subfamily Caesalpinioideae (Polhill and Raven, 1981;
Kantz, 1996). Similarly, the tribe Sophoreae includes
the taxa of subfamily Papilionoideae that have the fewest floral
specializations. However, recent molecular-based phylogenetic analyses
(Doyle, 1995; Doyle et al., 2000;
Bruneau et al., 2001) indicate that neither
Caesalpinieae nor Sophoreae are monophyletic groups, but instead each
includes several diverse, distantly related groups. Unspecialized
flowers in legumes tend to share similar ontogenies (Kantz,
1996), although these taxa usually have a few specialized
character states that serve to distinguish them. Comparisons in such
taxa demonstrate that they share simple straightforward pathways of development.
Most legume flowers, both unspecialized and specialized, share a similar ontogenetic pathway, at least for the early stages during organ initiation and midstages as development begins. For example, flowers of Papilionoideae share early and midstages of floral ontogeny, whether they will become zygomorphic or remain radially symmetrical. Specialized flowers, in contrast, have extra developmental steps added in late stages of ontogeny that produce the specializations. Some examples include differing petal shapes of the "papilionoid" or "flag" flower, fusion of stamen filaments into a tube, and poricidal anther dehiscence.
Shared assemblages of specialized characters generally are viewed as
evidence of close evolutionary relationships. Nevertheless, in one
genus, Cassia sensu lato in the caesalpinioid tribe
Cassieae, shared specializations are deceptive. Howard S. Irwin (Long
Island University, Greenvale, NY) and Rupert C. Barnaby (New
York Botanical Garden, Bronx, NY) (Polhill and Raven,
1981, and refs. therein) split Cassia into three
genera: Cassia sensu stricto, Chamaecrista, and
Senna. These are superficially similar and share many
specialized characters such as yellow flower color, pentamerous
corolla, zygomorphy, dorsiventral heterostemony, and poricidal stamen
dehiscence. Comparison of floral ontogenies (Tucker,
1996) showed marked developmental differences in their
inflorescence architecture, phyllotaxy, bracteole formation, order of
organ initiation, amount of overlap in time between whorl initiations,
the basis for asymmetry, and the basis for poricidal dehiscence. These
differences in development strongly suggest that the superficial
similarities in the flowers have resulted from evolutionary convergence.
Comparative floral ontogeny has demonstrated its usefulness in showing shared similarities in a basic ground plan throughout the monophyletic Fabaceae. It also has shown the developmental basis for significant differences in floral form. These modifications of the basic ground plan result in different inflorescence types, differences in symmetry, petal aestivation, loss and increase in number of parts per flower, homogeneous versus heterogeneous whorls, and unisexuality in some taxa.
Hierarchical Theory
The framework of this research is a systematic and phylogenetic
one rather than experimental. The emphasis is on exploring concepts of
floral diversification and how such changes are produced during
development, expressed within subfamilies, tribes, genera, and species.
Floral development in over 300 representative legume taxa has been
studied and compared using scanning electron microscopy (SEM) to date
(124 Papilionoideae, 136 Caesalpinioideae, and 49 Mimosoideae). A
hypothesis has been proposed (Tucker, 1984a,
1997) that a correlation exists between the timing of
character expression and the hierarchical level at which it is
significant. For example, order of initiation and positions of organs
are determined early in ontogeny (during organogenesis). Both are
significant at the level of subfamily. In contrast, characters such as
petal fusions, petal shapes, and absolute or relative size differences
are determined late in ontogeny, and these distinguish taxa at the
level of species.
Trends in Legume Evolution
Developmental differences among suprageneric taxa (subfamilies and
tribes) have been emphasized here to show evolutionary trends in
Fabaceae. Two of the three traditional subfamilies, Mimosoideae and
Papilionoideae, are clearly monophyletic and have been derived from the
third subfamily, Caesalpinioideae, which is basal and paraphyletic
(Doyle, 1995; Doyle et al., 2000;
Bruneau et al., 2001).
The systematic diversity among legumes is reflected in diverse floral ontogenies. Although developmental differences among legumes have been emphasized here, they share a basic ground plan and a basic pattern of floral ontogeny. Parallel current research on molecular systematics of legumes greatly enhances the developmental investigations by providing a phylogenetic framework that helps to make sense of developmental trends.
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ACKNOWLEDGMENTS |
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The author thanks Jo Anna Bass (University of California, Santa Barbara) and former students Andrew Douglas (University of Mississippi, University), Katherine Kantz (Grand Valley State University, Allendale, MI), Elizabeth Harris (Ohio State University, Columbus), and José Ramirez-Doménech (Xavier University, New Orleans) for their technical assistance with scanning electron microscopy and photography; Jan Beckert (Santa Barbara Botanical Garden, CA) for drawings; and the following for collections: Frans J. Breteler and Jan J. Wieringa (University of Wageningen, The Netherlands), Gurilym Lewis (Royal Botanic Gardens, Kew, UK), and Bente Klitgaard (Museum of Natural History, London).
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FOOTNOTES |
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Received November 11, 2002; returned for revision December 4, 2002; accepted December 26, 2002.
1 The research was supported in part by the National Science Foundation (grant nos. BSR84-18922, BSR87-22514, DEB92-07671, and DEB94-20158 [DEB-9596281]) and by Louisiana State University (Baton Rouge; Boyd Professor funds).
* E-mail tucker{at}lifesci.ucsb.edu; fax 805-893-4724.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.102.017459.
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LITERATURE CITED |
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TOP
INTRODUCTION
SUBFAMILY CAESALPINIOIDEAE
SUBFAMILY MIMOSOIDEAE
SUBFAMILY PAPILIONOIDEAE
WHAT CAN WE LEARN...
LITERATURE CITED
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