Bot. J. Linn. Soc., 66: 55-74. With 6 figures
January 1973
Carpel morphology and axis-sharing in syncarpy
in some Rutaceae, with further comments on
“New Morphology”
MICHEL GUEDES
Laboratoire de Ph,ytornorphologie, Ecole des Hautes Etudes,
Muskurn d’Histoire Naturelle, Paris
Accepted f o r publication June 1972
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Carpels in Choisya, Rufa, Poncirus and Citrus are peltate. In Citrus the style contains as many
isolated canals as there are carpels, and these canals are shown to be bounded by the
morphologically outer (lower) surface of the carpel. All instances exhibit an at least incipient
syncarpy, and the floral axis is always involved in the central merging of the carpels. This is
especially obvious here on account of vascular anatomy. Both peculiarities are probably much
more widespread than is generally allowed; some other examples are afforded. The axis of the
flower is certainly the same as that of the vegetative portion of the plant, and Meeuse’s concept
of a pseudo-axis in the flower cannot apply here.
CONTENTS
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Choisya ternata Kunth
. . . .
Ruta graveolens L.
. . . . .
Poncirus trifoliata ( L . ) Raf.
. .
Citrus medica var. limon L .
. .
Introduction
Observations
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55
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Citrus aurantium subsp. bergarnia (Risso & Poit.) Wight & Arn.
Discussion
. . . . . . . . . . . . . . . . . . . . . .
Carpel morphology
. . . . . . . . . . . . . . . . . .
Outer carpellary bundles
. . . . . . . . . . . . . . . .
Axis-sharing in syncarpy
. . . . . . . . . . . . . . . .
References
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58
58
60
61
62
62
66
66
69
70
73
INTRODUCTION
Like Corner (1966) I am more and more of a classical morphologist and
more and more proudly so. With respect to carpels, we were recently told again
by the well-known “neomorphologist” A. D. J . Meeuse (1971) that ovules “are
fundamentally borne on an organ of independent origin. . . which can only by
hook or by crook be forced into one of the rigid categories of Leaf, Stem and
Root of the Old Morphology”.
The situation, however, is perfectly clear. The plant itself chooses the right
category for its carpels to be placed in: it always transforms them
55
56
M.
GUBD~S
teratologically into leaves or other phyllomes. In a way, in Meeuse’s terms, the
carpel is “an organ sui generis at the post-telomic level of the cormophytic
evolution”. Functionally this is unquestionable, but something in the genome
enables it to produce an appendage intermediate in organization between the
carpel and a phyllome. This is undoubtedly an indication of some cryptic
relation between phyllomes, and these only, and carpels (see Guidts, 19668,
1970a; Gukdks & Dupuy, 1970, 1971).
Among Meeuse’s last criticisms are his remarks on the lack of vascular tissue
in the floral axis of several allegedly primitive Dicotyledons, which lead him to
contrive a peculiar pseudo-axis for their flowers; and he briefly mentions that
the same interpretation may hold for the “rosalean assembly”.
In these circumstances it may not be unwarranted to present some
observations on carpel morphology and axis-sharing in syncarpy of some
Rutaceous gynoecia, the more so as both problems still are of interest to “old”
morphologists as well. I t may also be useful to do so in a British journal, for to
a foreigner it is rather a pity that in the country of Mrs Arber, practically the
only active morphologist is a “new” one, Dr R. Melville,* whose opinions are at
variance with those of Professor Meeuse.
The axis was considered by Schleiden (1849) or Saint-Hilaire (1842) as
giving rise to all placentas, even in gynoecia with parietal placentation. Their
views, in some ways, are thus akin to those of Melville (see GuCdes, 1 9 6 6 ~ )On
.
the other hand, even among those morphologists admitting that the parietal
placenta is leaf-borne, some supported the axial interpretation of central ones.
In his great memoir on floral anatomy of 1875 (submitted in 1868), Van
Tieghem (1875) was able to show that parietal placentas can only be
leaf-borne, and so are the so-called axile ones; both as a rule have inverted
bundles, which cannot belong to a stele. The floral axis was first thought of by
him as giving rise to the central placenta of the Primulaceae, but after a fresh
study of the problem, Van Tieghem (1869) came to the conclusion that its
bundles, being inverted in contradistinction to his first description, could
belong only to the carpellary leaf. He therefore asserted that the floral axis
never bears any ovule. Despite sundry neo-morphological attempts to
resuscitate “stachyospory”, the classical “phyllosporic” interpretation is still
by far the most generally held, in my view rightly so (Guidks, 1966b).
This is not to say, however, that the axis takes no part in making up the
gynoecium. In some instances, Van Tieghem pointed out that inside the circle
of the inverted placental bundles of an axile placenta, another circle could be
seen with normally oriented bundles, prolonging the floral stele and
representing the upper part of the floral axis. The latter was coated with the
ventral carpel walls, provided with inverted placental bundles. This condition
he admitted for the Caryophyllaceae, but his conclusions regarding this family
were recently doubted by Bocquet (1959) and Rohweder (1967a), although in
my opinion the question needs reinvestigation with teratological material. In
the Ericaceae, Van Tieghem also saw such a vascularized axis in Rhododendron,
at least occasionally, and Moseley (1961, 1965, 1967) described the same in
Nymphueu and Nuphur.
Several instances in which the axis was considered to be present as the core
* See Melville (1969, with quotations of former works) for the latest state of his views.
CARPELS IN SOME RUTACEAE
57
of the syncarpous gynoecium were admitted only on account of their mode of
dehiscence, an interpretation which could not be confirmed, e.g. in the
Geraniaceae or Coriaria (Guidis, 1971). In others, only ontogeny was used to
support the interpretation and was “overplayed”, as in Nigella, where Troll
reported (wrongly, in my view) that the axis is present in the centre of the
ovary and between the lateral walls of the carpels (see GuCdPs, 1966a;
Rohweder, 1967b).
But Bosch (1947) in the Palmae, Leinfellner (1950) in the Liliaceae, Rao
(1954) in Ochroma, Wassmer (1955) in the Crassulaceae, Nair & Joseph (1957)
as well as Nair & Joshi (1958) in the Simaroubaceae and Schaeppi & Frank
(1967) in the Rosaceae provided cogent evidence, since in these instances,
although the axis above the carpel insertion has no vascular bundles (except in
Brucea of the Simaroubaceae), it appears to be free on top of the axile
placenta, above the basal fused portions of the carpels. Since the central mount
may be free at this level, it must necessarily be connected by some axial though
unvascularized tissue with the lower region of the flower, where stelar bundles
are still evident. I t would be highly desirable to have teratologic
transformations of such flowers into vegetative buds, for the axis in them
would probably be found to sever itself from the carpels and progressively
acquire stelar bundles.
In the Rutaceae, Hart1 (1957) had called attention to the sharing of the axis
in syncarpy, but Gut (1966) must be credited with very detailed observations
on the matter. As in the Nymphaeaceae and occasionally in the Ericaceae, the
gynoecium axis is sometimes vascularized with normally orientated bundles,
superimposed centrally to the inverted placental ones. My own work was at
first undertaken without knowledge of that of Gut, and has often confirmed it.
Even in instances where the axis neither appears free above the fused portion
of the carpels nor is found vascularized with readily recognizable bundles, its
presence may be detected at least basally from the occurrence of Van
Tieghem’s “transient axis” (axe transitoire) or “transient prolongation of the
axis”. Above the stamen level, notably in the Scrophulariaceae and the
Campanulaceae, various floral steles are still made up of normally orientated
bundles and thus appear to belong to axes, whereas on the outside carpel
locules are already apparent, vascularized by dorsal bundles emitted below
them by the stele. Only higher up does this stele break up, giving off the
inverted placental bundles which, moving outwards, can then vascularize the
placentas. In these cases, it appears that the axis is present at the base of the
placenta; but at higher levels, where there are only inverted bundles, it remains
to be seen whether non-vascularized axial tissue still occurs. This observation of
Van Tieghem has generally been overlooked, but will be found to apply to the
Rutaceae as well.
As regards carpel morphology, I have already called attention to the peltate
concept as a mere precision, though a most useful one, of the classical view,
only stressing that the union of the carpellary margins in the lower or ascidiate
region is congenital (Gutdis, 1966b, 1971). The ovules, which are but
carpellary leaflets (Guedts & Dupuy, 1970), necessarily prolong the carpellary
margins, which are free above, but can also be found free inside the ascidiate
portion, where the closure arises from congenital union along two submarginal
dorsal lines after inrolling of the margins proper (Guedes, 1966b, 1970b).
58
M
GUBDBS
Finally, the consideration of the congenital character and extension of the
union between peltate or non-peltate (epeltate) carpels has led Germanspeaking morphologists, notably Leinfellner, to a reassessment of the
morphology of the syncarpous gynoecium, which I have previously discussed
and supplemented (GuCdks, 1970b, 1971).
OBSERVATIONS
Choisyu ternutu Kunth
In this plant, the pentacarpellate gynoecium is practically apocarpous, but in
fact shows a syncarpous basal portion (Fig. 1B-C). The floral stele is not
prolonged above the level where it breaks up into lateral (ventral) bundles for
the carpels (Fig. 1). The floral axis thus appears flat above this region (Fig. lA,
arrow). This is in accordance with the observations of Gut (1966), but a point
not mentioned by him is that often (at least in my material) a further
carpellary whorl was formed above the normal one. Its carpels were mere
unvascularized horseshoe-shaped primordia, more or less regularly alternating
with the normal carpels. The floral apex had thus clearly retained its
organogenetic potency after the initiation of the normal carpellary whorl.
Below the point where the stele splits up, this has still normally orientated
bundles, although carpellary locules begin t o appear (Fig. 1B). We are at the
transient axis level. After the departure of the readily ramifying median
(dorsal) bundle, the stele has five intercarpellary normally orientated bundles.
They divide, and the ten issuing bundles become inverted and located by pairs
at the inner angles of the locules (Fig. IB-C). Each becomes extended
tangentially although no clear discrete bundle is produced parallel t o it (Fig.
ID-E). Each supplies an ovule (there are two such ovules per carpel), then
proceeds upwards, merging first with a horizontal branch from the median
bundle on each side (Fig. IA), then with vertical bundles from this branch and
with the division products of the median itself. Two lateral bundles thus enter
the style (Fig. l F ) , disappearing above at the stigmatic level (Fig. 1G). The
stigma is probably unifacial, but this point is difficult t o ascertain.
At first sight the two-levelled vascularization of the carpel, with its median
departing well below the laterals, seems at variance with the conventional
peltate carpel concept (Gukdks, 1971). However the general morphology is that
Figure 1. A-G. Choisyu tevnatu: A. Longitudinal section of the flower. T h e carpel on the left is
cut through its locule, that on the right tangentially through its wall. B-F. Cross-sections at the
levels of the transient axis (B), of the free apical dome with congenitally closed carpels (C) in a
normal flower, and a little higher up in a flower whose axis bears a second whorl of carpel
primordia (D). A t this level the carpels are only post-genitally closed. E. Detail of a carpel at the
latter level. 12. Base of the style of a normal flower. G . T o p of two styles devoid of vascular
bundles. H-L. Rutu gvuveolens; cross-sections of the gynoecium: H. Departure of the medians. I.
Transient axis level. J . T o p of the same, the stelar bundles began t o divide into laterals. K. T h e
laterals are formed and inverted. L. Hemisymplicate portion of the gynoecium. The style is
nearly free in the lower carpel. Carpels bulge o u t above. The very short zone of post-genital
carpel closure is very difficult to make o u t in an adult flower. Upper and middle left carpels are
cut in their congenitally closed regions, the other two in their post-genitally closed one. A axial
bundles, C’ carpels of the supernumerary whorl, 1. lateral bundles. Arrow in Fig. 1A indicates t h e
flattened axis dome; crosses in A and C indicate the horizontal branch of the median fusing
with a lateral.
59
CARPELS IN SOME RUTACEAE
L
60
M. GUEDOS
of such a carpel. Most often lateral (ventral) bundles arise separately from the
median, but at the same level as it does from the floral stele. That they may
depart somewhat above the median does not seem really troublesome, as will
be explained in discussion.
The carpel is congenitally closed at the level of the transient axis, and above
up to about ovular insertion, then a suture is obvious (Fig. 1D-E). The closure
has become post-genital at this level, but the carpel is peltate. The gynoecium is
syncarpous in that the five carpels have a short lower syncarpous zone (a
hemisyncarpous portion with incomplete fusion of their lateral walls is found
just above; see Gut, 1966). The floral axis is present as the core of this
syncarpous portion, free and dome-shaped above, but often still forming carpel
primordia.
I t will be noticed that the medians depart well below the carpellary locules
(Fig. 1A): they arise from the stele, but also receive some bundles connected
with stamen traces. The gynoecium is therefore located on top of a disk, which
may well be axial, or it might be carpellary, being a fusion product of adnate
lower spurs from the carpels. This will be a matter for teratology to decide. If
the carpels are transformed into leaves, then it will be seen whether or not the
disk is severed from the axis and emerges as an appendage of these foliar
carpels.
Rutu gruveolens L.
Many bundles connected with the stele ascend into the disk and also into the
carpellary walls before the departure of the medians (Fig. 1H). When these
medians have departed, the locules appear. The gynoecium is thus already in
existence, but four normally orientated bundles are found jn thc centre,
alternating with the locules. They cannot belong to inrolled carpellary margins,
and must be attributed to a transient axis. Somewhat higher up, they each
divide into two, turn about, and come to be located by pairs in an inverted
state at the inner angles of the locules. They have become carpellary laterals
(ventrals) like those of Choisya (Fig. 1J-K). Without ever merging into a
ventro-median, they vascularize the placentas (Fig. IK), then pass up into the
at first free styles, of which each has two bundles. The median bundle appears
to be unbranched or almost so: it does not penetrate into the style. The four
carpel styles are finally postgenitally fused along most of their upper parts.
Since the bundles going into the disk are of the same kind as those of the
carpel, except for the median, it seems that the disk can only be an appendage
of the carpels (see below in discussion).
The closure of the carpels up to the placentas is congenital, and Payer's
(1857) ontogenetic studies show that the margins are free above at first, so we
are clearly concerned with four peltate carpels.* The gynoecium is of course
syncarpous with a well-developed apocarpous portion separated from the
syncarpous one by a hemisyncarpous region (Fig. 1L). The axis takes part in
joining the carpels in the syncarpous portion; and, since they still have their
margins congenitally fused above that portion, it seems most probable that
despite their lack of lateral bundles, the carpels are already congenitally closed
* I n m y matcrial the placentas were notably lcss longitudinally extended than they are in Payer's
plate 15, fig. 20-21.
CARPELS IN SOME RUTACEAE
61
at the level where the axis is still apparent as a transient one (Fig. lJ),as they
are in the three upper carpels of Fig. 5F.
Poncirus trijoliuta (L.) Raf.
Syncarpy is much more advanced here and there is only one style, formed by
congenital fusion of carpel styles. Axis-sharing is also much more pronounced.
At the base of the disk (Fig. 2A) the stele is made up of several small normally
orientated bundles. As many of them as there are carpels depart outwards
(Fig. 2B) and each divides into three: one outer median and two placentals.
Each pair of the latter becomes inverted and its components fuse into as many
ventro-medians in front of each median (Fig. 2B-C). Outside the still remaining
axis stele there are then radial pairs made up of a (dorso-)median or dorsal
bundle and a ventro-median inverted bundle.
With the stele still obvious, carpellary locules appear between each
dorso-median and its opposite ventro-median (Fig. 2D). The peltate state of the
carpels is here especially unmistakable, since the ventro-medians indicate the
congenital closure of their margins (Guidts, 1971), and these carpels merge
centrally with a well-vascularized axis stump.
At this level many bundles have appeared in the outward ovary wall; they are
not connected with the median, although they may perhaps become so in older
flowers. Here too this wall is comparable in this respect with the disk, at this
stage almost unvascularized but later acquiring bundles which connect with
carpel and stamen traces and the axis. But in contradistinction to Rutu, these
supernumerary bundles are clearly located outside the dorso-median carpellary
bundles and their own branches (Fig. 2C-G).
Each dorso-median emits several branches, but two of them, located distally,
soon become more developed and will be termed the medio-laterals* (Fig. 2E).
They generally become obscured anew in the upper part of the ovary
(Fig. 2F-G).
The ventro-medians are short and limited to the sterile portion of the
carpellary locules. Higher up they divide into their two constituting placentals
(Fig. 2E) and these vascularize one or two pairs of lower ovules, then disappear
by fusing with new carpel bundles that have just arisen from the axis.
The axis bundles indeed move to the outside. The stele is thus broken up
into as many inverted bundles as there are carpels, and each of these bundles is
located at the level of a septum (Fig. 2F-GI J ) and emits branches vascularizing
all the upper ovules of two neighbouring margins from two different carpels.
Basically the same disposition is seen as in Choisya and Ruta, but here at the
level of the transient axis there is already a ventro-median supplying a lower
set of ovules. The inverted bundles are fused laterals or synfuterufs, and often
divide upwards into two laterals (Fig. 21).
Above the point of subdivision of the stele there is still a bulky
parenchymatous central tissue, and it is impossible t o make up one’s mind
whether it is already carpellary or still axial in nature. The latter view obviously
applies to Gut’s flowers, where some axial vascular tissue was found above the
departure of the laterals up to the base of the style.
* Should the median be called dorsal, as is often done, then they would be the dorso-laterals.
M. GUEDOS
62
The style has one transmitting canal per carpel, and the method of its
appearance is analogous to that described by Van Tieghem (1875) in Citrus. At
the level of the upper pair of ovules (Fig. 2G, J ) a deep notch is seen between
their “roots”, lined with a peculiar glandular epidermis of the same kind as that
of the transmitting canals. While the ovules disappear, the notches become
canals by the fusion of their outer borders and each carpel has thus two radially
superposed cavities: the outer now sterile locular one and the conducting inner
one (Figs 2H and 51). The medians and medio-laterals disappear along with the
carpellary locules and only the transmitting canals pass up into the style, with
the synlaterals or their constituting bundles (Fig. 21, K).
Citrus medicu var. lirnon L.
In the lemon, the organization of the gynoecium is basically the same. The
medians, however, travel up without branching for some length (Fig. 3A) even
after the appearance of the carpellary locules (Fig. 3B). ’They emit bundles
which give rise more or less clearly to mcdio-laterals which, in turn, generally
merge with their neighbours from adjacent carpels. The still obvious axis then
emits placental bundles, here unconnected with the medians. They may fuse in
pairs to form ventro-medians, but do not generally do so (Fig. 3C). As in
Poncirus, they vascularize the lower ovules, then disappear by uniting with
inverted bundles arising from the break-up of the stele. These united bundles
(synlaterals) vascularize the upper ovules, then proceed into the style and may
divide radially or tangentially into two at the stigmatic level (Fig. 3H-I).
The way of forming the stylar transmitting canals is exactly the same as in
Poncirus and is especially clear in this case (Fig. 3F-H).
No axial vascular tissue is left after the departure of the synlaterals, and the
existence of unvascularized stelar tissue can neither be ruled out nor
demonstrated. But the jlorul axis is present ut leust u p to the level ofdepurturc
o j the synluteruls.
As in Poncirus, many bundles are found distally in the ovary wall, but here
there are many connections between these and the median and medio-lateral
bundles.
Citrus aurantium subsp. hergumia (Risso & Poit.) Wight & Arn.
In my flowers the gynoecium was sometimes disturbed at the stylar level:
the styles burst and corrugated little blades were seen emerging from its inside.
The ovary proper was normal and able to mature into fruit.
~
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~.
. . ~
~
~
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~
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Figure 2. Poncivus trifoliutu. A-I. Cross-sections of the gynoecium: A. Floral stele at disk level.
B . T h e medians depart and each emits two placentals. C. T h e placentals have fused by pairs into
ventro-medians. The floral axis remains. D. L.ocules appear. E. Lower ovules vascularized by
split ventro-medians. F . Fading o u t of t h e placentals (split ventro-medians), breaking up of the
stele into synlaterals (fused laterals). G. Synlaterals supplying upper ovules. Appearance of
notches to become as many stylar canals. H . Sterile locules, stylar canals closed. Between them
the synlaterals remain and may divide. All other bundles fuse and d o not reach higher. I . Style.
Canals extended, all synlaterals divided except the upper one. J-K. Interpretative schemes: J. A
carpel with marginal ovules prolonging inrolled margins, with inverted synlaterals. T h e
morphologically upper surface lines the cleft between ovule “roots” and gives rise to the
transmitting tissue. K. Stylar canal, theoretical location of the laterals. This is rarely so clear,
however. Lettering as in Fig. 1. MI medio-lateral bundles (see text), P piacentals, SI synlaterals,
T t transmitting tissue, Vm ventro-medians. In J-K, broken line indicates the limits of the carpel
and arrows the way of inrolling of its wall.
CARPELS IN SOME RUTACEAE
63
64
M . GUkDES
Figure 3 . Citrus medica var. limon; cross-section of the gynoecium: A. Medians emitted. B.
Appearance of the locules. C . Branching off of the placentals fusing occasionally into
ventro-medians. D. Breaking up of the stele into synlaterals. E . Above the fertile zone,
appearance of the stylar canals. F . Locules nearly obliterated. Srylar canals well developed. G.
Style base. Only stylar canals represent the carpellary cavities. Synlaterals still apparent, other
bundles disappearing by fusing with each other. H. Style. I. Stigma. Most synlaterals have
divided. Lettering as in Fig. 1 B and C. Sml, fused medio-laterals. Arrows in E-F indicate
carpellary margins (see Fig. 2 3 ) .
Although only gynoecia normal in appearance were studied in detail, they
were always found to be affected by the same only less obvious anomaly, but
their ovaries were also perfectly normal.
The stele comprises many normally orientated bundles from which the
carpellary medians depart in the usual way (Fig. 4A). They emit laterals, which
fuse into ventro-medians or remain discrete, and medio-laterals (Fig. 4A, B).
s9
66
M. GUEDES
At that level the still relatively bulky stele has emitted other bundles, which
soon divide into threes: they form the vascularization of a second carpel whorl
(Fig. 4E). These carpels do not acquire a clear carpellary morphology, but only
assume the shape of corrugated little leaves, which in these instances remained
hidden within the style, but were seen to break out of it in more modified
flowers. The stele is seen as residual vascular tissue after the departure of these
carpel traces (Fig. 4E), then the whole floral axis comes to an end and the
supernumerary carpels are freed in a central stylar cavity, except for some
fusions between themselves and the wall (Fig. 4F). The phenomenon is
fundamentally the same as that produced by the free supernumerary carpel
primordia in Choisya, but the second carpellary whorl is here imprisoned in the
cavity bounded by the fused stylar portions of the normal carpels. At the
stigmatic level (Fig. 4H) the cavity is post-genitally closed above and its wall
must be torn away if the supernumerary carpels are to unfold outside.
Although Gut’s flowers did not show such supernumerary carpels, their
floral stele was prolonged above the level of departure of the synlaterals, as one
or two late-differentiating bundles reaching up to the base of an empty stylar
cavity, evidently that occupied by the second carpel whorl in my material.
Such a little “bud” terminating the flower axis was also seen occasionally by
Van Tieghem (1875) in Rhododendron and only then was the floral stele still
vascularized in the middle of the axile placenta. The floral stele of the Rutaceae
is seen for at least some distance, even in the absence of this bud. On the other
hand the bud, when more developed, may produce fertile carpels which may
characterize normal taxa (e.g. Nolana paradoxa, Di Fulvio, 1971) perhaps of
teratological origin (Van Steenis, 1969). I t may also form another flower, an
inflorescence or a vegetative shoot. All these productions are mediun
proliferations, i.e. those arising from resumption of the terminal apex activity,
whereas the initiation and development of lateral buds of various floral
phyllomes defines the lateral proliferations (Godron, 1877). And since floral
phyllomes themselves are by no means fundamentally modified in such
instances, be they sepals, petals or carpels, it is unconceivable that any lateral
bud should be normally incorporated into them, as several old theories and
Melville’s one would have us believe. Lateral buds are lacking in the axils of
floral phyllomes as they occasionally are in those of vegetative ones, e.g. in
Linaria.
When in Citrus the supernumerary carpels assume the shape of a little
orange, the well-known “navel-orange” arises (Leroy, 195 3). More or less
identical abnormalities are known in apples, the Cruciferae and various other
plants (Masters, 1869: 388). In Sinocrussula yunnanensis of the Crassulaceae,
Wassmer (1955) has also reported the occurrence of one or two supernumerary
carpels inside the normal carpellary whorl.
DISCUSSION
Carpel morphology
A peltate carpel is nothing more than a carpel with the lower margins
congenitally fused. In most instances, even without studying ontogeny such a
congenital fusion will be apparent from the lack of a suture, which would be
CARPELS IN SOME RUTACEAE
67
visible if post-genital fusion of the margins had occurred. Congenital fusion is
even more obvious when a ventro-median is encountered. This trace belongs to
both carpellary margins and arises from fusion of both their bundles and
separates into two again above. Along the closure level there is only one bundle
for two margins, which therefore can only have developed as a whole.
In some peltate carpels, below the locule a solid unifacial petiole (ix. one
bounded all round by the outer or dorsal surface) is found. I t has a
(dorso-)median and a ventro-median, or the two inverted laterals homologous
with the latter. This disposition is also that found in many unifacial petioles of
vegetative leaves. In these as in carpels, at the lamina level the margins may be
congenitally fused below, and the leaf is ascidiate (or peltate) or free. A carpel
with such a unifacial petiole but with margins not congenitally fused is termed
latent-peltate by Troll (see Guidis, 1971).
In this connection two points must be discussed. Firstly, style unifaciality:
in the same way as both leaf margins may meet above the lamina, the meeting
level being topped by an unifacial leaf-tip (sometimes very Iong as in
Ornithogalum cazddatum, whose specific epithet is taken from it), such a
unifacial tip may exist in carpels and make up the style, as will be shown
presently. Secondly, as already mentioned in connection with Choisya, an
explanation is necessary for the departure of lateral bundles above the median,
an arrangement which, although not unknown, is not a classical feature of
floral anatomy.
I have shown that the style is often unifacial (Gutdes, 1968, 1971), with
the possible downward proliferation of its lower cross-zone into an “apical
septum”. The situation is uncertain in Choisya and Ruta, but in Poncirus and
Citrus there occurs a peculiar aspect of style unifaciality which is very
reminiscent of that described in Sempervivum (Guidis, 1966a). The Rutaceae,
indeed, is one of the families in which the leaflet theory of the ovule was
established (Celakovsky, 1874, in Dictamnus). As ovular leaflets, the ovules are
strictly marginal; in these circumstances the process of making up the stylar
canal of each carpel is as indicated on Fig. 51; the inrolled carpel blade bounds
it by means of its (hatched) morphologically outer or lower surface. At the
stylar level the carpellary locule proper disappears. The style is unifacial, since
only its morphologically outer surface is apparent, but it is hollow, and its
canal, too, is bounded by the outer surface. Furthermore each style of course
merges with its neighbours.
In this connection a further example of stylar unifaciality is provided by
Linaria vulgaris (Scrophulariaceae). Above the synascidiate portion of the ovary
(Fig. 6A), the base of the symplicate one is still fertile, with inrolled margins
(Fig. 6B). I t looks as if the ovules were borne on the outer carpellary surface
(broken arrows). Higher up, the ovary becomes sterile and its cavity more and
more reduced (Fig. 6C-D). The carpellary margins are located in the position
indicated by arrows in Fig. 6D, since, some distance below, the ovuliferous
placentas are located there. The transmitting tissue thus appears on the
morphologically outer (lower) carpellary surface (Fig. 6E), as has been
demonstrated teratologically in Merremia (Convolvulaceae) (Gutdes, 1968). In
Fig. 6F only one carpellary locule has disappeared, the other shows a ventral
notch reminiscent of that in Poncirus or Citrus. In Fig. 6G the notch is closed
to form a transmitting canal, which ends shortly above this point. In all
?4
L
I\
L
L
M
Vm
“a
3
Figure 5. Interpretative schemes. A-E. Carpel vascularization: A. Ruta, Choisya. B. Poncirus. C . Citrus medica. D. Citrus aurantium with supernumerary carpels. E.
Conventional peltate carpel, ventro-median originating b y fusion of laterals, whereas it arises from merging of placentals in B-D. See text. F-I. Cross-sections: F.
Gynoecium of Rutu or Choisya a t the transient axis level, with carpels theoretically severed from the axis. Three (upper and lateral) carpels peltate (most probable
interpretation), lower carpel ventrally open. G. Same. Upper and right carpels cut just above the symplicate zone, b u t still congenitally closed. No axis in t h e centre.
Lower and left carpels cut above departure of t h e laterals, now inverted, b u t with a remnant of the axis, unvascularized. Compare Fig. 1C. H . Carpel of Poncirus or
Ci?rus a t t h e transient axis level, below lower ovules, indicated as severed from t h e axis. Two laterals are in t h e ventral carpel wall, and inverted, while t h e axis
retains its normally orientated bundles. 1. Formation of a stylar canal in Poncims and Citrus. The axis may exist, though unvascularized (broken circle above). The
“roots” of t h e ovules, i.e. t h e distal portion of the carpel wall, give rise to the canal bounded all round b y the outer carpellary surface (hatched, as in H). Lettering
as in previous figures.
CARPELS IN SOME RUTACEAE
69
instances the style has a central solid core of transmitting tissue (Fig. 6H). This
should be interpreted in the way indicated by Fig. 61-K (Fig. 61 schematizes
Fig. 6C-D and Fig. 65 and K do the same for Fig. 6E and G respectively).
In all carpels studied the median departs well below the laterals or placentals.
This is known elsewhere, e.g. in Caltha (Ranunculaceae) (Skipworth, 1970a)
and the Magnoliaceae, but the matter is more complicated in the latter case
because medians and laterals are not connected with the same part of the stele.
Such a difference in the departure level of medians and laterals of course occurs
in all flowers with transient axes (Van Tieghem, 1875).
A conventional peltate carpel (Fig. 5E) wiIl have its median and two laterals
departing at the same level, the stele being used up in vascularizing the carpels.
Somewhat higher up, the laterals will fuse into a ventro-median, liable to
separate its two constituting laterals a little above.
In such carpels as those of Ruta or Choisya (Fig. 5A), after the departure of
the median a transient axis remains, and is used up above in giving out the
laterals, which do not fuse into ventro-medians. In Poncirus (Fig. 5B) the stele
gives off a median and two placentals and the latter fuse to form a
ventro-median ; but a central transient axis remains nonetheless and emits two
laterals (fused with their neighbours to form synlaterals). The axis may even
proceed upwards as residual vascular tissue (Gut, 1966). In Citrus medica the
organization is the same, but the placentals are produced a little above the
medians (Fig. 5C); and in Citrus aurantium, while the latter situation still
occurs, the axis, far from being used up in producing the laterals, vascularizes a
further whorl of carpels (Fig. SD).
An alternative view in terms of Melville’s theory could be that only this
portion vascularized by the median is the carpel proper, with some axillary
system sharing in the make-up of the transient axis by coming close to the
homologous ones from other carpels. But this approximation into something so
closely identical with a floral stele would be rather miraculous; and it would
still be necessary to explain why on departure the bundles of the transient axis
split and turn about so as to assume orientations just fitting those of bundles of
involute carpellary blades. The latter remark would also apply if it were
admitted that a floral stele indeed exists but that it vascularizes a carpel
(median portion) first and then two peculiar kinds of placental appendages.
In Ruta or Choisya one may ask whether at the transient axis level the
carpels are open ventrally (Fig. 5F, bottom carpel) or closed by a
non-vascularized ventral suture. This cannot be decided, but in the other plants
studied the existence of a ventro-median or its constituent inverted placentals
(Fig. 5H) makes the second interpretation obvious. I t should be considered
very likely in Choisya and Ruta as well.
Outer carpellary bundles
The bundles outside the median in carpel walls of Citrus and Poncirus might
lead one to think that an axial cup coats the whole ovary. They are
comparable, however, with those located at the same tangential level as the
medians in Ruta. In the latter case, moreover, the carpel, though free, still
contains them. If these bundles belong to the axis, it will be necessary to
consider the latter as emitting four tags of tissue deeply fused with the
70
M . GUBDES
carpellary walls. I t is much more natural, as Gut (1966) has done, to consider
these bundles as belonging to the carpellary wall. In Coleonema, however, the
axis really builds a distal cup free from the ovary (Gut, 1966).
Although no detailed ontogenetic study was carried out, it appears from the
young flowers studied that these outer bundles, at least as far as xylem is
concerned, arise inside the bulk of the carpellary walls, then join the main
carpellary bundles and occasionally the transient axis, without these
connections becoming very numerous. I t should be remembered that such
plexuses are also found in vegetative leaves, notably among the Gramineae. I
have seen similar bundles in the gynoecium of Yucca, in the Liliaceae.
These bundles are also fully comparable with those in the carpels of the
Nymphaeaceae, which, as Moseley (1965) points out, can be perfectly
carpellary. As early as 1821, De Candolle had envisioned a cup around the
gynoecium formed by the torus or receptacle. At that time he did not speak of
it as axial. Related ideas were independently restated by Troll (1933), who
spoke of axial tissue around the carpels, but with erroneous arguments from
fruit dehiscence (see Moseley, 1965). The same opinion was held by De
Candolle in respect of the gynoecium of Citrus and Papczver; but when the
latter, also provided with analogous outer bundles, splits into its component
carpels and these turn into stamens (i.e. into phyllomes without any axis),
nothing like an axis or axis tag can be seen to free itself and/or disappear
(Guedks, 1969). So in Papaver, the Nymphaeaceae and the Rutaceae the same
interpretation must hold true. In vegetative leaves, too, several tangential rows
of bundles are to be found at the petiole level. I t will be interesting to look for
the fate of these outer carpellary bundles when a Citrus carpel is turned into a
stamen, which has been reported (see Le Maout, 1844), but as usual without
detailed investigations.
Axis-sharing in syncarpy
The participation of the axis is obvious when a central vascular core is seen.
When a free axial stump is found between the carpels, it is clear that the axis
exists below, even if unvascularized. The same interpretation applies if a
dome-shaped unvascularized axis is able to produce carpel primordia, as in
Choisya or Sinocrassula (Wassmer, 195 5). In Nuphar (Moseley, 1965),
depending on the species, the stelar tissue may or may not exist although the
gynoecium retains the same shape, and it is reasonable to assume that the latter
is provided with an axis core in both instances.
Purely ontogenetical or histogenetical observations, on the other hand, often
do not appear to be reliable. I t will remain very difficult in most cases to decide
whether a cell group is cauline or foliar, although histological differences may
help in this respect (Wassmer, 1955). We must as a rule wait until they give rise
to clearly recognizable tissue (e.g. normally or inversely orientated bundles).
l h i s was already the conclusion of a survey by Vidal (1900).
The transient axis is precisely a clear indication of the presence of the axis at
the base of several gynoecia without residual vascular tissue above the level of
departure of lateral or placental bundles. I t has been generally overlooked since
Van Tieghem’s and Vidal’s works, but may be detected in the illustrations of
many modern papers, e.g. in the Ericaceae (Palser & Murty, 1967), in
P
C
M
Figure 6 . Linaria vulgaris. Intermediate zone between ovary and style. A. Upper portion of the synascidiate zone: b o t h carpels are congenitally united, each in turn
being peltate. B. Symplicate zone, carpels congenitally united b u t both open. C. Same, above. D. Style base. T w o little locules. Arrows indicate carpel margins,
prolonged below b y t h e placentas. E-F. Lower locules disappearing. The sections are taken from another gynoecium in which some ovules were borne at a very high
level. Their location corresponds to that of the location of carpel margins indicated b y arrows in D. G. Another gynoecium, above lower locule, upper one closed in
the same way as in Poncirus, leading to the appearance of a stylar canal, soon obliterated above (H). I-K. Interpretative schemes, upper carpellary surface hatched: 1.
Interpretation of C-D. J. Same of E. K. Same of G . The stylar canal, as in the Rutaceae, is bounded b y the morphologically upper surface. Lettering as in previous
figures.
72
M GUEDBS
Geissoloina (Dahlgren & Rao, 1969) and especially in the Crassulaceae
(Wassmer, 1955).
In Choisya and Ruta the upper limit of the transient axis is located where
the normally orientated bundles split and turn about (Fig. l B , J-K). I t may be
(Fig. 5G, lower left) that some unvascularized axial tissue remains at the level
of Fig. 1K in Kzita, but this cannot be decided upon. The very flat axis dome is
free above that level in Choisya (Fig. IC).
In Poncirus and Citrus rnedica the same restraint must be exercised in the
interpretation of the unvascularized central tissue, with respect to a much
longer portion of the gynoecium. Clearly the axis reaches as high as the level at
which the central normally orientated bundles pass out and turn about to
become the synlaterals (Figs 2F and 3D). In Gut’s (1966) material this axis was
well defined up to the upper end of the residual strands above the level of
departure of the synlaterals. In both instances, however, the nature of the
unvascularized core of the style is doubtful. ‘I’eratologically, if it were to
develop normally orientated stelar bundles without any other modification of
the gynoecium, it could be safely claimed as axial. A related situation is that of
the central placenta of the Primulaceae, on top of which a bud has often been
described teratologically, although its bundles are inverted or centric and
probably carpellary. In fact no detailed morphological and anatomical study oE
these instances ever seems to have been published.
N o such doubt exists in Citrus aurantium. We have seen that the style of our
gynoecia is hollow and encloses the supernumerary carpels. Even in the normal
gynoecium without such carpels, the style is hollow (Gut, 1966). There can be
no axis in its centre, the latter reaches only up to the upper level of the locule,
terminating in much the same way as in Choisya.
So syncarpy may often involve the sharing of the axis and is not always so
simple as Eyde (1967, Figs 1 to 4), for instance, depicts it, although of course
many such simple carpel fusions will be found. Coriuria vziscifolia recently
provided quite a rudimentary stage (Guedis, 1971).
I can see no reason why this axis should be false. The fact that it may have
no stelar tissue just below its tip, stressed by Meeuse (197 l), is certainly no
problem at all. For the tip of any vegetative apex has no vascular tissue either.
N o ontogenetic discrepancy exists between vegetative and floral apices. On the
contrary, as I have explained elsewhere (Guedts, 1970a), the very same
students of apices of the Plantefol-Buvat school who tried t o demonstrate that
the floral apex and its appendages can have nothing in common with the
vegetative apex and its phyllomes above the calyx level now put emphasis on
the “transient stage” when the apex is intermediate in structure between the
two states. The two types of apex are thus not fundamentally different. By
manipulating eco-physiological conditions, they are able to have an apex that is
cytologically nearly floral produce easily recognizable vegetative leaves.
Conversely, in Michelia Tucker (1960) saw that the floral apex is remarkable in
retaining a zonation and a plastochronic arrangement like those of a vegetative
one, and other similar instances are on record. If therefore the floral apex is
false, and produces a false axis, so is the vegetative one. The point is that both
are fundamentally alike.
As to the vascularization, one can certainly not envisage that stamens and
carpels are here borne by axillary branches of perianth members: the stelar
CARPELS IN SOME RUTACEAE
73
organization is clear throughout the flower (Tillson & Bamford, 1938), and
there is only one stele supplying all appendages. Taken too literally, the
vascularization of magnoliaceous flowers might perhaps lead to such a view
because of the cortical system. But at any rate only the laterals would then be
borne on axillary axes from the bracts, all appendages still derive their medians
from the stelar tissue proper. I t is thus much better to think of the matter as a
very peculiar condition, advanced in its own way, as are many other characters
of these far too morphologicalIy praised plants (see also Skipworth, 1970b).
With respect to Luctoris (Carlquist, 1964), upon which Meeuse places so much
stress, I fail to see why the three bundles, each of which sends forth traces to
one petal, two superposed stamens and a carpel, cannot be conventional stelar
bundles.
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