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Year: 1998
Theligonum cynocrambe: Developmental morphology of a peculiar
rubiaceous herb
Rutishauser, Rolf ; Decraene, Louis P Ronse ; Smets, Erik ; Mendoza-Heuer, Ilse
Abstract: The annual Mediterranean herbTheligonum cynocrambe shows a peculiar combination of morphological characters, e.g., switch from decussate to spiral phyllotaxis with 90-100° divergence, combined
with a change from interpetiolar to lateral stipules, anemophily, lack of calyx, flowers often dimerous
to trimerous, corolla fused in both male and female flowers, male flowers extra-axillary, with 2-19 stamens per flower, female flowers axillary, with inferior uniovulate ovary, basilateral style and perianth,
nut-like fruits with elaiosome. In male flowers the androecium emerges as an (uneven) elliptical rim with
a central depression. This common girdling primordium is divided up into several stamen primordia. In
male flowers with low stamen number the stamen primordia may occupy the corners alternating with the
corolla lobes. There are no epipetalous androecial primordia that secondarily divide into stamens. Male
flowers occasionally show a hemispherical base that may be interpreted as remnant of the inferior ovary.
In female flowers a ring primordium grows into a tube on which the petal lobes arise. The perianth and
style become displaced adaxially by uneven growth of the inferior ovary. The ovary is basically bilocular.
The lower region of the ovary is provided with a septum that is overtopped and hidden by the single
curved ovule.Theligonum is referred to theRubiaceae-Rubioideae, with theAnthospermeae andPaederieae
as most closely related tribes
DOI: https://doi.org/10.1007/bf00984724
Posted at the Zurich Open Repository and Archive, University of Zurich
ZORA URL: https://doi.org/10.5167/uzh-156572
Journal Article
Published Version
Originally published at:
Rutishauser, Rolf; Decraene, Louis P Ronse; Smets, Erik; Mendoza-Heuer, Ilse (1998). Theligonum
cynocrambe: Developmental morphology of a peculiar rubiaceous herb. Plant Systematics and Evolution,
210(1-2):1-24.
DOI: https://doi.org/10.1007/bf00984724
Pl. Syst. Evol. 210:1-24 (1998)
--Hant,
Systematics
and
Evolution
© Springer-Verlag 1998
Printed in Austria
Theligonum cynocrambe: developmental
morphology of a peculiar rubiaceous herb
ROLF RUTISHAUSER,LOUIS P. RONSE DECRAENE, ERIK SMETS, and ILSE MENDOZA-HEUER
Received July 29, 1996; in revised version December 13, 1996
Key words: Rubiaceae, Rubioideae, Theligonum cynocrambe. - Developmental morphology, life history, flower structure, systematics.
Abstract: The annual Mediterranean herb Theligonum cynocrambe shows a peculiar
combination of morphological characters, e.g., switch from decussate to spiral phyllotaxis
with 90-100 ° divergence, combined with a change from interpetiolar to lateral stipules,
anemophily, lack of calyx, flowers orten dimerous to trimerous, corolla fused in both male
and female flowers, male flowers extra-axillary, with 2-19 stamens per flower, female
flowers axillary, with inferior uniovulate ovary, basilateral style and perianth, nut-like fruits
with elaiosome. In male flowers the androecium emerges as an (uneven) elliptical rim with
a central depression. This common girdling primordium is divided up into several stamen
primordia. In male flowers with low statuen number the statuen primordia may occupy the
corners altemating with the corolla lobes. There are no epipetalous androecial primordia
that secondarily divide into stamens. Male flowers occasionally show a hemispherical base
that may be interpreted as remnant of the inferior ovary. In female flowers a ring
primordium grows into a tube on which the petal lobes arise. The perianth and style
become displaced adaxially by uneven growth of the inferior ovary. The ovary is basically
bilocular. The lower region of the ovary is provided with a septum that is overtopped and
hidden by the single curved ovule. Theligonum is referred to the Rubiaceae-Rubioideae,
with the Anthospermeae and Paederieae as most closely related tribes.
Theligonum cynocrambe is an annual prostrate herb with shoots of 5-20(-75) cm
length, with cordate and petiolate foliage leaves (up to 2.5 cm long), and
inconspicuous flowers arising from the same nodes as the foliage leaves (Fig. 1).
Theligonum cynocrambe occurs in the Mediterranean region (from Syria to
Portugal and Morocco) and on the Canary Islands. It is often found growing on
damp or shady solls, rocks and walls (ULBRICn 1933, 1934). The genus Theligonum
L. consists of three species that show a disjunct geographic distribution in the
Northern hemisphere: one Mediterranean species (T. cynocrambe L.) and two
Asiatic species. Theligonum japonicum OKU~O & MAKINO (from Central and S
Japan) seems to be perennial and monoecious (YAMAZAKI1993). Theligonum
macranthum FRANCH. (from W China, former Tibet) is annual and supposedly
dioecious (ULBmCH 1933, 1934; PUFF 1986: 520).
2
R. RUTISHAUSER8Z al.:
Theligonum is now regarded as a member of the Rubiaceae (WUNDERLICrI1971;
ROBBRECHT 1988, 1993; THORNE 1992; NICHOLAS& BAIJNATH 1994; BR~MER & al.
1995; NATALI& al. 1995; BREM~R 1996; MANEN & NATALI 1996) or as a closely
related family within the Gentianales (DAHLGREN 1989) or Rubiales (CRONQUIST
1981). Features in common with Asteridae - and unlike the Caryophyllidae - are,
e.g., the tubular perianth, S-sieve tube plastids, iridoid compounds, seeds with
endosperm, and the unitegmic tenuinucellate ovules (WUNDERLICH1971, CRONQUIST
& THOm~Ein BEHNKE & MABRY 1994: 5--25).
In order to stress the homology with the corolla of other Rubiaceae, the
perianth of Theligonum flowers (both sexes) is interpreted as a corolla (with fused
petals). This view is based on the assumption that the calyx is totally suppressed.
Such an assumption seems to be justified because calyx reduction as an
evolutionary trend is also observable in other Rubiaceae (RUTISHAUSER1985, PUFF
1986, ROBBe,ECHT 1988: 74). Nonetheless, the neutral term "perianth" is preferred
here, as it avoids circular reasoning.
There is already a considerable amount of valuable information on
Theligonum. Some developmental and morphological data, however, are still
lacking or have been misinterpreted, especially with respect to the primordial
stages of foliage leaves, stipules, male and female flowers, and micromorphological data. Since BALICKA-IWANOWSKA(1897), SCHNEIDER (1914), ULBRICH
(1934), WUNDERLICH (1971) and ROBBRECm: (1988) it is believed that the
male flowers show secondarily increased stamen number due to the presence
of two or three common epipetalous primordia that divide into 6-30 stamens.
Such a dédoublement of the androecium in Theligonum would be exceptional
for the Rubiaceae and most other Asteridae (ROBBRECHT 1988: 85). Other
exceptions in the subclass would be Coprosma nepheIephila within the
Rubiaceae (FLORENCE 1986), the Hoplestigmataceae (RONSE DECRAENE &
SMETS 1995) and possibly the Dialypetalanthaceae (RoBBm~CHT1993, PIESSCrIAERT
1995). Another hypothesis considers the male flowers as pseudanthia consisting of naked flowers with about four stamens each (WtrNDEaLICH 1971).
Pistillate flowers are interpreted as unicarpellate by most authors. However,
Wunderlich postulates a derivation from two carpels, linking Theligonum with
the basically bicarpellate Rubiaceae. These statements will be tested in this
paper.
Materials and methods
Material was collected either in the wild (Sardinia, collections 1982/1995) by the first
author, or grown from seed at the Botanical Institutes of Leuven and Zürich. Seed was
obtained from the wild (Sardinia) as well as from the Botanic Gardens of Göttingen,
Glasgow and Marburg. Plants from these three gardens did not differ morphologically.
Whole plants were fixed in formalin - acetic acid - ethyl alcohol (FAA) and later stored in
70% ethanol. Voucher specimens (herbarium and pickled) are kept at the Botanical
Institutes of Leuven (LV) and Zürich (Z). For the scanning electron microscopy the
dissected shoot tips were dehydrated in acetone or dimethoxymethane, then critical-point
dried with carbon dioxide and sputter-coated (Au). The micrographs were taken with a
Cambridge $4 (Z) and a Jeol JSM 6400 (LV) scanning electron microscope at 20 kV.
Developmental morphology of Theligonum
3
For light microscopy the material was run through an alcohol and alcohol-tertiary
butanol series and was hext embedded in paraffin. Serial sections, 10gin thick, were
stained with safranin and fast green.
Results
Foliage leaves: from decussate to 1/4 spiral phyllotaxis. There is a remarkable
switch from decussate to spiral phyllotaxis that is not common in other genera of
flowering plants. Cotyledons and seedling leaves show decussate phyllotaxis with
membraneous interpetiolar stipules (Figs. 3-4). The cotyledons do not differ
morphologically from the leaves; they also bear shoot buds and colleters in their
axils. There are (2-)3- 4(-6) leaf pairs (including the cotyledons) prior to the switch
to the helical (alternate) phyllotaxis of the adult plant. Each vegetative axillary
shoot starts with a few leaf pairs before switching to an alternate phyllotaxis.
Vegetative axillary shoots in addition to pistillate flowers are confined to the lower
part of the main stem (nodes 1-3). Higher up only pistillate flowers are produced in
the leaf axils.
The spiral phyllotaxis of the adult plant is unique among angiosperms. The
foliage leaves (each with two lateral stipules) are arranged along a helix with c.
90-100 ° divergence (Figs. 1, 2, 51-53; LOISEAU1969). This type is called 1/4 spiral
phyllotaxis because the divergence is close to 90 ° (ULBt~ICH 1933, 1934). This
phyllotaxis type may be seen as a case of extreme anisophylly, with the (+) leaves
of the basically decussate pattern arranged along a helix, whereas all ( - ) leaves are
nearly or completely suppressed (Im,~ISCH 1856; ROBB~CaT 1988, 1993). Also the
stipules at each node are unequal, at least during their development, with the
anodic stipule (Sa) 1 favoured as compared to the cathodic one (Sc2 in Figs. 6-8,
11, 51-53, see LOISEAU1969). The anodic stipule (e.g., Sa4 in Fig. 51) of a leaf is
adjacent to the next younger leaf (3) whereas the cathodic stipule (Sc4) is closer to
the next older leaf (5 in Fig. 51). Theligonum shoots show a slight anisophylly
already in the lowermost decussate zones (e.g., Figs. 2, 5). Younger stages of the
development of the shoot show stipules which are initially larger than the
associated leaves (Figs. 5-7). Stipules may bear an apical gland or colleter. The
switch to the 1/4 spiral arrangement is not as gradual as described by PUFF (1986:
519). Only in a few nodes of the transition zone rudiments of the normally
suppressed ( - ) leaf may be observed (IRMISCH 1856, EICHLER 1878, SCHNEIDER
1914). We occasionally observed a short scale in the position of the ( - ) leaf.
1 Explanation of the terms anodic and cathodic: The terms anodic and cathodic are used
in shoots with a spiral phyllotaxis and asymmetric leaf sheaths and/or unequal lateral
stipules. The anodic stipule points towards the distal end of the ontogenetic helix whereas
the cathodic stipule points towards the proximal end (LoISEAU1969, KIRCHOFF• RUTISaAUSER 1990). In Theligonum with spiral phyllotaxis and two male flowers opposite the
leaves, these two flowers (e.g., ~a4 and ~c4 in Fig. 51) are also positionally defined with
respect to the direction of the ontogenetic helix. The anodic flower (e.g., ~a4) is closer to
the anodic stipule (Sa4) which is covering the next younger leaf (3 in Fig. 51). The cathodic
flower (e.g., c~c4) is closer to the cathodic stipule (Sc4) that is in front of the next older leaf
(5 in Fig. 51).
4
R. RUTISHAUSER& al.:
Developmental morphology of Theligonum
5
Higher up the ( - ) leaf subtending the male flowers is lacking except for an
inconspicuous bump or appendage that may or may not be present in early
developmental stages (Fig. 8: arrow).
Monoeey, anthesis of male and female flowers, pollen strueture. Instead of
the bisexual flowers that are typical for most Rubiaceae there is a differentiation
into female and male flowers within each plant (monoecy) and even within each
node of the adult shoot zone. Female flowers arise in groups of (1-)2-4(-7) in the
axils of foliage leaves, and are already present in the axils of the seedling leaves.
Male flowers only occur higher up after the change to single leaf nodes (Figs. 1, 51;
LOISEAU 1969).
At anthesis the length of the female flower (measured from ovary base to
stigma) is 0.8-2 m m (Figs. 39, 40). The cylindrical stigma (with papillate cells)
protrudes beyond the corolla tube for a length of about 200-300 pm (Figs. 39-41).
As compared to the male flowers of the same node, development of the female
flowers often seems to follow that of the male flowers. Male flowers most often
arise in pairs, rarely in groups of three. They are extra-axillary and opposite to the
spirally arranged foliage leaves (Figs. 1, 8-10, 31, 51). Such a flower position
seems advantageous for wind pollination, and is combined with pendulous
stamens, elongate threadlike filaments, and powdery pollen. The length of male
flowers during anthesis is c. 3-5 mm. In this stage the corolla lobes are coiled
backwards (Figs. 30-31). We observed a high number of stomata in transversal
rows, and the process of coiling is probably related to changes in the water content
of the cells. The dorsifix anthers are elongate and dehisce by two longitudinal slits
(one per theca). Afterwards the empty anthers may or may not become helically
twisted during drying (Figs. 30-31).
In the material studied we only found 6- to 7-zonoporate pollen with a
reticulate exine provided with muri covered with numerous suprategillar elements
(Figs. 32-33). (3-)4-8 equatorial apertures (pori) per pollen were described in
Theligonum spp. by BALICKA-IWANOWSKA(1897), ULBRICH (1934), PRAGLOWSKI
(1973), NowIcv~ & SKVA~A (1979), and ROBB~CHT (1988).
Figs. 1-5. Theligonum cynocrambe. - Fig. 1. Lateral view of an adult erect shoot, showing
the stalked foliage leaves VI-XI with spiral phyllotaxis along elongated axis (IX*, with
blade removed). More distal leaves crowded in terminal rosette. The leaf bases with lateral
stipules. The male flowers (~X, ~XI) opposite the leaves X-XI are in anthesis (with glossy
coiled corolla lobes). - Fig. 2. Top view of the terminal rosette of another shoot after
having switched from decussate (II-II1/III-III') to spiral phyllotaxis (IV-VII). The foliage
leaves are numbered according to their ontogenetical order. The spiral phyllotaxis shows
divergence angles of c. 100°. - Fig. 3. Cotyledonary node of seedling, with basal portions
of the two cotyledons (C*, removed) and two membranous stipules (S) in intercotyledonary
position. Note the colleter(s) in the axils of the cotyledons. - Fig. 4. Terminal bud of
seedling axis, with third pair of foliage leaves (III/III*, one blade removed). Note the two
interpetiolar stipules (SIII) that are folded along the median plane covering the terminal
bud. - Fig. 5. Top view of young vegetative shoot, with decussate arrangement of leaves.
Note the unequal size of leaf pair L3/L3 t. The interpetiolar stipules ($2) of the next
younger node are exceeding the size of the leaf primordia L2/LT. S 1 are stipules of the
youngest node (leaf primordia hidden). - Bars: Figs. 1-2, 5 mm; Figs. 3-4, 1 mm; Fig. 5,
100 ~tm
6
R. RL~ISHAUSER& al.:
Figs. 6-11. 77~eligonumcynocrambe. Adult shoot tips, after switch to 1/4 spiral
phyllotaxis. - Figs. 6-8. Three views of adult shoot apex, ontogenetical helix in counterclockwise direction. Youngest node next to shoot apical meristem (A) with girdling
primordium (t) not clearly differentiated into leaf bulge and associated stiputar primordia.
31, initial male flower belonging to node 1. Next older node with leaf primordium (L2),
associated unequal stipules: Sa2 (anodic stipule) larger than Sc2 (cathodic stipule). From
the next older leaf (L3) both stipules removed ($3"). ~a2/3c2, male flower primordia of
Developmental morphology of Theligonum
7
Development and position of male flowers. Male flowers occupy the site of
the suppressed ( - ) leaves. In early developmental stages we occasionally detected
a rudiment of the subtending ( - ) leaf (Fig. 8: arrow). There are mostly two (rarely
three) male flowers of slightly unequal size and shape per node. The cathodic
flower primordium (e.g., ~c4 in Fig. 9) is favored whereas the anodic flower
primordium (e.g., $a4) is slightly retarded in development and anthesis (BALIC~IWANOWSKA1897). However, the cathodic flower orten ends up as being the smaller
flower of the pair, showing fewer stamens than the anodic one (Figs. 26, 27).
Moreover, as compared to the anodic flower (laterally flattened and with two
corolla lobes) the cathodic one is normally less flattened and quite orten provided
with three corolla lobes instead of two (Figs. 17, 18). Rudimentary scales associated with the male flower groups are occasionally present (Figs. 8, 17; EICHLER
1878, ULBRICH 1934). Thus, it is possible to interpret the developmental sequence
of two (or rarely three) male flowers per site as ä highly reduced cyme, with nearly
or completely lacking prophylls, analogous to the female flower groups (see
below).
Perianth development in male flowers. Male flowers are initiated as
hemispherical bumps (Figs. 8, 10). Then they may produce a circular rim (Figs.
12-14), or they become flattened with two (or three) perianth primordia arising on
the periphery (Figs. 15, 16). In dimerous flowers the perianth arises in the form of
two tat primordia (one adaxial and one abaxial). In trimerous flowers there arise
three tat primordia (one abaxial and two adaxial). They tend to grow at unequal
rates. There is always one perianth primordium facing the abaxial side (Figs. 17,
18). The adaxial lobe is usually larger and may enclose more stamens in a row than
the abaxial lobe (Figs. 23, 24). Before anthesis a basal tube is produced by
intercalary growth below the perianth lobes (Figs. 28, 30, 31). The two (or three)
perianth lobes show valvate aestivation before anthesis (Figs. 28, 29). When the
flowers open, the lobes are reflexed, exposing the long filaments and anthers (Figs.
30, 31).
Meristic variation and stamen initiation in male flowers. Unlike most
members of the Rubiaceae, Theligonum cynocrambe shows a considerable meristic
variation, especially with respect to the male flowers. Such a situation may be
called "leakiness" of the Rubiaceae-"Bauplan" (as proposed by V. ALBERT,pers.
node 2 (a = anodic flower, c = cathodic one); c~c3, primordium of cathodic male flower of
node 3. Black arrow in Fig. 8 points to primordial bump that may be interpreted as
rudimentary leaf subtending the male flowers. - Figs. %10. Two views of another shoot
apex, with clockwise helix. Shoot apical meristem (A) with initial stage of new appendage
node (not labeled). Second appendage node with leaf primordium (L2), two stipules ($2),
two male ttower primordia (~2) opposite to the leaf. Leaf (L3) and male flower pair
(~a3,~c3) opposite each other. Stipules of older nodes 3-4 removed, d~a4,~c4, anodic and
cathodic male flowers of fourth node with unequal size. - Fig. 11. Transverse section of the
shoot apex at the switch from decussate to spiral phyllotaxis with leaf pair (L3/L3~).
Ontogenetical helix of younger leaves in counter-clockwise direction: L2 with anodic (Sa2)
stipule broader than cathodic (Sc2) one. L1, insertion area of even younger leaf. da2,d'c2,
anodic and cathodic male flowers opposite to L2. - Bars: Figs. 6-8, 100 gm; Figs. 9-10,
200 gin; Fig. 11,300 ~tm
8
R. RUTISHAUSER& al.:
Figs. 12-19. Theligonumcynocrambe. Early development of male flowers. - Fig. 12.
Early stage of perianth formation of cathodic flower. Note depression surrounded by a
continuous rim. - Fig. 13. Anodic flower just after perianth initiation. Arrows point to two
altemipetalous androecial primordia. - Fig. 14. Young flower with girdling perianth, and an
elliptical rim of four (?) androecial primordia surrounding a central depression. - Fig. 15.
Young cathodic flower with two corolla lobes and an elliptical androecial rim surrounding a
central depression. Stamen primordia on rim not yet observable. - Fig. 16. Young flower
with three androecial primordia parallel to the two corolla lobes. - Fig. 17. Two flowers
with their perianth. Cathodic flower (above) trimerous and slightly preceding anodic
Developmental morphology of Theligonum
9
comm.). In the material studied the statuen number varies from two to six in
smaller flowers (Figs. 22, 25, 27) to up to 11-19 in larger flowers (Figs. 24, 26). In
male flowers there is normally no rudiment of the styles and the inferior ovary.
Occasionally male flowers show a nearly globular base at anthesis that may be
interpreted as remnant of the inferior ovary (Fig. 30). Cross-sections through such
swollen floral bases do not add more information to corroborate the hypothesis on
the rudimentary inferior ovary in male flowers (A. IGERSUEIM,unpubl.).
Stamen initiation patterns are quite variable. Depending on the number of
perianth lobes (two or three) of the male flowers, stamen initiation starts with the
formation of two or three alternipetalous bumps (arrows in Fig. 13, also Figs. 16,
18). When these primordia become directly stamens, then there are only two or
three stamens per flower. In other floral primordia with two perianth lobes,
however, the androecium emerges as an elliptical rim (common girdling
primordium) with a central depression (Figs. 14, 15). Then, this rim is nearly
simultaneously divided up into five to eleven or even more stamen primordia. Often
one stamen ends a row in alternipetalous position (Figs. 23, 24). The development
of the median stamens (in front of the corolla lobes) is normally not accelerated as
compared to the lateral ones (Figs. 16, 19). In older flowers with a higher stamen
number, the middle stamens of a row may become displaced to the center of the
flower or more externally (Figs. 24, 26). Not obvious in our material is the fascicle
(cluster) formation among the stamens. Only rarely two filaments were fused at
their base (Fig. 27: arrow). It was not possible for us to see fascicles of mainly two,
four, or six stamens as described by BALICKA-IWANOWSKA(1897), SCrr~IDER (1914)
and WtJYD~~ICH (1971: 370). Moreover, male flower primordia do not show bulgeshaped epipetalous common primordia prior to stamen initiation. Such common
primordia (two or three according to the tepal number) were described and
illustrated by BAIaC~-IWANOWS~A(1897: figs. 6, 7) and SCHNEIDER(1914: fig. 9).
CARtmL'S (1873) observations tend to be more correct, as he described the initiation
of two outer alternipetalous primordia, followed by the epipetalous stamens in two
rows. However, we often observed a continuous rim, i.e., a common girdling
primordium around a central depression, though the extremities at the perianth
interstices may not always be clearly developed (Figs. 14, 15, 19, 23). Additional
material needs to be studied in order to estimate the whole range of statuen
initiation pattems in Theligonum!
Development and position of female flowers. In the material studied there
are (1-)2-3(-5) female flowers per leaf axil. The set of female flowers of a leaf axil
is called "female unit" in the present paper. According to BALICKA-IWANOWSKA
(1897) and Wtrm~~~ici-I (1971) there are normally three flowers (fruits) per female
unit, occasionally even up to five flowers (fruits) on vigorous shoots. Each female
unit is best interpreted as a cymose inflorescence, because there is a clear
dimerous flower (below). Arrow points to scales that may belong to the rudimentary leaf
supporting the male flowers. - Fig. 18. Younger flower pair. Again cathodic flower (above)
trimerous and anodic flower dimerous (below). - Fig. 19. Young anodic flower with
androecial primordia differentiating on the rim (the two perianth lobes removed). - Bars:
Figs. 12-16, 19, 30 gm; Figs. 17, 18, 100 gm
10
R. RUTISHAUSER& al.:
Figs. 20-27. Theligonumcynocrambe. Further development of male flowers. - Figs. 20,
21. Two views of anodic flower after inception of eight stamen primordia. - Fig. 22. Two
flowers after removal of the abaxial perianth lobe. The cathodic flower (on the right) with
five young stamens whereas the anodic flower with at least six stamens. - Fig. 23. Apical
view of flower with nine stamen primordia along two rows inside the two perianth lobes
(removed). The adaxial lobe (on the left) is curved and encloses more stamens tharl the
abaxial lobe. - Fig. 24. Slightly older flower bud with 12 stamen primordia, including a
central stamen that may be displaced by crowding. Note one stamen at both ends. - Fig. 25.
Developmental morphology of Theligonum
11
Figs. 28-33. Theligonum cynocrambe. Male flowers prior and at anthesis, pollen structure.
- Fig. 28. Lateral view of nearly mature flower bud. Note the valvate aestivation of the
perianth lobes fringed with unicellular hairs. Perianth tube still very short. - Fig. 29.
Longisection through anodic flower bud at a developmental stage similar to Fig. 28. Note
the central depression and the slight adnation of the stamens to the perianth base. - Fig. 30.
Flower during anthesis, with anthers already dehisced and the corolla lobes coiled
backwards. Note the globular floral base that might be a rudimentary inferior ovary. - Fig.
31. Two flowers at anthesis, seen from adaxial side, with less prominent floral bases. Both
flowers with two coiled corolla lobes. Note the helical twisting of the dehisced anthers. Fig. 32. Hexazonoporate pollen, equatorial view. - Fig. 33. Close-up of pollen, with porate
aperture, reticulate exine and warts. - Bars: Figs. 28, 29, 300 btm; Figs. 30-31, 1 mm; Fig.
32, 5 btm; Fig. 33, 2 btm
Older flower bud with six stamens along one row. - Fig. 26. Anodic flower, one tepal
removed, 11 stamens observable. - Fig. 27. Cathodic flower (sister flower of anodic flower
shown in Fig. 26), perianth partially removed. The six stamens much further developed
than those of sister flower. Two filaments are fused at base (arrow). - Bars: Figs. 20, 21, 23,
24, 50 gm; Figs. 22, 25, 100 gm; Figs. 26, 27, 300 gm
12
R. RUTISHAUSER& al.:
Figs. 34-38. Theligonum cynocrambe. Early development of female flowers. - Fig. 34.
Early development of a female unit in leaf axil, seen from the side of the subtending leaf
(L*, removed). First forrned flower (~ 1) of female unit (cyme) surrounded by two prophylls
(I/It), one stipule (SI*, removed) on the abaxial side, and another stipule (SI) on the
adaxial side. - Fig. 35. Older female unit with central flower (~1, with initial perianth),
seen from the side of the subtending leaf (L*, rernoved). I/I r, two prophylls; SI, stipule
belonging to the prophyllar pair. ~2, position of next younger female flower (hidden). Note
upper male flower (~) belonging to another n o d e . - Fig. 36. Slightly older developmental
stage, central flower (~1) with perianth rim. Abbreviations as above. - Fig. 37. Abaxial
view of female unit. First formed flower (~1) with initial three-lobed corolla and initial
inferior ovary (already asymmetrically swollen). Younger lateral flower visible (~2). Note
interpetiolar adaxial stipule (SiI). Other abbreviations as above. - Fig. 38. Female flower
(~1) with displacement of the dimerous corolla to the adaxial side due to unequal growth of
the inferior ovary. L*, subtending leaf (removed); M, position of mother shoot axis. - B ars:
Figs. 34-36, 50 gm; Fig. 37, 100 lam; Fig. 38, 150 ~tm
Developmental morphology of Theligonum
13
Figs. 39-44. Theligonumcynocrambe. Female flowers at anthesis. -Fig. 39. Flower (~1)
at anthesis, with ovary (O), basilateral perianth (P) and long protmding stigma (G). ~2, hext
younger flower bud in axil of prophyll (I). M, sectioned axis of mother shoot. - Fig. 40.
Another flower at anthesis, with clearly bilobed perianth tube. Abbreviations as above. Fig. 41. Distal portion of trilobed perianth tube (one lobe hidden). Note papillae on stigma.
- Fig. 42. Lateral view of ovary at anthesis, with ovary wall partially removed in order to
see the solitary campylotropous ovule arising from a basal placental bulge (arrow) that later
on will form the septum. - Fig. 43. Transverse section through the flower base showing the
ovule (V) and septum (arrow) dividing the ovary into two loculi. - Fig. 44. Longisection
through young ovary with basal septum (arrow), one curved ovule (V) and elaiosome (E) at
the flower base. - Bars: Figs. 39-40, 200 gin; Figs. 41-43, 100 gin; Fig. 44, 300 gm
developmental difference between the first flower (~1 in Figs. 34-39) and the
successive ones (~2 in Figs. 37, 39). The terminal flower (~1) arises centrally
between the two prophylls, prior to the formation of an additional flower bud (~)2)
in the axil of one of the two prophylls (Figs. 34, 37). Very orten the smaller flowers
do not reach maturity. Each female unit starts with the formation of a transversal
pair of prophylls combined with one interpetiolar (= interfoliar) stipule on the
14
R. RUTISHAUSER8¢ al.:
Figs. 45-50. Theligonumcynocrambe. Development of fruit and embryo. - Fig. 45.
Longisection of very young fruit with curved ovule (V), basal septum (arrow), and region
with small embryo (*). Note the well-developed elaiosome (E), showing radially elongated
secretory cells. - Fig. 46. Longisection of young fruit showing still straight embryo
(arrow), surrounded by endosperm. - Figs. 47, 48. Slightly and strongly curved embryo,
with two cotyledons, of an immature and a mature fruit, respectively. - Fig. 49. Mature nutlike fruit, with ringlike elaiosome surrounding the insertion area of the globular one-seeded
fruit. - Fig. 50. Longitudinal section of the elaiosome region, showing the elongated
secretory cells. - Bars: Fig. 45, 1 mm; Figs. 46, 48, 300 ~tm; Fig. 47, 100 ~tm; Fig. 49, 500
Bin; Fig. 50, 200 ~tm
adaxial side and two free and often minute stipules on the abaxial side (Figs.
36-37).
The female flower starts its development with the formation of a hemispherical
primordium on which a ring primordium develops as the initial perianth tube (Figs.
34-36). No rudiments of a second (= calyx) perianth whorl are observable. Then
Developmental morphology of Theligonum
15
the inferior ovary becomes visible as a slightly asymmetrical inflated area by a
constriction below the initial corolla tube (Fig. 37). In later developmental stages
the corolla shows two or three lobes (Figs. 37, 38, 40). A single style pushes
through the perianth tube and grows into a functional stigma covered with short
papillae. The length of the style is variable (Figs. 39-41). Due to asymmetrical
ovary growth the perianth and style position shifts downwards on the adaxial ovary
side, leading to an almost gynobasic attachment of the style surrounded by the
tubular perianth (Figs. 39-40; BALICKA-IWANOWSKA1897: 364, fig. 8; Wt~,~DERHCH
1971: 368; CRONQUIST1981).
Developmental morphology of fruits and seeds. After anthesis the perianth
and style of female flowers are shed, leaving a scar which is rapidly hidden by the
inflation of the globular fruits. The nut-like fruits were often called drupaceous
although the fleshy mesocarp is very thin. There are a few (two or three)
parenchymatous layers and thick endocarp with brachysclereids (KAPIL & RAO
1966; and own observations, unpubl.).
There is only one basal and campylotropous ovule in the seemingly single
locule of Theligonum (Figs. 42, 45). Similar to other Rubiaceae the reduction of
the septum is accompanied by a stronger curvature of the single remaining ovule,
which becomes campylotropous. This was also observed by WUYDB~IeH (1971:
353): "Allem Anschein nach ist das Wachstum der Plazenta stark gehemmt, so dass
die Samenanlage früh kampylotrop wird." After anthesis and fertilization the ovule
becomes strongly curved leading to a seemingly globular seed with a basal incision
that is occupied by a basal septum of the ovary. This septum divides the lower half
of the ovary into two incomplete locules (see arrows in Figs. 42-45). Thus, the
Theligonum ovary is basically bilocular as typical for most Rubiaceae with only
one curved ovule that overtops and hides the basal septum.
During seed development the young embryo inside the curved ovule (mainly
endosperm) starts with a nearly straight form finally becoming horseshoe-like with
two cotyledons on one side and the radicular pole on the other side (Figs. 46-48).
Ripe nut-like fruits show a prominent brown elaiosome that arises as a ringlike
outgrowth from the insertion area of the inferior ovary after anthesis (E in Figs.
44-45). The elaiosome may be evenly ringlike or slightly lobed (Fig. 49). It
consists of radially elongated cells that are rich of mucilage and oll serving as food
for ants (Fig. 50; SEP,NANI~ZR1906, ULBRICH1934).
Discussion
Rubiaceous affinity/palynology
The rubiaceous affinity of Theligonum was overlooked until 1971 (W~DERLICH
1971; ROBBP,ECnT 1982, 1988, 1993) although the Russian botanist NE~q:KOV
already anticipated this view in 1939 (according to CROYQU~Sr 1981: 1001).
ROBB~¢HT (1993: 27) rightly refers to a "systematic camouflage". Based on
palynological data, PRAGLOWSKI(1973), and NowI¢I~ & SKVARLA(1979) again
questioned the inclusion of Theligonum into the Rubiaceae. According to them
Theligonum should be placed in the Caryophyllidae (see also KApm & MOHANARAO
16
R. RUTISHAUSER8¢ al.:
1966). Pollen of the 4-8-zonoporate type is not found in other Rubiaceae although
WtrND~~ICH (1971) and PPa~GLOWSI~(1973) described some palynological features
that are shared by Theligonum and some Rubiaceae, especially Anthospermeae
(also Spermacoceae, Rubieae): three-nuclear pollen, zonal arrangement of
apertures, size and type of pori, tenuinexinous (compare also with ROBBRECHW
1982). The exine surface of Theligonum is almost the same as in Paederia subg.
Lecontea (IGERSHErM 1991). A table given by WtrNDE~~CH (1971) summarizes a
number of similarities between Theligonum and other Rubiaceae.
TheIigonum is either included in the Rubiaceae, subfam. Rubioideae, tribe
Theligoneae (WtrNDZ~ICH 1971; PUFF 1982, 1986; ROBB~CHT 1988, 1993; THORNE
1992) or placed in a small satellite family Theligonaceae in the Gentianales
(MABRY& al. 1975, CRONQUIST1981, DAHLGREN1989, THEISZN& BAR~rmOWT1994).
There are several morphological, anatomical and embryological arguments in favor
of the Rubiaceae as next relatives of Theligonum (WtrNOERI~rCI-I 1971): e.g.,
colleters, raphids, interpetiolar (interfoliar) stipules in the basal decussate region.
In addition there is phytochemical, ultrastructural and molecular evidence
supporting a rubiaceous affinity of Theligonum, excluding it from the subclasses
Caryophyllidae and Rosidae (especially from Haloragaceae) (KOOIMAN 1971,
MABRY& al. 1975, B~IvmR & al. 1995, NATALI& al. 1995, B~MER 1996, MANEN&
NATALI 1996).
According to Wt:NI~E~I¢H (1971) and Pt~F (1982, 1986) the rubiaceous tribes
Anthospermeae and Paederieae may be regarded as hext related to Theligonum (=
tribe Theligoneae, ROBB~¢HT 1988, 1993). These three tribes may have 'common
roots' (Ptr~ 1982, 1986: 519). Theligonum plants produce the foetid odour
characteristic of many Anthospermeae and Paederieae, and the compounds
asperuloside and galiumglucoside are also present (KOOIMAN1971, PUFF 1982). The
geographical distribution of Theligonum overlaps with that of several genera of
Paederieae: Canary Islands, the Mediterranean area and east to Japan (ULBRICH
1934, PUFF 1982). Chloroplast DNA analysis data seem to support Paederieae such
as Putoria besides Rubieae and Didymeae as close relatives of Theligonum (MANZN
& al. 1994, and pers.comm.; NATALI& al. 1995, 1996; MANEN & NATALI 1996).
B~MER & al. (1995) and B~MER (1996) also place Theligonum closer to the
Rubieae and Paederieae than to the Anthospermeae. However, PUFF (1986, and
pers. comm.) points to the strong similarity between Theligonum and the windpollinated Anthospermeae.
Features of Theligonum that are also found in other Rubiaceae
Anisophylly and 1/4 spiral phyllotaxis. The spiral phyllotaxis of Theligonum is
traditionally explained by extreme anisophylly of a decussate system as typical for
most Rubiaceae, with the (+) leaves of the basically decussate pattern arranged
along a helix whereas all ( - ) leaves are suppressed (I~IS¢H 1856; SCHNEIDER1914;
ROBB~CWr 1988, 1993). Anisophylly, i.e. the unequal development of the two
leaves of an opposite pair, is clearly visible on the lateral branches of Theligonum
and is very common in Rubiaceae, including Anthospermeae, as summarized by
PUFF (1986: 519), and ROBBRZCHT(1988: 48). The second ( - ) leaf of a pair may be
Developmental morphology of Theligonum
17
totally suppressed in other Rubiaceae such as Pseudosabicea sthenula (ROBBm~CHT
1988: fig. 11 C), Argostemma humilis (ScmNANN 1891: 22, fig. 8V). Because of
the suppression of the ( - ) leaf in Theligonum the male flower pairs (rarely triplets)
regularly arise without a subtending leaf, i.e. in an extra-axillary position. In
Theligonum cynocrambe SCHNEIDER (1914: fig. 8) observed a shoot where two
nodes again were provided with leaf pairs although the more proximal nodes
showed 1/4 spiral phyllotaxis with one leaf per node. Anisophylly and anisoclady
are spiral in many Rubiaceae (e.g., Plocama pendula of the tribe Paederieae,
RUTISHAUSER1981: 68--69, fig. 14a-g; for other examples see Sc~IotrrE 1938).
The spital phyllotaxis with a divergence of 90-100 ° is consistent with the
suppression hypothesis of one leaf per pair. There is, however, another possibility
to interpret the 1/4 spiral phyllotaxis in Theligonum. It might be interpreted as a
Lucas system (with divergence d approximating 99.5°): Figs. 2, 52, 53 and show
the mean divergence closer to 99 ° than to 90°! Also LOlSEAU(1969) mentioned in
Theligonum divergence angles d > 90 °. The cross-sections of Theligonum shoot
apices (Figs. 52, 53) reveal divergence angles around 100 °. Both Lucas systems
(d=99.5 °) and Fibonacci systems (d=137.5 °) are spiral phyllotactic patterns related
to the Golden angle (RuTISHAUSER1981, 1982, 1997): In contrast to the widespread
Fibonacci systems typical Lucas systems are restricted to plant taxa with narrow
insertion angles (i) of the leaves (i _< 70°): certain conifers, Crassulaceae (Sedum
spp.), Euphorbiaceae (e.g., Euphorbia myrsinites). Theligonum, therefore, would
be an exceptional Lucas system because of leaf insertion angles up to 300 ° when
the leaf and the two associated stipules are taken as one developmental unit (Figs.
6, 11, 52).
Complete reduction of the calyx. As already explained in the introduction,
the simple perianth of Theligonum is best homologized with the corolla of other
Rubiaceae (e.g., tribes Anthospermeae, Paederieae, Rubieae, Spermacoceae), also
having valvate aestivation (WUNDERLICH1971; ROBBRECax 1988: 82). The corolla
development of Theligonum corresponds to the early sympetaly sensu E~AR
(1991) observed in some other Rubiaceae (ERBAR& LEINS 1996). There is a similar
depression surrounded by a low girdle. Early floral ontogeny of Rubiaceae without
calyx (e.g., Galium, Cruciata) resembles Theligonum to a great extent (PöTXER &
KLOP~R 1987, ERBAR1991, ERBAR& LEINS 1996). This coincides with the tendency
of calyx reduction in other Rubiaceae: Coffea with only a short calyx rim,
Spermacoce spp. with minute lobes, Phyllis nobla (tribe Anthospermeae) with a
strongly reduced calyx (ME~OZA-HEUER 1977), Neogaillonia (tribe Paederieae;
ROBB~CHT 1988: 74) and Galium (PöTTER& KLOPFeR1987) with calyx totally absent.
Dimerous to trimerous flowers. Flowers in Rubiaceae are mosfly pentamerous. However, a trend to tetramerous flowers can be observed in almost every tribe
(ROBBRECHX 1988). Trimerous flowers are exceptional. Besides Theligonum
trimerous flowers are found in rubiaceous genera such as Alibertia, Asperula,
Corynanthe, Mitchella, Opercularia, Pouchetia (see ROBBRECHX1988: 73, ERBAR&
LEINS 1996: Figs. 6-7). Dimerous flowers in Rubiaceae seem to be restricted to
Theligonum. A simple explanation for the derivation of dimery is by the lateral
fusion (interprimordial growth) of petals leading to a reduction of sectors in the
flower. Indeed, the adaxial petal in dimerous flowers is occasionally larger and
enclosing more stamens than the abaxial one (Figs. 23, 24).
18
R. RUTISHAUSER& al.:
5
c
Figs. 51-53. Theligonumcynocrambe. Branching pattern, position of the mate and female
flowers, 1/4 spiral phyllotaxis. Note that the leaves are labeled with Arabic numerals
according to their age from shoot tip to base, with youngest leaf numbered 1. - Fig. 51.
Diagrammatic scheme of young plant (similar to Fig. 2) showing switch from uppermost
leaf pair (6/6~) to spirally arranged leaves (5, 4, 3, 2, 1). Ontogenetical helix drawn in
clockwise direction. Uppermost leaf pair with interpetiolar stipules (Si6). Each of the
Developmental morphology of
Theligonum
19
Dimorphic flowers with lack of the opposite sex (or nearly so). Dimorphic
flowers occur in various Rubiaceae (WUNDERLICH 1971: 368). Monoecy or even
dioecy can be found abundantly in this family. Sexual flower morphs of unequal
size (male flowers with larger corolla than the female ones) are relatively frequent
in the tribe Anthospermeae (WUNDERLIC~ 1971: fig. 6, MENDOZA-HEUER 1977,
FLORENCE 1986, PUFF 1986): e.g., Anthospermum, Coprosma, Nertera, Phyllis. In
some genera of Anthospermeae (Anthospermum, Carpacoce, Galopina, Nenax,
Phyllis) the corolla lobes are curved backwards as is typical for the male flowers of
Theligonum (WUNDERLICH 1971, MENDOZA-HEVER 1977, PUFF 1986: fig. 33 g).
Male and female flowers of Theligonum seem to lack any rudiment of the
opposite sex. We did not observe rudimentary stamens inside the corolla tube of
female Theligonum flowers. Occasionally the male flowers of Theligonum possess
a globular base (Fig. 30) that may be homologous to a rudimentary inferior ovary.
This globular base is similar in size and shape with the rudimentary ovary of male
flowers in Nenax spp. (PUFF 1982, 1986: fig. 33e-g). In Nenax and other
Anthospermeae with floral dimorphism the opposite sex may be observable just as
a rudiment during floral development. Only exceptionally (e.g., in Anthospermum)
male flowers lack any gynoecial rudiment (WUNDE~ICH 1971: 369; PUFF 1986).
Polyandry and basal fusion of filaments in male flowers. There are only two
rubiaceous genera (Theligonum, Coprosma) with an increased statuen number if
Dia[ypetalanthus is not regarded as a m e m b e r of the Rubiaceae (FLORENCE 1986,
PIESSCttAERT 1995). In Theligonum the statuen number may considerably exceed the
number of corolla lobes whereas Coprosma (especially C. nephelephila) shows a
slight increase of statuen number (5-12) in flowers with five or six corolla lobes
(FLORENCE 1986, ROBBRECm: 1993). In the Theligonum cynocrambe material
studied we did not observe male flowers with more than 19 stamens although up
to 30 stamens per flower are mentioned in the literature (ScI~YEIDER 1914,
WtJNDE~ICI~ 1971, CRONQUIST 1981, ROBBRECI-IT 1988). Additional developmental
studies are needed in order to find out if there are other rubiaceous genera (tribes
Anthospermeae, Paederieae) besides Coprosma having at least slightly more
stamens than corolla lobes. In the monotypic Canarian genus Plocama (tribe
Paederieae) the male flowers show five to seven stamens but this seems to be
always correlated with an identical number of five to seven corolla lobes
(MENDOZA-HEt;ER 1987; PUFF 1982: table 2, 1991).
spirally arranged leaves with two lateral stipules, the anodic stipules (Sa5,Sa4,.) slightly
more vigorous than the cathodic ortes (Sc5,Sc4,.). Female units (~) in axils of leaves (6, 5,
4,.), each unit cymose, consisting of c. 2-3 female flowers. Male units extraaxillary,
opposite the single leaves (5, 4,.), consisting of slightly unequal male flowers: anodic
flower ((~a) adjacent to anodic stipule of same node, and cathodic flower (c~c) adjacent to
cathodic stipule. - Figs. 52-53. Two cross-sections of an apical shoot bud. All symbols as
mentioned in Fig. 51. - Fig. 52. Level of the shoot apical meristem (black area). - Fig. 53.
Insertion level of leaf 5. All leaves (dotted areas) are arranged along a spiral with
divergence of c. 100 °. The stipules (white) of each leaf are unequal, with the anodic stipule
(Sa) slightly bigger than the cathodic one (Sc). Male flowers (~, hatched areas) in pairs,
without subtending leaf, opposite to the leaf. - Bars: Figs. 52, 53, 500 gm. - Fig. 51
redrawn from,EICHLER (1878), Figs. 52 and 53 redrawn from LOISEAU(1969)
20
R. RUTISHAUSER& al.:
The position of androecial primordia in flowers with few stamens of
Theligonum (two or three depending on the number of petals!) alternate with the
positions of the petals as usual for Rubiaceae and other Asteridae. Especially male
flowers with a dimerous corolla may show an elliptical rim (common girdling
primordium) in early development. This rim is then divided up into several stamen
primordia nearly simultaneously following the curvature of the petals. The loss of a
calyx in Theligonum (linked with variable floral symmetry) may have induced a
chaotic increase of the stamens (cf. ENDRESS 1994). There is mostly one stamen in
alternipetalous position. The observation of BALICKA-IWANOWSr~ (1897) and
SCHNEIDER(1914) who described epipetalous primordia is therefore only partially
true.
We only exceptionally found fascicle formation among the stamens of
Theligonum (groups of stamens with fused filament bases as partial monadelphy)
as hypothesized by WUNDERLICH(1971). However, we do not exclude an increased
ratio of partial monadelphy in other Theligonum cynocrambe populations because
the initial girdling primordium (Figs. 14-15) may give rise to an androecial tube or
stamen fascicles (partial monadelphy) quite easily. An androecial tube was found
in other Rubiaceae such as Exostema, Chiococca (Portlandia group, subfam.
Antirheoideae) as weil as Strumpfia by B~MZR & STRVWE(1992) and IGERSm~~
(1993, also pers. comm.). In these genera it is necessary to study early androecium
development in order to know if there is also an initial common girdling
primordium similar to that found in Theligonum.
Trend towards a unilocular ovary. Most authors, such as BALICKAIWANOWSKA (1897), WUNDERLICH (1971) and ROBBRECHT (1988: 90) described
Theligonum with an unilocular ovary that does not show any trace of the second
locule. In Rubiaceae with a normally bicarpellate ovary there are only very few
taxa with a total reduction of the second locule. In Otiophora and Calanda the
unilocular ovary still possesses a trace of the second carpel (ROBBRECHT1988: 90).
In the post-anthesis ovary of Theligonum cynocrambe the lower third is
provided with a septum that shows a delayed development as compared to the
single ovule afising from its center (Figs. 42-44). The attachment of the ovule is
situated at the base of the septal ridge. Thus, Theligonum has an ovary that is
bilocular in the lower region.
WUNDERLICH (1971: 353, fig. 3g-h) already saw this septum. She called it
placental tissue. Thus, as already BALICKA-IWANOWS~(1897), WUNDERLICH(1971)
concluded that Theligonum does not show any trace of the second carpel (see
ROBBRECHT1988:90 for a similar statement). WUNDERLICHinterpreted the septum as
a special formation of the basal placenta that may be derived from the transversal
zone ("Querzone") of the only carpel. We agree with WUNDERLICHonly to some
extent. In various Rubiaceae with a reduced ovule number the ovules arise from the
center of the upper rim of the incomplete septum (RoBBRECHT 1988). DE BLOCK
(1995) also described the reduction of one of the two ovules of Rutidea (Pavetteae)
and the filling-up of the whole cavity by the seed, which literally invades the sterile
locule. As in Theligonum the septum is incomplete, hut there is an apical residue of
the septum separate from the basal part. Thus, the only ovule of the Theligonum
ovary arises at the very same site except that this septum shows a somewhat
delayed development.
Developmental morphology of Theligonum
21
Curved (campylotropous) ovules with insertion along their concave side seem
to be present in various Rubiaceae (Figs. 4 5 - 4 6 , ROBB~CHr 1988, ROBB~CIar & al.
1991). Especially those Rubiaceae members with a reduced ovule number (or even
an uniovular ovary) often show seeds with coiled endosperm and horseshoe-like
embryo (A. IaERSnEN, pers. comm.). Some Rubiaceae, however, show a unilocular
ovary with a single anatropous ovule (including straight endosperm and embryo),
as mentioned by PUFF (1986: Carpacoce spp.) and ROBBe,ECHT (1988: Calanda,
Otiophora).
Anemophily. Most Rubiaceae are entomophilous (Wt~mERLICn 1971: 369).
However, in the tribes Anthospermeae and Paederieae there is a tendency towards
anemophily with pendulous stamens, elongated filaments, and versatile anthers
(e.g., in Anthospermeae: Nertera, Phyllis), as stated by MEYOOZA-HEVER (1972,
1977, 1987), P u R (1986: 519). Thus, the anemophily of Theligonum is not
exceptional in Rubiaceae (ROBBR~Cm: 1988).
Conclusions and outlook
This paper provides a better knowledge of the developmental morphology of
Theligonum (tribe Theligoneae) as compared to other Rubiaceae. Theligonum
seems less exceptional than thought until now. Some of its features are observable
as evolutionary trends already in other tribes of subfam. Rubioideae. For example,
6-7-zonoporate pollen grains also occur in some Borreria spp. (tribe Spermacoceae; P r ~ 1996). Male flowers of Theligonum occasionally are provided with
a base that may be interpreted as a rudimentary ovary. Female flowers show
a bilocular ovary with an incomplete septum that is overarched by the only ovule.
We agree with ROBBRECHT'S (1993) conclusion that "Theligonum is a very
advanced evolutionary line w i t h i n Rubiaceae". It is justified to speak of a
leakiness of the "Bauplan" in Rubiaceae especially when we focus on the
polyandry of male flowers in Theligonum with a developmental pattern not found
or very rare in other Asteridae. There are other features such as the elaiosome, the
twisting of dehisced stamens, papillate filaments, gynobasic style associated with
an inferior ovary that are not (yet) known from other Rubiaceae. Still needed is a
cladistic analysis including anatomical and morphological characters besides
molecular data in order to find the closest relatives of Theligonum within the
Rubiaceae (BI~MER & STRUWE 1992, MANEN & al. 1994, B~MER & al. 1995,
Br~MER 1996, NATALI & al. 1995, MANEN & NATALI 1996). This analysis is in
progress.
We thank the directors of the Botanical Gardens of Glasgow, Göttingen and Marburg,
as well as Mr M. SEINER(Basel) and his colleagues for providing seeds of Theligonum.
The Swiss contributors thank Mr U. JAUCHfor technical assistance with the scanning
electron microscopy at the Institute of Plant Biology (University of Zürich) and Dr A.
IHERSnEIM(Wien and Zürich) for valuable comments on the first draft of the manuscript.
The Belgian contributors thank the National Fund for Scientific Research (N.EW.O.;
projects N ° 2.OO38.91, SEM and N ° G.O143.95, General research project). L. R RONSE
DECRAENEis a postdoctoral researcher of the N.EW.O.
22
R. RUTISHAUSER& al.:
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Addresses of the authors: R. RUTISHAUSER (correspondence), ILSE MENDOZA-HEUER,
Institut für Systematische Botanik, Universität Zürich, Zollikerstrasse 107, CH-8008
Züfich, Switzefland. - Louis P. RONSE DECRAENE,ERIK SMETS, Plantkundig Instituut,
Katholieke Universiteit Leuven, Kardinal Mercier-Laan 92, B-3001 Heverlee, Belgium.
Accepted December 13, 1996 by E EH~~Om~ER