the floral development and floral anatomy of coris monspeliensis
TRANSCRIPT
The floral development and floral anatomy of Coris monspeliensis
L.P. Ronse Decraene, E.F. Smets, and D. Clinckemaillie
Abstract: The floral development of Coris was investigated to clarify its controversial relationship with either Primulaceae (Primulales) or Lythraceae (Myrtales). We demonstrate that Coris is strongly related to the Primulaceae but differs in a few important features, such as the presence of an epicalyx and partial zygomorphy. The saccate calyx and epicalyx with unilateral development encloses an actinomorphic flower. The stamen-petal tube has two sections that arise through three growth processes: a lower common part for stamens and petals and an upper section representing a fused corolla. The central ovule-bearing part of the ovary arises separated from the carpel wall. The formation of ridges with teethlike appendages between the ovules suggests a derivation of the free-central placentation from an axile arrangement. Several characters support the monotypic family Coridaceae near the Primulaceae.
Key words: Coridaceae, Primulaceae, Lythraceae, floral development, floral vasculature, epicalyx, free-central placentation, common primordium, zygomorphy.
RCsumC : Le developpement floral de Coris a BC CtudiC afin de clarifier ses affinitCs controversCes avec les PrimulacCes (Primulales) ou les LythracCes (Myrtales). L'Cvidence ontogCnique et anatomique dCmontre que Coris est Ctroitement lie aux PrimulacCes, mais diffkre par quelques caractkres importants, comme la presence d'un calicule et une zygomorphie partielle. Le calice avec calicule (dont le dCveloppement est unilateral) enveloppe une fleur rCgulikre. Le tube commun des Ctamines et pCtales comprend deux sections qui naissent par trois modes de croissance : une partie infkrieure commune aux Ctamines et pCtales et une partie superieure qui reprCsente une corolle gamopktale. La partie centrale de l'ovaire portant les ovules nait independamment de la paroi qui l'entoure. La formation de crCtes entre les ovules suggkre que la placentation centrale est dCrivCe d'une disposition axiale. L'existence des CoridacCes comme famille monotypique proche des Primulactes, est soutenue par plusieurs caractkres.
Mots cle's : CoridacCes, PrimulacCes, LythracCes, dtveloppement floral, vascularisation florale, calicule, placentation centrale, primordium commun, zygomorphie.
Introduction
Coris is a small Mediterranean genus with two described species, Coris monspeliensis L. and Coris hispanica Lange, differing mainly in flower colour and the number of spines on the calyx tube (Ferguson 1972). They probably represent two varieties of the same species (Chant 1978; Carrion et al. 1993; Mabberley 1987). The position of Coris in the Primulaceae has been acknowledged by most authors as a separate subfamily Corideae (Pax 1897; Chant 1978) or Coridoideae (Takhtajan 1980) but not unanimously so. Some authors (e.g., Sattler 1962; Willis 1966; Dahlgren 1989) accept a family Coridaceae near the Primulaceae or inter- mediate between the Primulaceae and the Lythraceae. Indeed, Coris differs in a number of conspicuous characters from the Primulaceae, such as the subshrubby habit, zygo- morphic flower, and toothed calyx tube. Sattler (1962) found sufficient differences in the floral development of Coris to support the acceptance of a family Coridaceae, which he
I related to the Lythraceae on a number of selected characters.
1 Received January 5, 1995.
I L.P. Ronse Decraene, E.F. Smets, and D. Clinckemaillie. Laboratory of Systematics, Botanical Institute, Katholieke Universiteit Leuven, Kardinaal Mercierlaan 92, B-3001 Heverlee, Belgium.
However, other characters tend to be highly similar to the Primulaceae (e.g., the obhaplostemony , common stamen - petal primordia, the small globose ovary with free-central placentation and filiform style) and do not seem to justify a separation of Coris from the Primulaceae. Therefore the position of Coris remains debatable and is clarified by a renewed ontogenetic investigation as well as a study of the floral anatomy.
Materials and methods
The first author had the opportunity to collect flower buds of C. monspeliensis, growing on sand dunes in Jerba (Tunisia). Material was fixed in 85 mL 70% ethanol, 10 mL acetic acid, and 5 mL 40% formaldehyde (FAA). The buds were trans- ferred to 70% ethanol and dissected under a Wild M3 dis- secting microscope. The material was washed repeatedly in 70% ethanol and dehydrated by putting the buds in a 1: 1 mix- ture ethanol -dimethoxymethan (DMM, or formaldehyde - dimethylacetal) for 5 min and for 20 min in pure DMM (cf. Erbar 1988; Erbar and Leins 1989). Buds were critical point dried using liquid C 0 2 in the CPD 030 (Balzers, Liechten- stein). The dried material was mounted on aluminium stubs using Leit-C (after Gocke) and coated with approximately 180 nm of gold (SCD 020, Balzers). SEM observations were partly carried out at Heidelberg, Meise, and Leuven.
Can. J . Bot. 73: 1687- 1698 (1995). Prlnted in Canada / Imprune au Canada
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
Can. J. Bot. Vol. 73, 1995
Figs. 1-5. Scanning electron micrographs of the floral development of Coris monspeliensis. Fig. 1 . Apical view of an inflorescence apex (*) with successive inception of floral primordia at different stages of development. C , common stamen-petal primordium; Eu, adaxial (upper) spine; F , floral primordium. Scale bar = 100 pm. Fig. 2. Another inflorescence primordium showing numerous floral buds and protecting spines. *, inflorescence apex; Eu, adaxial spine; Em, latero-adaxial (median) spine; F, young floral primordium; Su, adaxial sepal; Sm, latero-abaxial sepal; S1, abaxial sepal. Scale bar = 100 prn. Fig. 3. Detail of a young flower bud with sepal primordia initiated on a circular rim. *, inflorescence apex; S1, abaxial (lower) sepal primordium; Sm, latero-abaxial primordia; Su, adaxial (upper) sepal primordia. Scale bar = 10 pm. Fig. 4. Detail of two flowers at different stages of development, the right one with a later stage of sepal inception and the left one with common stamen-petal primordia (C). The arrow points to the initiation of the adaxial spine. Su, adaxial sepal; Sm, lateral (median) sepal; S1, abaxial sepal; *, inflorescence apex. Scale bar =
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
Ronse Decraene et al. 1689
100 pm. Fig. 5. Detail of two flowers at different stages, the right one showing a bud enclosed by sepals and spines, and the left one being an older stage with the inception of a gynoecial ring primordium (arrow). C, common stamen-petal primordium; SI, abaxial sepal; Sm, lateral sepal; Su, adaxial sepal; Em, lateral spine; Eu, adaxial spine. Scale bar = 100 pm.
For light microscopy only mature buds were analysed and customary methods of preparation were used. The material was run through an alcohol as well as an alcohol - tertiary butanol series and was next embedded in paraffin, using the histokinette 2000 (Reichert-Jung, Vienna, Austria) automatic tissue processor and the paraffin dispenser PAG 12 (Medite,
. . . Isernhagen, Germany). Serial sections, about 8 - 11 pm thick, .. . . . . were stained with safranin and fast green using the automatic
staining machine Varistain 24-3 (Shandon, Runcorn, England). Photographs were taken under a Leitz Dialux 20 equipped with a Wild MPS 45/51 photoautomat.
Reference material (preserved and herbarium specimens: Ronse Decraene 327 Lt and 1039) is kept at the Botanical Institute of Leuven (LV).
Observations
Floral ontogeny Coris is a small thymelike woody herb found in coastal sand dunes. Purplish pink flowers arise in closely packed terminal racemes. The lower mature flowers cover the apical part of the inflorescence by the presence of long spines or append- ages on top of the calyx tube that act as a protection for younger buds (Figs. 1, 2 , Eu).
Flower buds emerge successively on the compressed raceme (Figs. 1, 2). They arise as hemispherical bodies without evidence of bract or bracteole primordia (Figs. 1, 2, F). On each flower bud five calyx primordia develop in rapid succession and become continuous at once (Fig. 3). This results in a rim with a sinuous outline formed bv the five primordia. Two sepal primordia arise on the adaxial side (Su), simultaneously or slightly after an abaxial primordium (Sl; Figs. 3, 4); they are rapidly followed by two latero- abaxial primordia (Sm). Sepal lobes grow rapidly and become valvate in bud (Figs. 5 , 6 , 25).
The regular development of the calyx is soon interrupted by the successive inception of five appendages on the outer edge of the rim, immediately following the inception of the calyx lobes (Figs. 4-6). A first primordium is initiated between the two adaxial calyx lobes (Fig. 4 , arrow) and is followed by four other primordia in descending order. The irregular development of the appendages is underlined by their unequal growth. The upper appendage (Eu) grows into a flap that covers the inflorescence apex (Figs. 1, 2 , 5 , 6), protecting younger flower buds. The twd latero-adaxial appendages (Em) extend laterally but remain shorter, while the two latero-abaxial lobes remain much smaller (Fig. 6, arrows). These appendages grow into spines with an inflated base (Fig. 25); the upper (adaxial) appendage remains the largest (Eu), flanked by the two upper lateral spines (Em), with two smaller spines (El) on the lower side (Figs. 25, 26). The zygomorphic appearance of the flower is stressed by the orientation of the adaxial (upper) spines, which protect younger flowers positioned in a higher position. The lower spines play no role in the protection of the inflorescence (Fig. 25).
The sepals and spines become rapidly covered by trichomes
with a spherical head (Figs. 2, 6, 25, 26). Calyx lobes and spines are lifted by common basal growth and extend into a large tube enclosing the young flower (Figs. 25, 26). Calyx lobes remain on top and do not enlarge much while the spines become flattened and much inflated-at their base. ow ever, at maturity there is a difference in size between the calyx lobes, as the three abaxial lobes are larger than the two adax- ial, as if they compensate for the smaller size of the spines (Fig. 25). The three abaxial sepal lobes also bear a central protuberance (brown mark), similar to the one found on vegetative leaves (Figs. 25 (white arrow), 27). Closer inspection reveals the presence of a lentil-shaped hardened structure situated in the lacuna between the dorsal and ventral epidermis (Fig. 28). Willis (1966) described these structures as immersed glands. The calyx with spines surrounds the developing flower as a saccate harness. The inner surface of the calyx tube is smooth (Fig. 26) while 10 veins are clearly visible in fresh and preserved material: 5 connect the sepal midribs and 5 run to the spines. On the upper flowers of the inflorescence the abaxial spines are much more reduced, while the three adaxial remain erect. Smaller secondary spines may emerge laterally of the first-formed spines (Fig. 25, black arrows). This is also one of the diagnostic features separating C. monspeliensis from C. hispanic; (see Ferguson 1972).
The apex of the flower is globular at the time the calyx lobes emerge (Figs. 3, 4) but later takes a pentagonal shape, when the sepal lobes have completely covered the flower. Contrary to the calyx, the remaining flower does not show any sign of zygomorphy in its early development. Five broad common stamen - petal primordia (C) emerge on the periph- ery of the pentagonal apex simultaneously or in a rapid sequence as they may differ in size (Figs. 1, 4, 5). They become continuous by the growth of a peripheral ringlike zone (Fig. 7). At this time the central area becomes demar- cated as another pentagon (Figs. 5 , 7). Stamen -petal pri- mordia divide and a smaller petal primordium is detached as an outgrowth from the base of the larger stamen primordium (Figs. 7 (arrow), 8- 10). Petals appear thus as crescent- shaped lobes, which are continuous from an early stage onwards (Figs. 9-13). Petal growth is retarded compared with the stamens (Figs. 9- 12) and it is only after complete anther and filament differentiation that the petals cover the androecium and gynoecium. The petal primordia become con- tinuous between and above the stamen insertion (Figs. 11, 13, 19, arrows). The top of each petal becomes two-lobed to trifid (Fig. 19). Below the stamen insertion a common ring primordium gives rise to a tubular zone by intercalary growth (Fig. 23); stamens could thus be described as fused with the petals (epipetalous).
Stamen development is typical: four pollen sacs are pro- duced (Figs. 10, 11, 12, 19), with the outer turned slightly outwards and initially larger than the inner (Figs. 12, 19). There is little connective tissue. Filaments extend in size after the differentiation of the ovules (Fig. 23). Long trichomes are initiated in large numbers on the lower half of the filaments (Fig. 21); they consist of a multicellular stalk
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
1690 Can. J. Bot. Vol. 73, 1995
Figs. 6-14. Scanning electron micrographs of Coris monspeliensis. All scale bars = 100 pm. Fig. 6. Same detail as in Fig. 5 . Note the irregular size of the spines and valvate aestivation of the sepal lobes. Eu, adaxial spine; Em, latero-adaxial spine; SI, abaxial sepal. The position of the abaxial spines is shown by arrows; the left one was removed during preparation. Fig. 7. View of the floral primordium at the stage of tangential division of common stamen-petal primordia (arrow). Note the central pentagonal apex. Fig. 8. Tetramerous flower primordium showing the ring primordium connecting the petals and the gynoecial ring primordium. Fig. 9. Lateral view of a slightly older bud. Note the continuous petal primordia. A, stamen primordium; P, petal primordium; W, gynoecial wall. Fig. 10. Slightly older stage with the differentiation of anthers; the gynoecial ring grows as a tube around the central apex. Fig. 11. Lateral view of another tetramerous flower. Note the boat-shaped petals surrounding the stamens; the ring primordium grows above the stamen insertion (arrow). Fig. 12. Upper view showing the closure of the gynoecial tube. Fig. 13. Section through the gynoecial wall showing the central stalk (Ax) with developing ovules (0); corolla ring is shown by arrow. A, stamen cut through. Fig. 14. Detail of an older stage. Note the ovules arising on a common platform (B) around the central stalk (Ax) and separated from the gynoecial wall (W). St, style.
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
Ronse Decraene et al.
with a spherical head. It is not known whether they play a particular role in the ecology of the flower. Before anthesis, filaments are characteristically curved (Fig. 24).
After stamen-petal initiation the remaining apex is pen- tagonal' at first (Fig. 7). Very rapidly an equal peripheral rim is initiated (Fig. 5, arrow). This circular primordium extends in size and grows as a saccate structure over the floral apex (Figs. 8-12, W). It takes the shape of a small bottle with the neck extending in a tubular style (Figs. 12- 14, St). The lower part develops as the ovary wall and becomes covered by a large number of stalked trichomes similar to those on the filaments (Figs. 17, 19, 20, 24). The style rapidly extends in size and is curved in the young bud (Figs. 17, 24); the upper part develops as a small flattened stigmatic area densely covered with papillae (Fig. 22).
The central basal area (B), which might be completely separated from the surrounding gynoecial tissue, develops as the placenta (Fig. 13). Placentation could be described as freeIcentra1, andearly stages of ovule development are par- ticularly illustrative. The central part of the gynoecium (which is undoubtedly an extension of the floral apex) develops a short pointed stalk (Ax), ending where the style begins (Figs. 13 - 16, 18). Later it resembles an arrowhead (Figs. 18,44). Five ovules (or most often six in our material) are initiated as globular primordia on the upper part of a broadened gynoecial base or basal platform (Figs. 13, 14, B). Ovules are rapidly separated by protuberances arising through the enlargement of the platform (Figs. 15 (arrow), 16); these extend into prominent basal ridges (Fig. 17, arrow) running between the ovules to the base of the central stalk. At the same time, the ridges extend in height as teeth (T). While the ovules grow outwards, they progressively fill the locular cavity between the teeth (Figs. 14- 16). Ovules are anatropous with two integuments and the micropyle directed towards the periphery (Figs. 14 - 17). The triangu- lar protuberances grow between the micropylar area and enclose the ovules tightly (Fig. 18). At this time the dissected gynoecium resembles a young closed flower bud, while the teeth could be taken for calyx lobes and ovules for petals (Fig. 18).
Prior to anthesis a nectary arises at the base of the gynoecium on the naked area just below the mass of tri- chomes (Fig. 20). It possesses nectarostomata with an open aperture. Pollen grains are tricolporate with a large margo. More details about pollen are given by Carrion et al. (1993).
Floral anatomy The pedicel of young flowers has a central pith surrounded by xylem and a broad band of collenchymatous cells (Fig. 29). The cortex consists of large parenchymatous cells (P) with- out lignification. The epidermis (E) bears multicellular tri- chomes (t) with spherical heads.
At the base o f the flower the central vascular tissue is disrupted by the simultaneous departure of 10 traces (not illustrated), which rapidly form a peripheral ring as the calyx tube becomes detached from the central tissue (Fig. 30, ct). The traces form the sepal median traces that alternate with traces running to the five spines.
' Flowers may occasionally be tetramerous (Figs. 8, 1 I ) , in which case the outline of the gynoecium is tetragonal.
The remaining vascular tissue is reorganized as a hollow star with five arms (Fig. 30). At a slightly higher level the five arms become detached and run to the periphery, leaving a few central bundles (Figs. 31, 32). They immediately trifurcate but not at the same level (Figs. 3 1, 32). As a result 15 traces are distributed in a ring, which is detached at a higher level (Figs. 33, 34). The five larger traces represent a common supply to the petal medians and the stamens, while the lateral arms develop as supportive tissue for the stamen- petal tube (Figs. 34-39).
Another set of traces departs from the central vascular tis- sue in an irregular pattern (Fig. 33). They are rearranged as another ring with five larger traces standing opposite the median petal traces and a few smaller traces in between (Fig. 34, arrows). At the level of detachment of the stamen- petal tube, the central area is demarcated by a gap as a small stalk with an inner ring of traces (Fig. 34). The ring of outer traces surrounding the gap is embedded in a broad band of small-sized parenchymatous cells (Figs. 34, 35). As the gap widens, another band of parenchymatous tissue develops around the central stalk, concomitantly with a decrease in size of the peripheral parenchymatous tissue (Figs. 36, 37, 44-46). In longitudinal section the ovary has a broad base on which the central stalk is fixed as a small stem (Figs. 44- 46). The outer band of parenchymatous tissue bears numer- ous trichomes externally and represents the ovary wall (W); the five larger traces represent the carpellary dorsals and the smaller traces carpellary laterals (Figs. 35 - 37).
The central stalk supports an extension, seen as two wings (B) in longitudinal section (Fig. 45). We described this as the basal platform, which consists of densely packed paren- chymatous cells filled with starch (Fig. 46) on which the ovules repose. In transverse section the central ring of vascu- lar tissue breaks up into a ring of small traces (V) surround- ing a few centrally placed bundles, which end at a higher level (Fig. 36). The basal platform is fragmented into trapezia (T) alternating with the stalks of the ovules (Figs. 36, 37). Ovules are supplied by the central vascular supply, which reaches its upper limit at this point, as the extension bears no vascular tissue (Figs. 37, 38, 44). At this level the lateral traces of the carpellary wall have also vanished, leaving only five dorsal traces (Figs. 37 (arrows), 38).
Ovules are pear-shaped, alternating with the extensions of parenchymatous tissue; they are detached ventrally from the central stalk, which is hexagonal at this level because of the pressure of the ovules (Fig. 38). The outer layer (outer integ- ument) of the ovules is tanniferous, and the inner integument consists of two layers of cells. At the top of the ovary, the gynoecial wall covers the locule, as the five dorsal traces bend towards the middle of the flower and end as five small traces running through the style (Figs. 39-42). The central stalk ends as a small point at the level of division of stamen traces and petal median traces (Fig. 39, arrow). Higher up the petal laterals also disappear as the stamen outline becomes visible on the inner side of the tube (Fig. 40). Five filaments, heavily covered with trichomes at their base, occupy the area between style and petal tube (Fig. 40); the vascular tissue breaks up into two traces but reunites at a higher level (Figs. 40-42, black arrows).
A higher section reveals the fragmentation of the calyx tube into sepal lobes alternating with V-shaped extensions of
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
1692 Can. J. Bot. Vol. 73, 1995
Figs. 15-25. Scanning electron micrographs of Coris monspeliensis. Fig. 15. Older stage showing the protruded growth of the stalk (Ax) and the curving of the ovules (0). Note the inception of alternating ovarian teeth (arrow). Scale bar = 100 pm. Fig. 16. Lateral view of the ovary showing C U N ~ ovules with fully developed integuments and triangular appendages in between. Ax, central stalk. Scale bar = 100 pm. Fig. 17. Partly opened ovary showing extensions (arrow) running from the triangular appendages (T) to the
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
Ronse Decraene et al. 1
stalk. 0 , ovule; W, gynoecial wall. Scale bar = 100 pm. Fig. 18. Lateral view of nearly mature ovary; gynoecial wall removed. Note the pointed stalk (Ax), tightly packed ovules (O), and triangular teeth (T). Scale bar = 100 pm. Fig. 19. Partly sectioned flower showing petals with bi(tri-)fid apex and curved style. Arrow points to the corolla ring. Scale bar = 1 mm. Fig. 20. Detail of the base of the ovary showing multicellular trichomes and nectarostomata (arrows). Scale bar = 100 pm. Fig. 21. Detail of the base of the filaments with numerous multicellular trichomes. Scale bar = 1 mm. Fig. 22. Stigmatic surface with papillae. Scale bar = 100 pm. Fig. 23. Half-sectioned flower bud. Note the short filaments and common zone for stamens and petals below filament insertion. Scale bar = 100 pm. Fig. 24. Section through a nearly mature bud. Note the curved stamens and style. Arrow points to the nectariferous area of Fig. 20. Scale bar = 100 pm. Fig. 25. Calyx tube with spines. Note three larger upper spines (Em, Eu) and two smaller in front (El); secondary spines are also visible (black arrows). The white arrow points to an impression formed by a cavity on each sepal lobe. Scale bar = 1 mm.
Figs. 26-28. Scanning electron micrographs of Coris monspeliensis. Fig. 26. Section through the calyx-epicalyx tube with adaxial upper (Eu) and median (Em) spines. Scale bar = 1 mm. Fig. 27. Detail of a protuberance on a sepal lobe, seen from the ventral side. Scale bar = 100 pm. Fig. 28. Lentil-shaped body within the lacuna of each sepal lobe. Scale bar = 100 pm.
the petals (Fig. 41). At this level the sepal median trace breaks into two traces and a central red-staining cavity appears, containing amorphous deposits of resinlike material (Figs. 42, 43). This area corresponds to the lentil-shaped body seen with the SEM (Fig. 28). In the mature flower the filaments and style are extended above the perianth and the unequal petal lobes are curved over the spines. Anatomical evidence of nectarial tissue (N) was seen at the thickened base of the ovary corresponding to the position of nectaro- stomata below the trichomes (Figs. 45, 46).
Discussion
Morphology Sattler (1962) also studied the floral ontogeny of Coris. Our results agree with his observations in several aspects, but some differences were also found. We agree with Sattler (1962) that the two first sepals arise adaxially, but his obser- vations differ from ours as-far as the sequence of sepal initia- tion is concerned: sepal inception is not running from the adaxial to the abaxial side of the flower, but an adaxial pair (Su) arises with a single abaxial sepal (Sl) before the two laterals (Sm) emerge (Figs. 3, 4). On the other hand, the spines arise from the adaxial to the abaxial side of the flower (Figs. 5, 6).
Coris conforms with other Primulaceae in several details of its floral development and anatomy. Stamens and petals arise from common stamen-petal primordia, which are char- acteristic for the Primulales (Figs. 4, 5, 7; e.g., Roth 1959; Sattler 1962; Sundberg 1982; Nishino 1983; Clinckemaillie 1991). Petals appear as dorsal outgrowths of a much larger stamen primordium (Figs. 7 - 1 l), as occurs in most other Primulaceae (Sattler 1962; Nishino 1983; Clinckemaillie 1991). A similar continuity between petal primordia is also reported for species of Primulaceae. Petal-tube growth and stamen-petal fusion are totally similar. However, one can- not speak of fusion in a strict sense, because it is common basal(interca1ary) growth that is responsible for the elevation of petals and stamens (see below). Early gynoecial develop- ment is also completely comparable to the Primulaceae in the formation of a circular rim enclosing the gynoecium as a sac- cate structure (Figs. 8- 12). The only difference, as observed
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
1694 Can. J. Bot. Vol. 73. 1995
Figs. 29-40. Transverse light microscopic sections of Coris monspeliensis at successive levels. See text for further explanations. ~ l l scale bars = 100 pm. Fig. 29. Section through the pedicel of the flower. E, epidermis; P, cortical parenchyma; t, trichome; V, vascular tissue. Fig. 30. Star-shaped inner vascular ring that remains after the separation of the calyx-epicalyx tube (ct). P, parenchyma; V, vascular tissue. Fig. 31. Departure of five traces, two of which form lateral branches. P, parenchyma; V, vascular tissue. Fig. 32. Irregular trifurcation of the five traces leaving a few central bundles. cr, calyx-epicalyx tube. Fig. 33. Section with five outer triplets of a median petal-stamen trace (Pm) and two lateral petal traces (PI). Fig. 34. Separation of
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
Ronse Decraene et al. 1695
stamen-petal tube and formation of a central gap surrounding a ring of traces. Arrows point to five dorsal traces. ct, calyx-epicalyx tube. Fig. 35. Separation of gynoecial wall with dorsal (d) and lateral traces and extension of the basal platform for the ovules. Fig. 36. Separation of the supply for the ovules from the central vascular trunk. d , dorsal trace; P1, lateral petal trace; Pm, common median petal-stamen trace; v, ventral trace. Fig. 37. Section at the level of ovule insertion. Note three of the six alternating trapezia or teeth (T); all central vascular tissue is used up. The arrows point to the five dorsal traces lying in the gynoecial wall (W). Fig. 38. Separation of the six ovules from the central stalk (Ax). T, triangular appendage; W , gynoecial wall. Fig. 39. Section at the base of the style. Note the extremity of the central stalk (white arrow) surrounded by the five dorsal traces. Division of the common supply for petals and stamens (black arrows). Fig. 40. Separation of the filaments (A) from the common petal-stamen tube. The arrows point to the splitting of the stamen trace. St, style; Pm, petal median trace.
Figs. 41-46. Transverse and longitudinal light microscopic sections of Coris rnonspeliensis at successive levels. See text for further explanations. All scale bars = 100 pm. Fig. 41. Section at the level of separation of the calyx lobes. Note the bifurcation of the sepal median trace (arrows). A, filament; S, sepal lobe. Fig. 42. Higher level with separated sepal traces (white arrows) and central lacuna; the black arrows point to divided stamen traces. Note the regular arrangement of the flower. Fig. 43. Detail of a lacuna with central resinous body within a sepal lobe (S). A, filament; P, petal lobe. Fig. 44. Longitudinal section of the gynoecium. Note the arrowlike central stalk (Ax) with ovules(o) and basal platform (B). AP, stamen-petal tube. Fig. 45. Longitudinal section of the gynoecium. Note the treelike basal platform (B) and thickened nectariferous base of the gynoecium (N). Fig. 46. Detail of the base of the gynoecium showing histology of the nectary (N) and basal platform (B). W , gynoecial wall; AP, stamen-petal tube.
by Sattler (1962), lies in the fact that the first stage of gynoe- cia1 initiation of Primulaceae is the formation of a depression due to peripheral growth, while the gynoecial rim of Coris emerges on a convex apex (compare with illustrations in Sundberg 1982; Clinckemaillie 1991). The free-central placentation arises in a similar way, but the number of ovules in Coris is much lower and they are separated by prominent ridges (Figs. 13-18). Similar trichomes are common in
Primulaceae (Figs. 17, 21). The nectaries (with nectaro- stomata) are gynobasal (Figs. 20,46), as may be found in the Primulaceae (Smets 1988; Clinckemaillie and Smets 1992). The outline of the ovary (with slender style and flattened papillate stigma (Figs. 22, 24) is wholly consistent with the common structure in Primulaceae (Clinckemaillie 1991). Pollen grains of Coris conform completely to the general pat- terns of the Primulaceae (Carrion et al. 1993).
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
Can. J. Bot. Vol. 73, 1995
Floral anatomy also reveals striking similarities. Stamens and petals are usually supplied by common traces (Figs. 32 - 40; see Douglas 1936; Clinckemaillie 1991); the ventral vas- cular supply ends with the ovules (Fig. 36), and five dorsal traces are commonly formed (Figs. 35 - 38).
Coris differs from the Primulaceae essentially by the development of its calyx with appendages. Referring to Coris as having zygomorphic (monosymmetric) flowers is not fully correct, as only the calyx with its appendages is zygomorphic and is initiated as such. Sepal inception of the Primulaceae is more regular (Clinckemaillie 1991) and flowers are never zygomorphic. However, other Primulaceae also have a sac- cate calyx enclosing the tubular corolla in a loose manner. The zygomorphy of Coris is rather unusual as it is only weakly expressed and is introduced late in organogenesis in the rest of the flower; only the calyx and appendages arise unidirectionally. On the other hand, most zygomorphic flowers of largely monosymmetric groups have all floral organs arising unidirectionally (see Tucker 1984; Endress 1994).
Sattler (1962) described the spines of Coris as an epi- calyx. Indeed, as in some other taxa with an epicalyx (e.g., Rosaceae, Neuradaceae, Lythraceae), the spines arise after or before sepal inception and alternate with the calyx lobes. The origin of the epicalyx remains obscure, since one refers to bracts, fused stipules, or emergences (Weberling 1989). In Coris, the presence of regular bundles alternating with those for the calyx tends to exclude the possibility of emergences. The absence of bracts in Coris, contrary to other ~ r i m u - laceae, may be related to the compact inflorescence or may indicate that the epicalyx is of bracteolar origin. However, as stipules are present on the vegetative parts, homology of the spines with fused stipules is not excluded. The other pos- sibility is that the spines represent both bracts and stipules. Their function is also different: in the Rosaceae and Neuradaceae the epicalyx enables fruits to be dispersed by encroachment, whereas in Cons its function is obviously protective. The formation of the calyx tube is also interest- ing; it arises by common basal growth lifting calyx members and epicalyx in a way similar to stamen-petal growth.
Stamen-petal growth and fusions remain controversial and have been analysed by several authors (e.g., Pfeffer 1872; Roth 1959; Sattler 1962; Nishino 1983). In Coris, three growth processes could be discerned in the association of petals and stamens. (i) Petal primordia appear dorsally on a larger stamen primordium (by the division of a common stamen-petal primordium) and are at once confluent by a ringlike structure. One could describe this lateral fusion as interprimordial growth, although meristem extension (sensu Sattler 1978) or a de novo formation of a common meristem are better terms. (ii) Vertical extension of this ringlike struc- ture lifts petal lobes and stamen primordia alike, the latter appearing as fused to a petal tube. However, it is clearly the growth of the basal rim that is responsible for the formation of the tube. (iii) The area above the stamen insertion devel- ops into a tubular corolla by intercalary growth beneath the corolla lobes.
Nishino (1983) described this development accurately for the Primulaceae but interpreted this in a puzzling way. He denied the upward elongation of the common base of petals and stamens and interpreted the lower portion of the tube as
androecial. In fact he saw the petals as clinging appendages on a rim with a fully androecial nature. This interpretation rejoins earlier ideas of the nature of petals as secondary dor- sal appendages (e.g., Roth 1959) or dorsally fused stipules (e.g., Pfeffer 1872; Mattfeld 1938). We observed that the petal and stamen primordia appear as common primordia, possibly as a result of a phylogenetic fusion (cf. Sattler 1978; Ronse Decraene et al. 1993); petals become continuous later- ally through the formation of a ring primordium. This ring extends upwards as a common tube for petals and stamens; only higher up at the level of stamen insertion a true petaline tube becomes apparent, resulting from the formation and growth of a basal intercalary meristem. It is not a coinci- dence that the lateral petal traces end where the stamens become detached from the tube (Figs. 39, 40). The tube has thus two sections: a lower common part for stamen and petal that lifts stamens and petals alike (by zonal growth "auf gemeinschaftlichem Piedestal emporgeschoben" (Pfeffer 1872, p. 202) or "a circular intercalary diffuse meristem" (Erbar 1991, p. 418) and an upper section that represents a fused corolla. This development is similar to other Sympeta- lae (see, e.g., Leins and Erbar 1987; Erbar 1991), although Coris differs by its obhaplostemony and common stamen- petal primordia. Erbar (1991) distinguished two growth forms of corolla development: early and late sympetaly. In early sympetalous taxa, a ring primordium is formed before or at the same time as the individual corolla lobes appear; in late sympetaly, initially free petal primordia fuse laterally through interprimordial connections at the back of the stamens. Coris (and the Primulaceae) tend to have an inter- mediate inception, as petal primordia arise before they become connected by a ringlike meristem.
Sattler (1978) avoided the difficulty of distinguishing different forms of fusions and nonfusions by the term con- tinuity. While avoiding the possibility of making incorrect assumptions, this concept does not help to distinguish between effective growth processes. In this context the renewed descriptive terminology of Ritterbusch (1991) is more useful: he described the whole corolla with fused androecium as a stapetum, made up of a stamen-petal tube (synstapetalum) and a petal tube (apostapetalum). Leins and Erbar (1987) and Erbar (1991) similarly use the terms stamen-corolla tube and corolla tube s.str. The apostapetalum consists of a petal tube (coenopetalous) and petal lobes (apopetalous). Although this terminology does not rely on ontogenetic evidence, it has its usefulness as it helps to describe different nonhomologous or partly homologous structures.
The gynoecium of Coris reveals several interesting facts. It is difficult to understand the number of carpels on a strictly ontogenetic basis. In fact, primulaceous flowers could even be approached as acarpellate (see Clinckemaillie and Smets 1992; Sattler 1974; Sattler and Lacroix 1988). In this case the carpel is seen as a gynoecial envelope that does not neces- sarily bear the ovules; the ovules are produced by the floral apex (Sattler 1974; Sattler and Lacroix 1988).
However, certain facts of the ontogeny of Coris tend to substantiate the view of a five-carpellate gynoecium. The pentagonal apex that arises before the formation of the gynoecial rim is a poor argument, but it becomes supported by the presence of five dorsal traces in the carpellary wall (Figs. 34 -38). Also the five ovules (often six) separated by
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
Ronse Decraene et al.
low ridges (running between the placentae) and external tri- angular teeth support the five-carpellate hypothesis. These ridges could well be interpreted as rudimentary septa, as argued by Sattler (1962) who also found it in several other Primulaceae. He derived the free-central placentation from an axial placentation by the reduction of the septa and consid- ered it as a form of neoteny. The fact that there are only five or six ovules in Coris arising from the base of the central stalk, which also alternate with the stamens, seems to support this idea. The view of reduced septa was also supported ana- tomically by Douglas (1936), who mentioned the presence of cavities at the base of the ovary in several species of Primulaceae. The triangular teeth supporting the ovules are of particular interest. he^ appear-as supporting struc- tures for the massive ovules, keeping them tightly packed (Figs. 18, 45).
Systematic position As discussed above, a wealth of evidence points to a close relationship between Coris and the Primulaceae. However, Sattler (1962) stressed the differences in morphology and floral development of Coris with Primulaceae and indicated an affinity with Lythraceae on a number of selected charac- ters. In our opinion the differences between Primulaceae and Coris tend to be minor against the wealth of similarities in their respective floral developments. We also see little evi- dence to interpret Coris as intermediate between Primulaceae and Lythraceae.
The fact that Coris lacks bracts may be related to the com- pact inflorescence and the presence of an epicalyx as dis- cussed above. Also the dorsiventrality of the flower is essentially restricted to the calyx and epicalyx; the remaining flower may become zygomorphic only at a very late stage of development. Other mainly polysymmetric families also have the occasional odd zygomorphic member (e.g., Dictamnus in Rutaceae; Schizanthus in Solanaceae). The fact that contrary to the other Primulales, the circular gynoecial rim arises on a convex apex, seems important at-first but may well be found in other uninvestigated taxa of the Primulales. Primula elatior (L.) Mill. (Clinckemaillie 1991) has the ring wall arising on a flat apex.
To consider Coris as intermediate between Primulaceae and Lythraceae (Sattler 1962; Willis 1966) is another matter. The similarities given by Sattler (e.g., a descending incep- tion of the calyx (not in Coris), a valvate calyx, the presence of an epicalyx, zygomorphy, obhaplostemony, common stamen-petal primordia, gynoecial rim, the colour of the petals) are nonspecific and may apply to numerous other taxa as well. The Lythraceae are a family with a high variability, and many similarities are probably a reflection of parallel evolution.
The existence of a separate family Coridaceae may well be accepted but is rather a matter of choice. A close affinity with the Primulaceae is undeniable, as Coris takes a highly evolved, separate position that invariably refers to the bulk of the Primulales.
Acknowledgements
We are greatly indebted to Professor Dr. P. Leins and the staff of the Institut fiir Systematische Botanik und Pflanzen-
geographie in Heidelberg for valuable help with improving our preparation techniques for the SEM. The Botanical Insti- tute of Heidelberg and the National Botanical Garden of Belgium are thanked for permission to use their SEM facili- ties. We are indebted to Professor Dr. C. Vandenberghen for heading a trip to Tunisia in 1988. We thank Dr. J . Kemp and an anonymous reviewer for constructive suggestions to improve the manuscript. This study was supported by research grants (project No. 2.0038.91; scanning electron microscope and project No. G.0143.95; general research project) from the National Fund for Scientific Research (N.F.W.O.). The first author is a postdoctoral researcher of the N.F.W.O.
References Carrion, J.S., Delgado, M.J., and Garcia, M. 1993. Pollen grain
morphology of Coris (Primulaceae). Plant Syst. Evol. 184: 89- 100.
Chant, S.R. 1978. Primulaceae. In Flowering plants of the world. Edited by V.H. Heywood. Oxford University Press, Oxford. p. 134.
Clinckemaillie, D. 1991. Plumbaginaceae en Primulaceae - Bloemontogenetische obsewaties met betrekking tot hun sys- tematische verwantschap. B.Sc. thesis, Department of Botany, Katholieke Universiteit Leuven, Belgium.
Clinckemaillie, D., and Smets, E. 1992. Floral similarities between Plumbaginaceae and Primulaceae: systematic significance. Belg. J. Bot. 125: 151 - 153.
Dahlgren, G. 1989. The last Dahlgrenogram. System of classifica- tion of the dicotyledons. In The Davis and Hedge Festschrift. Edited by K. Tan. Edinburgh University Press, Edinburgh. pp. 249-261.
Douglas, G.E. 1936. Studies in the vascular anatomy of the Primulaceae. Am. J. Bot. 23: 199-212.
Endress, P.K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge, England.
Erbar, C. 1988. Early developmental patterns in flowers and their value for systematics. In Aspects of floral development. Edited by P. Leins, S.C. Tucker, and P.K. Endress. J. Cramer, Berlin. pp. 7-23.
Erbar, C. 1991. Sympetaly - a systematic character? Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 112: 417 -45 1.
Erbar, C., and Leins, P. 1989. On the early floral development and the mechanisms of secondary pollen presentation in Campanula, Jasione, and Lobelia. Bot. Jahrb. Syst. Pflanzengesch. Pflan- zengeogr. 111: 29-55.
Ferguson, L.F. 1972. hi Flora Europaea. Vol. 3. Diapensiaceae to Myoporaceae. Edited by T.G. Tutin, V.H. Heywood, N.A. Burges, D.M. Moore, D.H. Valentine, S.M. Walters, and D.A. Webb. Cambridge University Press, Cambridge, England. p. 29.
Leins, P., and Erbar, C. 1987. Studien zur Bliitenentwicklung an Compositen. Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 108: 381-401.
Mabberley, D.J. 1987. The plant-book. Cambridge University Press, Cambridge, England.
Mattfeld, J. 1938. Das morphologische Wesen und die phylo- genetische Bedeutung der Blumenblatter. Ber. Dtsch. Bot. Ges. 56: 86-116.
Nishino, E. 1983. Corolla tube formation in the Primulaceae and Ericales. Bot. Mag. Tokyo, 96: 319-342.
Pax, F. 1897. Primulaceae. In Die natiirlichen Pflanzenfamilien IV, 1. 1st ed. Edited by A. Engler and K. Prantl. W. Engelmann, Leipzig. pp. 98 - 1 16.
Pfeffer, W. 1872. Zur Bliithenentwicklung der Primulaceen und Ampelideen. Jahrb. Wiss. Bot. 8: 194-215.
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.
Can. J. Bot. Vol. 73, 1995
Ritterbusch, A. 1991. Morphologisches Beschreibungsmodell tubiflorer Kronen, ein Beitrag zu Terminologie und Morpho- logie der Asteriden-Blute. Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 112: 329 -345.
Ronse Decraene, L.P., Clinckemaillie, D., and Smets, E.F. 1993. Stamen-petal complexes in Magnoliatae. Bull. Jard. Bot. Natl. Belg. 62: 97-112.
Roth, I. 1959. Histogenese und morphologische Deutung der Kron- blatter von Primula. Bot. Jahrb. Syst. Pflanzengesch. Pflanzen- geogr. 79: 1 - 16.
Sattler, R. 1962. Zur friihen Infloreszenz- und Blutenentwicklung der Primulales sensu lato mit besonderer Beriicksichtigung der Stamen-Petalum-Entwicklung. Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 81: 358 -396.
Sattler, R. 1974. A new approach to gynoecial morphology. Phytomorphology, 24: 22 -34.
Sattler, R. 1978. "Fusion" and "continuity" in floral morphology. Notes R. Bot. Gard. Edinb. 36: 397-405.
Sattler, R., and Lacroix, C. 1988. Development and evolution of basal cauline placentation: Basella rubra. Am. J. Bot. 75: 918-927.
Smets, E. 1988. Florale nektarien van de Magnoliophytina: karak- terizering en systematische betekenis. Doctorate thesis, Depart- ment of Botany, Katholieke Universiteit Leuven, Belgium.
Sundberg, M.D. 1982. Petal-stamen initiation in the genus Cyclamen (Primulaceae). Am. J. Bot. 69: 1707- 1709.
Takhtajan, A. 1980. Outline of the classification of flowering plants (Magnoliophyta). Bot. Rev. 46: 225 -359.
Tucker, S.C. 1984. Origin of symmetry in flowers. In Contem- porary problems in plant anatomy. Edited by R.A. White and W.C. Dickison. Academic Press, New York. pp. 351 -395.
Weberling, F. 1989. Morphology of flowers and inflorescences. Cambridge University Press, Cambridge, England.
Willis, J.C. 1966. A dictionary of the flowering plants and ferns. 7th ed. Cambridge University Press, Cambridge, England.
Can
. J. B
ot. D
ownl
oade
d fr
om w
ww
.nrc
rese
arch
pres
s.co
m b
y U
nive
rsity
of
Sask
atch
ewan
on
02/2
1/13
For
pers
onal
use
onl
y.