Notes on the Vascular Anatomy of the Fruit of Takhtajania (Winteraceae) and Its Interpretation

9 Pages·2000·7.1 MB·

by  Thierry Deroin

NOTES ON THE VASCULAR
Thierry Deroin'
ANATOMY THE
OF FRUIT OF
TAKHTAJANIA
AND
(WINTERACEAE)
ITS
INTERPRETATION^
Abstract
During fmit set the vascular skeleton of the Takhtajania gynoeciuni ihd not alter fundainenlally, hul there a transfer
is
of role in ovule nutrition from the median carpel bundles to meridian-lateral and partly lateral ones, hi accordance
with a pattern pr dy recognized in Annonaceae and Magnoliaceae. Lack of sclerification (only some phloem fibers)
of secondary' tissues and weak lengthening of stipe demonstrate the jiaedomorphic character of ihis genus among the
Winteraceae. This correlated with wider morphogenetic potentialities: syncarpy and likely dehiscence.
trait is
Key paedomorphy.
words: ovary, [)aracarpy, Takhtajania, winteroids.
About 20 years ago, the description of bicarpel- cedures (Gerlach, 1984), and then cut into 12 pim
late syncarpy in Takhtajania perrieri (Capuron) Bar- transverse sections, which were stained successive-
&
10%
0.5%
anova J.-F. Leroy from Madagascar (Leroy, 1977, ly with aqueous Astrablue and Ziehl's
1978, 1980; Vink, 1978) catalyzed a phase of re- fuchsin, and then dehydrated using acetone and
h and analysis regarding the evolution of the mounted in Eukitt.
A
gynoecium of Winteraceae and of Magnoliales in similar protocol was used for an older flower
More
general. recently, Leroy (1993) presented a from the type material {Perrier de la Bdthie 10158,
10%
brief synthesis of the debate resulting from this dis- P) after restoration using aqueous ammonia,
covery, which was all the more interesting since the postfixation in FAA, and the preparation of 8 |xm
&
him Comparison
information available the time gave every sections (Deroin Leroy, 1993). of the
at
reason to believe that the genus Takhtajania was material from these two sources was thus facilitat-
extinct. However, after considerable effort, Mala- ed. Photographs were prepared using a Zeiss pho-
gasy foresters and their colleagues from the Mis- tomicroscope with an orange filter and Ilford Pan F
ASA
T
souri Botanical Garden found living plants of Plus 50 film.
made
1997, and thtuehy possible
perrieri in to
it
undertake a study of the vascular anatomy of the Obskrvations
The
fruits of this species. results presented here
The
material available contained only the later
thus represent an unexpected continuation of an
development The
stages of fruit (Fig. series of
1).
gynoecium
earlier study of the of this plant (Deroin
fruits showed that: no growth, either in length
& (1)
Leroy, 1993).
or thickness, occurs outside the gy^noecium; a
(2)
,, ,- basal stipe(s) observed in the fruit must have
Matkhials and MrniODS
-
i d» un•ng i- i- r r
lormeu an i any
earlier stage, as lur-
little
it
The fruits examined in this study were collected ther elongation can be seen in the late series stud-
MO)
by Birkinshaw Anjanaharibe- and
C. {483, in the ied here, the stipe is not yet differentiated at
FAA
Sud They were ahhough
reserve. fixed in the field in anthesis (Vink, 1978), vascularization
its
&
and then transferred in the lab to a glycerol: etha- can already be detected (Deroin Leroy, 1993);
One
nol water solution for storage. fruit was de- the ovary locule does, however, grow consid-
(3)
(1)
:
hydrated using tertiary butanol and embedded in erably, and is asymmetrical in the plane of the two
paraffin (melting point =^ 60°C) using standard pro- carpels, one of which elongates more than the other.
express my gratitude to l*ete Lowr) (MO) for his Fnghsli translation of the original draft, Dawn Frame (MontpeHier,
'
I
France) for her kind help in literature and diseussions, as well as the anonymous reviewer for his careful corrections
and construitive remarks.
Museum
^ l^boratoire de l*hanerogamie, National (rHistoire Naturelie, 16, rue Buffon, F-750()5 Paris, France, de-
[email protected]
Ann. Missouri Bot. Card. 398-406. 2000.
87:
Volume Number
3 Deroin 399
87,
2000 Anatomy
Vascular
Fruit
Figure 1. Four developmental stages of Takhtajania fruit. In the sample studied, dehiscence (C) can take place
maximum
l)efore size reached, androecial zone; calyx and corolla zone; area of the ovar) locules; pedicel;
is a: c: p:
1:
stipe.
s:
This differential growth could explain the rather which are relatively narrower at this level. The
ir- (si),
regular dehiscence that proceeds downward from stele then becomes more complex (Fig. 2T) by giv-
wh
the stigmatic scars. ing rise to meridian-lateral traces, th
The anatomy of the pedicel and receptacle of the tures extend far to the interior by a well-differen-
fruit does not differ substantially from that of the tiated epidermis (Fig. 4C). The center obliterated
is
The
flower (Fig. 2). highly elliptic stele, with 15 by large-celled parenchyma, although at anthesis
&
vascular strands (Fig. 2A), gives rise to 2 median this level is hollow (Deroin Leroy, 1993, figs.
1,
sepals (Fig. 2B, C), and then their lateral bundles
3).
2D—
(Fig. G). The stele, which then becomes cir- At the base of the locule in the fruit (Fig. 2U)
cular and broadly meduUate in cross section (Fig. the lateral and median-lateral vascularizations are
much
2H), gives rise farther up (Fig. 21, J) to all of the more developed than the median carpellary
separate traces feeding the petals and stamens (ca. complexes, whereas the inverse is true at anthesis.
Up
27 The changes
in all). histological that take place to the mid-level of the locule, these divided
following anthesis are minimal: lignification of the dian complexes give rise on each side to 3 me-
xylem (vessels stainable with fuchsin) and forma- dian-lateral bundles and Fig. 3A-C),
(1, 2, 3,
tion of subero-phellodermal strata at the level of whereas the lateral carpellary bundles are generally
the corolla and the androecium. No secondary- phlo- separate (Fig. 3A-E, and
11, 12).
em-xylem down
structures form. Fruit dehiscence proceeds from the top as
At the extreme base of the stipe (Fig. 2K) the the wall is torn either between the separated lat-
gynoecium appears to lack cork, and the stele di- erals or next to the synlateral. No specialized
tis-
2L—
vides (Fig. 0) in connection with the dorsal su- sues can be seen at this level (Fig. 4F). The vas-
Higher 2P-
tures of the carpels. in the stipe (Fig. cularization at the top of the fntit is formally
S) the stele condenses in the plane of the sutures, identical to that observed in the ovar)- (Fig. 5A, C,
forming two symmetrical lines of bundles. Two di- E): meridian-lateral traces 1 and 2 fuse back with
vided median carpellary bundles can thus be rec- the laterals to form the placental bundles Fig.
(pi,
ognized, as often seen in Winteraceae, which are 5B, D). should be noted, however, that pl2
It is
fused to the meridian-lateral bundles to form me- comprised only of the median-lateral traces 1 and
dian complexes (mc) and the two synlateral bundles 2 of carpel 2. The median-lateral traces 3 terminate
400 Annals the
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Missouri Botanical
mm
5
— — —
B-G. Androecium
Figure 2. Asronding sections of Takhtajania fruit. A. Pedicel. Perianth. H-J. (n<»te the
—
—
peripheral cork). K-T. Stipe. U. Extreme hase of the ovary locule. lateral bundle; mc: median com{)lex; si:
1:
byrdateral; 1', 2', median-laterals.
1, 2,
Volume Number 3 Deroin 401
87,
Anatomy
2000 Vascular
Fruit
mm
5
—
—
Lower Upper
Figure 3. Ascending sections of Takhtajania fruit. A-F. half of the ovary. G-J. half of the ovary,
al, a2: apical vascular arcs; m: carpellar) rnedlan; pi: placental bundle; 1, 1', 2, 2', 3, 3', meridian-laterals.
402 Annals
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Missouri Botanical
I
500
|jm
— —
Figure 4. Histology of the fruit wall of Takhiajania. A. Synlaleral bundle (si') (cf. Fig. 3E). B. Meridian-lateral
— —
bundle 2' Fig. 3F above). C. Transverse section of the wall the level of the median l)undle ml. Transverse
(ef. at 1).
—
section of the wall at the level of the insertion of the seeds. E. Transverse section of llie wall at the level of the
—
meridian-lateral (midille of the ovary loeule). Transverse section of the wall the level of the synlateral
F. at (si) (cf.
Fig. 3F); note the unspecialized dehiscence ch^ft, with no epidermal boundaries.
Volume Number 3 Deroin 403
87,
Anatomy
2000 Vascular
Fruit
4P«l?r»";«iJ
y
.V
9'\
*fc''
* I
-tAV s:ii ' t'< V.' \ //.
' 1
j;
•^^r^
>rl*. >•-
J¥/
*' I.-
r.^^
>;/.v
'::«/
*<r! *yr,iu
rfr.
^Tt^
*
I-', ^ ^*N
^'"^
-V-'-v*, -/
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jjm
^r *-. J •V
'
fr
—
Figure Placental vascularization of Takhtajania. A, C, E. Ascending sections of one of the Iwo placentas at
5.
—
anthesis. B, D. Ascending sections of half a placenta at fruit stage (cf. 1', pi 1', Fig. 3H, I), dehiscence cleft visible
—
on right. F. Apical vascular arc a2 (cf. Fig. 3,
1).
404 Annals
the
of
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Missouri Botanical
&
and
in the wall, and the placental bundles fuse back visible at anthesis (Deroin Leroy, 1993) only
with the median bundles form vascular arcs al appears later in the development of Takhiajania,
to
and a2 The vascularization con- whereas rather frequent and probably primitive
(Figs. 31, J, 5F). It is
nected the stigmas naturally disappears along in other Winteraceae (Leinfellner, 1965, 1966a,
to
&
1966b; Endress, 1994; Igersheim Endress,
with the
latter.
The histological changes of the gynoecium that 1997).
take place from anthesis formation of appear Several very small, isolated bundles are found in
to fruit
be minor. The ovary wall 4E) shows a rather the medullary parenchyma (Fig. 20-P) of the fruit
to (Fig.
which
ordinary structure mid-height: a thin epidermis that not yet present anthesis, but are
at at
that highly fuchsin-stainable throughout the loc- likely homologous with the basal plexus of the gy-
is
ule and covered with a fairly thick hypodermis that noecia in Annonaceae and even in Magnoliaceae
almost palisadal in places; and lacunar paren- (Deroin, 1999). Higher up, the steles open once
is
chyma ca, 15 cells thick, including some fuchsin- again toward one another while folding back around
stainable secretory cells as well as cells with cal- the median complexes, which divide, as is gener-
cium oxylate crystals, but lacking sclerified cells. ally the case in Winteraceae.
The vascular bundles are surrounded by a crown From a strictly vascular perspective, the syn-
(3)
of highly fuchsin-stainable cells and are largely carpy found in Takhtajania is not particularly ad-
comprlsed of metaxylem and metaphloem that are vanced, as confirmed by the organization of the
separated by 3 to 5 layers of cambial cells. The stipe and the synlateral bundles, which are often
protoxylem crushed and the protophloem disjointed (Fig. 2U, II', and 12'; Fig. 3E, II, and
is is
lumen
transformed into sclerified fibers with a that In this respect the situati<m is similar to that
12).
sometimes narrow (Fig. 4A, B). No secondary found in Monodora brevipes Benth. (Annonaceae)
is
formations are present in the g^'uoecium. (Deroin, 1997).
At all levels the external epidermis clearly ex- (4) Fruit dehiscence in the material studied is
tends to the center of the divided medians (Fig. 4C, initially difficult to interpret, as the splitting could
have resulted from the dehydrating action of the
D).
fixative, which would account for the irregularity of
the opening. Nevertheless, the simple fact that this
Discussion
phenomenon can occur of interest, as no other
is
On member
the basis of this study, five important features syncarpous of Magnoliales has dehiscent
of the fruit of Takhtajania can be identified; fruits. Moreover, the possible occurrence of dehis-
Winteraceae appear to be characterized in cence in the mericarps of apocarpous Winteraceae
(1)
and
general by floral vascularization that lacks a corti- is still poorly understood (Harvey, 1982: 167),
New
members
cal system, and in which secondary vascular struc- was not reported for of the family in
&
tures are absent (Nast, 1944; Deroin Frame, Caledonia (Vink, 1993).
On
By xylem and epidermis
1998). contrast, lignification of the the contrary, differentiation of the
the appearance of phloem fibers are clearly delayed between the halves of the divided median bundles
in Takhtajania, as compared, for example, to Ex- suggests primitive dehiscence at this level, which
&
ospermum Zygogynum Frame, many Magnoliaceae and
or (Deroin 1998), in fact functional in
is still
in which differentiation occurs at anthesis. The to- even some archaic Annonaceae such as Anaxago-
hyma The
absence of scl in Takhtajania, espe- rea and Xylopia. presence of apical vascular
tal
cially in the fruit wall, appears to be unique within arcs (Fig. 31, al, and a2) linking the placental
J,
the family, based on the w^ork of Harvey (1982: zones, which are present in all Winteraceae studied
&
164). This type of unspecialized histology is also to date (Bailey Nast, 1943; Nast, 1944; Ueda,
&
found in the syncarpous gynoecia of Annonaceae— 1978; Harvey, 1982) except Drimys (Tucker Gif-
Monodoroideae (Deroin, 1997), although at anthe- ford, 1964; Tucker, 1975; Doweld, 1996), does not,
however, favor dorsal dehiscence.
The evolution of a stipe, as in most species The vascular rearrangements during fruit de-
(2) (5)
of Bubbia (Winteraceae) (Harvey, 1982: 169), velopment (Fig. 6) confirm that the nutritive role is
makes from median bundle
easier to interpret the vascularization at transferred the carpellary (A)
it
the base of the gynoecium and thus its morphology. to the lateral bundles (B), a phenomenon that ap-
In the lower half of the gynoecium the stele divides pears to be very generalized among Annonaceae
to form two closed steles (Fig. 2K-P), which in fact (Deroin, 1997) and Magnoliaceae (Deroin, 1999).
The
clearly represent an incomplete fusion of the pel- strengthening in the fruit of the meridian-lat-
tate bases of the two carpels. This peltation was not eral bundles of the first and second orders (Fig. 6,
Volume Number
87, 3 Deroin 405
2000 Anatomy
Vascular
Fruit
#
a
»
4
4
ff
A
mc
I'
I
Figure 6. Interpretive schemes of transfer of vascular functionality in the gynoecium of Takhtajania from anthesis
(A) to mature fruit (B). a: apical vascular arc; lateral; m, median; mc, median complex; pi, placental l>undle; 2
1, 1,
and
median-lateral bundles.
3:
1, 1', 2, 2'), which then contribute in large part to ovules (to 4 per carpel in the material studied),
the apical placental bundles (Fig. 6, pi', pi), leads perhaps following fusion of the carpels. This re-
to a vascular pattern that is functionally compara- duction does not appear to have occurred in the
ble to that of the carpel in Amhavia gerrardii syncarps of Annonaceae— Monodoroideae (Deroin,
(BailL) Le Thomas, a rather primitive Malagasy An- 1991), and instead results from the distinctive pla-
nonaceae, in which the ovules are fed by the me- centation of Winteraceae.
&
ridian-lateral traces (Deroin Le Thomas, 1989).
In the case of Takhtajania (Fig. 6B), eight func-
Conclusions
tional meridian-lateral bundles (four per carpel)
feed the eight seeds, with an additional role being Study of the fruit of Takhtajania shows that only
played by the synlateral traces. The remaining four modest changes have taken place in the organiza-
meridian-lateral traces, of the third order, most tion of the ovary, but that they are nevertheless very
likely represent the relictual vascularizations of instructive. The latent peltation of the carpels and
four additional ovules. While the closely related ge- the formation of a very short stipe resemble the
nus Bubbia has an average of 12 ovules per carpel tricarpellate apocarpous gynoecium of Anaxagorea
(Harvey, 1982: 172), the genus TaA/jfq/ama appears luzonensis A. Gray, a primitive Annonaceae (De-
to have undergone a reduction in the number of roin, 1988), and thus suggest the early appearance
406 Annals the
of
Garden
Missouri Botanical
magnolialean
Annonaceae— Monodoroideae anatomical chararters relale^d to the par-
of syncaq>y as in (De-
Compt. Rend. Acad. Sen Vie
acarpv. Sci. Paris, 3, Sci.
roin, 1991), which presences in some way the prim-
725-729.
316:
open carpel structure. The vascularization of &
itively On
A. Le Thomas. 1989. systcmalics and ev-
Am
the seeds shows a delayed pattern which parallels olutive potentialities of Annonac-eae: Case of ha via
g>noecium Thomas, an endemic Malagasy spe-
that of the ovules of the syncarpous of gerrardii (Baill.) I.e
Compt. Rend. Acad. Vie
cies. Sci. Paris, S^r. 3, Sci.
gynoecium
Canellaceae (Leinfellner, 1967); the of
647-652.
309:
Takhtajania thus paedomorpic, with a carpel pat-
is
g ^^•_
^ ^,j,^^ q^^ ^^-^^^^ ^f ^.^^^^, ^^
^^^^^_^{^^^ ^,^^. j,^^.
tern very near that oi Buhhia, a rather few-carpelled denced vascniar skeh^on. Phytomorphology 46:
l)y its
and thus archaic genus to 11 carpels after Har- 387-394.
(1
Undress, K^^1994. Diversity and Evolutionaiy Biology
vey, 1982: 148). In these two genera the dehiscence P.
Cambridge Cambridge.
of Tropical Flowers. Univ. Press,
was dorsal, as demonstrated by the epider-
at first
Cerlach, D. 1984. liotanische Mikrotechnik, ed. 3, Thie-
mal median the
differentiation the trace level,
at
me,
Stuttgart.
ventral dehiscence being restored in Takhtajania Harvey, W. 1982. Systematic Studies Ruhhia Van
in
J.
Tieghem and Related (xenera. Unpuhlislied Thesis,
because of the imperfection In vascular syncarpy.
Reading.
University of
By Annonaceae— Monodoroideae,
comparison,
in all
&
Gynoecium
Igersheim, A. K. Endress. 1997. diver-
P.
with indehiscent however, vascular syncarpy
fruits,
and systemalics of the Magnoliales and winteroids.
sity
yet more advanced in Isolona than in Monodora, 213-271.
is Bot. binn. Soc. 124:
J.
sometimes even with an ultimate reduction and dis- Leinfellner, ^. 1965. sind die \^'interaceen-Karpel!e
\^'ie
—
gehaut? Die Karpelle von Drimys, Sek-
talsiiclilich
appearance of synlateral traces (Deroin, 1997). I
554—575.
tion Tasmannia. Osterr. Bot. Z. 112:
When
considering the continuum from the flower
W
Winteraceen-Karpelle
1966a. sind die
ie tat-
. —
morphological and functional con-
to the fruit, this
sachlic-h gebaut? Ober das Vorkonnnen einer rlng-
II
among Gondwanan
vergence Magnoliales appears formigen lUazenla den Karpellen von IJrimys, Sektlon
in
84-95.
highlight their shared dispersal syndrome, likely Wintera. Osterr. Rot. Z. 113:
to
Wie Winteraceen-Karpelle
1966b. sind die
tat-
common
due paleoenvironmental constraints. . —
to
sachlich gebaut? HI Die Kar[)elle von Bubhia. Bel-
As main
a remark, noticeable that the
final is
it
Exospcrmum und Zygogynum,
Pseudowinlera,
lioluni,
vascular angements during the fruit set are lo- 245-264.
Osterr. Bot. Z. 113:
cated in the winteraceous gynoecium only, while 1967. Ober die Karpelle verschiedener Magno-
.
bales. V. Pleodendron (Canellaceae). Osterr. Bot. Z.
the regular receptacle vasculature too subject to
is
502-507.
114:
Magnoliaceae and Annonaceae,
disruptions in in
A
Leroy, 1977. compound ovary with open carpels
J.-F.
close relation with seed nutrition (Deroin, 1999).
Winteraceae (Magnoliales); Evolutionary implica-
in
977-978.
Science 196:
tions.
1978. Une sous-famille monotypiipie de
\^'in-
Literature Cited .
teraceae endemi(|ue ^ Madagascar: Les Takhtajanioi-
&
Bailey, 1. W. C. G. Nast. 1943—. The comparative mor- deae. Adansonia, sen 2, 17: 383-395.
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.
472-181.
bor. 24: (Winteraceae-Takhlajanioideae). Adansonia,
tajania
T
Deroin, 1988. Aspects analomicjues et biologiques de 9-20.
20:
ser. 2,
des Annonac^es. Unpublished Thesis, Univer-
la fleur 1993. Histoire des travaux sur le Takhtajania.
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1991. Distribution of stigmatic plate [)aUenis Masson,
Fleurs. Paris.
.
and Annonaceae. Compt. Rend. Aead.
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—
Paris, S^r. 3, Sci, Vie 312: 561-5r)6. Winteraceae. VI Vascular anatomy of the flowering
1997. Confirmation and origin of the paracarpy shoot. Arnold Arbor. 25: 454-466.
. J.
comments some
in Annonaceae, with on methodological Tucker, C. 1975. Carpellary vasculature and the ovular
S.
CandoUea 45-58. 191-197.
aspects. 52: supply Drimys. Arner. 62:
in B(»t.
J.
&
1999, Functional impact of the vascular archi- E. M. Gilford. 1964. Carpel vascularization of
.
lecture of flowers in Annonaceae and Magn<»liaceae. Drimys lanceolata. Phytomori)liology 14: 197-203.
and bearing on the interpn»talioti of the magnolia- Ueda, K. 1978. Vasculature the carpels of Belliolum
its in
213-224.
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D. Frame. 1998. Flower vasculature in 119-125.
noliaceae, Annonaceae and Winteraceae: Lessons in Vink, W. 1978. The Winteraceae of the Old World. HI.
The Sym- Bhnnea 521—
evolutionary constraints. First International Notes on the ovary of Takhtajania. 24:
posium on ihe Family Magnoliaceae, Guanzhou, R. 525.
P.
&
Mackee
China, Abstracts: 26. 1993. Winteraceae. Morat H. S.
//(.• P.
.
&
On 90—171.
Feroy. 1993. the interjiretalion of ova- (editors), Flore de la Nouvelle-Caledonie 19:
J.-F.
Museum
vascularization Takhtajania interaceae). Sonie National d'Histoire Naturelle, Paris.
ry in (^^