599
Vol.48, n. 4 : pp. 599-610, July 2005
ISSN 1516-8913 Printed in Brazil
BRAZILIAN ARCHIVES OF
BIOLOGY AND TECHNOLOGY
A N
I N T E R N A T I O N A L
J O U R N A L
Anatomy of the Pericarp and Seed-coat of Lithraea
molleoides (Vell.) Engl. (Anacardiaceae) with Taxonomic
Notes
Sandra Maria Carmello-Guerreiro1* and Adelita Aparecida Sartori Paoli2
1
Departamento de Botânica; Instituto de Biologia; Universidade Estadual de Campinas - UNICAMP; C. P. 6109;
13083-970; Campinas - SP - Brasil. 2Departamento de Botânica; Instituto de Biociências; Universidade Estadual
Paulista - UNESP; C. P. 199; 13506-900; Rio Claro - SP - Brasil
ABSTRACT
The aim of the present work was to record anatomical data for the fruit and seed of Lithraea molleoides (Vell.)
Engl, and compare the results with those for L. brasiliensis and the genera Schinus and Rhus. The L. molleoides
fruit was a drupe with a friable and lignified exocarp. The mesocarp was parenchymatous with large secretory
canals associated with vascular bundles. The endocarp consisted of four layers: an outer layer of polyhedral cells
with prismatic crystals of calcium oxalate, and three inner layers of sclereids in a palisade arrangement. The ovule
was anatropous, unitegmic, and crassinucelate. In the chalazal region, a cup-like zone of tanniniferous parenchymal
cells formed the hypostase. The developing seed had a circinotropous–like shape, that originated through curvature
of the long, coarse funicle that surrounded the tegument and embryo sac. The ripe seed was endotestal with bar-like
thickenings or pittings in the cell walls.
Key words: Anacardiaceae, anatomy, pericarp, seed-coat
INTRODUCTION
The Anacardiaceae was currently divided into
five tribes (Anacardieae, Spondiadeae, Rhoeae,
Dobineeae and Semecarpeae), but this suprageneric classification was still controversial.
Morphological, anatomical and rbcL sequence
analyses by Terrazas and Chase (1996)
suggested that two large clades should be
recognized. One of these was monophyletic and
contained members of the Spondiadeae group,
while the second contained Anacardieae and
Rhoeae. Although floral features had been used
extensively to separate the taxa within the
Anacardiaceae, Terrazas and Chase (1996)
*
suggested that anatomical features of the endocarp
and wood characters were more useful.
The tribe Rhoeae contained the genera Rhus,
Schinus, Pistacia, Astronium, Schinopsis, Lithraea,
Myracrodruon and others. Based on an analysis of
the structure of the pericarp in 29 genera, Wannan
and Quinn (1990) identified two basic types of
endocarp- Spondias-type and Anacardium-type - in
the Anacardiaceae. The tribe Rhoeae could be
divided into three groups A, B and C based on
endocarp structure. Groups A and B were classified
as Anacardium–type and group C as Spondias-type.
The genera Rhus, Schinus, Schinopsis, Lithraea and
Myracrodruon were classified in group A, in which
the endocarp consists of four layers of cells. The
three internal layers were formed from sclereids
Author for correspondence
Brazilian Archives of Biology and Technology
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Carmello-Guerreiro, S. M. and Paoli, A. A. S.
organized in a palisade arrangement while the
external layer was crystalliferous layer.
The external morphology of the fruit and the
structure of the endocarp and seeds were very
similar in Rhus, Schinus and Lithraea. Based on
an analysis of the anatomical features of the fruit
and seeds of Lithraea brasiliensis, Pienaar and
Von Teichman (1998) concluded that this
species ought to be included in the genus Rhus
under the name Rhus brasiliensis,
a
combination that, until publication of the
foregoing article, was not valid.
In this report, we describe new anatomical data
for the fruit and seed of a Brazilian species of
Lithraea, L. molleoides, and compare the results
with those for L. brasiliensis and the genera
Schinus and Rhus. Currently, only four species
of Lithraea were known worldwide, with L.
molleoides and L. brasiliensis being native to
Brazil (Engler, 1876; Barkley, 1962).
MATERIALS AND METHODS
Fruits of Lithraea molleoides (Vell.) Engl. at
different stages of development were collected
from specimens grown in the Botanical Garden
of the Instituto de Biociências, UNESP,
Botucatu, SP, Brazil. The morphological and
anatomical studies were done using fresh
material and material fixed in FAA (Johansen,
1940). The morphological characteristics of the
fruits were described and illustrated using fruits
sampled from at least five trees. The
nomenclature used here was based on Radford et
al. (1974) for the formed of the fruits, Spjut
(1994) for the type of the fruit, and Roth (1977)
for the pericarp layers.
Permanent slides were prepared from fixed
samples embedded in plastic resin (Historesin,
Leica) using the technique described by Gerrits
(1991). The embedded material was glued to
blocks of wood with epoxy-glue. Sections were
cut on a rotary microtome with type C steel
knives. The sections were stained with 0.05%
toluidine blue in acetate buffer with pH 4.7
(O’Brien et al., 1964) and mounted in synthetic
resin.
For histochemical tests, the sections of fresh
material were treated with a) an aqueous
solution of FeCl3 to detect phenolic compounds,
b) phloroglucinol-HCL for lignified walls (Sass,
1951), c) Sudan IV for lipids, chloridric and d)
sulphuric acids for crystals (Johansen, 1940).
RESULTS
Morphology of the fruit and seed
The fruit was a white-greyish, smooth globose drupe
4-8mm in diameter, with a friable exocarp when
ripe. The secretory mesocarp was dark and joined to
the stone endocarp. The seed, one per fruit, was
laterally compressed (Fig. 7) and derived from an
anatropous ovule (Fig. 1) inserted on the basallateral side of the ovary. The seed-coat was
membranaceous, smooth, and light yellow with a
dark brown patch. As the seed grew, the long,
curved, coarse funicle stick to the tegument of the
seed (Figs. 2-7). The chalazal region and the funicle
were seen externally as a dark brown patch in the
ripe seed.
Ovary
The ovary was uniloculate with only one ovule (Fig.
1). The outer epidermis, which was uniseriate was
covered with a cuticle and has stomata. The
epidermal cells were radially elongated, with evident
nuclei (Figs. 8 and 9). The ovarian mesophyll was
formed by parenchyma cells and secretory canals
associated with vascular bundles. The parenchyma
cells close to the canals contained phenolic
compounds (Figs. 8 and 9)
The inner epidermis of the ovary was multilayered
with periclinal divisions that formed a pluristratified
endocarp (sensu stricto) (Figs. 10-12). The layer of
cells covering the locule had a cuticle and was the
first to elongate radially (Fig. 12).
The structure of the pericarp
Longitudinal and transversal sections of young fruits
showed the following anatomical features:
a) An outer epidermis with radially-elongated
cells (Fig. 13);
b) A
parenchymatous
central
zone
characterized by secretory canals associated
with vascular bundles arranged compactly,
next to the other, in one layer, and a large
number of parenchyma cells with phenolic
compounds surrounding the secretory canals
(Fig. 13); and
c) A multilayered inner epidermis with three
layers of radially-elongated cells and one
with crystals (Fig. 13)
Brazilian Archives of Biology and Technology
Anatomy of the Pericarp and Seed-coat of Lithraea molleoides
The outer epidermis form the exocarp (sensu
stricto) which, in the ripe fruit, lignified and
became friable (Figs. 13 and 14 ).
During the development of the fruit, the
mesocarp consisted of a parenchymatous zone,
secretory canals and vascular bundles and
underwent very few changes, most of which
involved an increase in the number of cells and
in the size of the secretory canals (Figs. 15-17).
The presence of parenchyma cells with phenolic
compounds (Figs. 16 and 17) and canals with an
amber colored secretion (Fig. 17) was
characteristic in this species. In the ripe fruit, the
mesocarp was secretory, became black and
detaches from the exocarp. The separation of the
exocarp and mesocarp occurred between the
epidermis and the first layer of mesocarp cells
(Fig. 14).
The endocarp consisted of four layers of cells,
that were fully derived from the inner epidermis
of the ovary wall and formed the endocarp sensu
stricto (Figs. 10-12). In ripe fruit, the endocarp
consisted of an outer layer of small polyhedric
cells with prismatic crystals of calcium oxalate
followed by three layers of sclereids in palisade
in which the second layer had smaller cells than
the first and third layers (Figs. 18-20). In ripe
fruit, the four layers of cells that formed the
endocarp became thicker and the walls became
lignified (Figs. 19 and 20).
The seed
The ovule was anatropous, unitegmic and
crassinucelate, with an evident dorsal raphe and
a coarse funicle inserted in a basal-lateral
position in the ovary wall (Figs.1 and 8). The
developing seed had a circinotropous–like shape
originates through the curvature of the long,
coarse funicle that surrounded the tegument and
embryo sac (Figs. 2-7, 21 and 26)
601
In the micropyle region, the tegument was formed by
5-12 layers of cells (Figs. 22 and 23). Tanniniferous
deposits were present in the outer epidermis (Fig.
23). In the inner epidermis the cells were small, with
a dense cytoplasm and were arranged compactly
(Fig. 23). In the anti-raphe region, the tegument was
formed by 4-5 layers of cells (Figs. 24 and 25). The
outer epidermis cells were radially elongated and
those of the inner epidermis were small and cubic,
with a dense cytoplasm, and were arranged
compactly. In the chalazal region, a very
characteristic cup-like zone of tanniniferous
parenchyma cells partially surrounded the nucellus
and the embryo sac to formed the hypostase (sensu
lato) (Figs. 21, 24, 26 and 27). The funicle was
coarse, with a vascular bundle that was surrounded
by a sheath of phenolic compound cells (Fig. 27) and
grew towards the micropyle to formed a funicular
obturator (Fig. 21 and 26).
In a further stage of development, the single
tegument or testa in the micropyle and anti-raphe
region had 4-12 layers of cells. The outer epidermis
of the testa was formed by large polyhedral radially
elongated cells containg phenolic compounds (Fig.
28). The inner epidermis of the testa has small, cubic
cells with evident nuclei and a dense cytoplasm (Fig.
28). The mesophyll had a loose fitting and were
compressed in some places. Immediately below the
tegument, a few cell layers of the nucellus were
compressed. The endosperm had several layers of
cells with an evident nucleus and dense cytoplasm in
the peripheral embryo sac (Figs. 25, 27and 28) and
was quite vacuolated in the center. The ripe seed was
exalbuminous, but showed the remainder of the
nucellus and endosperm.
In the raphe-chalazal region, the hypostase contained
cells with phenolic compounds and druses of
calcium oxalate (Fig. 30).
The growth of the funicle was not proportional to
seed development and ripe seeds show only
remnants of the funicle (Figs. 29 and 31).
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602
Carmello-Guerreiro, S. M. and Paoli, A. A. S.
SP
PE
VB
VB
FN
OV
OB
RA
RC
1
EP
HP
CA
2
CA RA
3
4
FN
7
5
6
Figures 1-7 - 1. Longitudinal section of a flower with an anatropous ovule inserted on the basal-lateral side
of the ovary. 2. Longitudinal section of a very young seed. 3-7. Stages of seed development.
(CA=chalaza; EP=epidermis; FN=funicle; HP=hypostase; RA=raphe; TE=testa; SP=sepal;
PE=petal; OV=ovule; OB=obturator; VB=vascular bundle; RC=receptacle)
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Anatomy of the Pericarp and Seed-coat of Lithraea molleoides
603
11
EN
OM
12
8
EX
EX
ME
9
SC
ME
SC
EN
13
EN
10
14
Figures 8-14 - 8. Longitudinal section of an ovary. (OM=ovarian mesophyll) (scale bar=250µm). 9-13. Transversal
secction of a young fruit. 9.Uniseriate exocarp (EX) and mesocarp (ME) (scale bar= 50µm). 10.
Mesocarp (ME) with secretory canals (SC) and the multilayered endocarp (EN) (scale bar=50µm).
11. Endocarp in division (arrows) (scale bar=50µm). 12. Multilayered young endocarp (EN) (scale
bar=50µm). 13. Pericarp. (SC=secretory canal; EN=endocarp; EX=exocarp; short arrow=stoma;
white arrows=phenolic compounds) (scale bar=50µm). 14. Detail of the mature exocarp. White
arrow showed the region of separation between the exocarp and mesocarp (scale bar= 125µm).
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Carmello-Guerreiro, S. M. and Paoli, A. A. S.
15
18
✱
19
SC
16
SC
EN
17
20
Figures 15-20 - 15. Transversal section of a ripe fruit (scale bar=1000µm). 16. Pericarp in longitudinal section
(scale bar=150µm). 17. Mesocarp with phenolic compounds and secretory canals with dense
secretion and multilayered endocarp (scale bar=500µm). 18. Four layers of endocarp without
lignification (scale bar=125µm). 19. Three outer layers of ripe endocarp. The arrow showed the
★ and ✱) (scale bar=50µm). 20. Lignified
crystalliferous layer and two palisade lignified layers (★
inner layer of ripe endocarp (scale bar=50µm).EN=endocarp; SC=secretory canal.
Brazilian Archives of Biology and Technology
Anatomy of the Pericarp and Seed-coat of Lithraea molleoides
VB
AR
605
ES
HP
21
TE
24
TE
ED
NU
ES
25
22
23
26
Figures 21-26 - 21. Longitudinal section of the circinotropous-like shape of a young seed. (VB=vascular bundle)
(scale bar=500µm). 22. Detail of the micropyle region of a young seed. (TE=testa; ES=Embryo
sac) (scale bar=125µm). 23. Testa in the micropyle region. The black arrow showed the outer
epidermis of the testa with phenolic compounds and the white arrow showed the inner epidermis of
the testa (scale bar=80µm). 24. The anti-raphe (AR) region indicated with arrow; hypostase (HP)
and embryo sac (ES)(scale bar=125µm). 25. Detail of the layers of the anti-raphe region.
(TE=testa; NU=nucellus; ED=endosperm) (scale bar=50µm). 26. Longitudinal section of a young
seed showing a well-developed hypostase (arrow); endosperm (ED) and heart-shaped embryo
(scale bar=100µm).
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Carmello-Guerreiro, S. M. and Paoli, A. A. S.
NU
HP
ED
EM
VB
27
30
TE
FA
NU
ED
28
31
29
32
Figures 27-32 - 27. Chalazal region showing the endosperm (ED), nucellus (NU), hypostase (HP), vascular bundle
(VB) (scale bar=250µm). 28. Longitudinal section of the anti-raphe region (TE=testa,
NU=nucellus; ED=endosperm) (scale bar=40µm). 29. Longitudinal section of the ripe seed. The
arrow indicates the vestigial funicular aril (scale bar=100µm). 30. Raphe-chalazal region of the ripe
seed. Arrows show druses (EM=embryo) (scale bar=50µm). 31. Anti-raphe region. The arrow
indicates secondarily thickened, lignified and abundantly pitted walls. (FA=vestigial funicular aril;
EM=embryo) (scale bar=250µm). 32. Remains of the testa (black arrow) and pitted walls (white
arrow) of the inner epidermis of the testa (scale bar=50µm).
Brazilian Archives of Biology and Technology
Anatomy of the Pericarp and Seed-coat of Lithraea molleoides
The seed-coat was formed by waste from the
testa, funicle, raphe-chalazal region and the
hypostase (Fig. 30), with the testa cells
appearing as flattered, non specialized cells
(Figs. 30 and 32). The cells of the inner
epidermis of the testa were small, secondarily
thickened, lignified and had extensively pitted
walls (Figs. 31 and 32), indicating an endostestal
status. In some parts of the anti-raphe, only the
endotesta covered the embryo (Fig.32).
In the ripe seeds, the only multiplicative region
was the raphe-chalazal, with the micropyle and
the
anti-raphe
regions
showing
little
stratification (Figs. 29-32).
DISCUSSION
In the Anacardiaceae, the structure of the
pericarp was an important diagnostic character,
especially at the generic level. According to
Wannan and Quinn (1990), the endocarp of the
Anacardiaceae could be divided into two basic
types: the Spondias-type, in which the sclereids
were irregularly guided, and the Anacardiumtype, in which they were regularly guided.
Lithraea, Rhus and Schinus all had an
Anacardium-type endocarp.
The structures of the exo-, meso- and endocarp
of Rhus, Schinus and Lithraea showed many
resemblances and were summarized in Table 1.
The exocarp in L. molleoides and in L.
brasiliensis (Pienaar and Von Teichman, 1998)
were formed only by the outer epidermis. In ripe
fruit, the cells had a thick non-lignified but very
strongly cutinized wall that was separated at the
mesocarp, which made it friable. In some
species of Schinus, such as S. terebinthifolius
(Carmello-Guerreiro and Paoli, 2002) and S.
molle (Soos and Hausknost, 1951), the exocarp
was formed by the epidermis plus the hypoderm,
and became lignified, friable and separeted from
the mesocarp. In Rhus lancea (Von Teichman
and Robbertse, 1986; Von Teichman,1989) and
in R. problematodes (Von Teichman and Van
Wyk, 1991), the exocarp consisted of the outer
epidermis, the hypoderm and a viariable number
of mesocarp layers. In R. lancea, the hypoderm
showed cells with thick, lignified walls, while in
Rhus problematodes they were not lignified. In
Rhus (Toxicodendron) diversiloba (Copeland
and Doyel, 1940), the exocarp was papery, but
its was unclear how many layers constitute the
607
exocarp. The exocarp of Rhus aromatica and R.
glabra was formed by the outer epidermis (Li et al.,
1999).
Schinus and Lithraea had a friable exocarp that
separeted from the mesocarp. In Rhus glabra and R.
aromatica, the single-layerd exocarp and the outer
mesocarp (with parenchyma cells) were considered
as “papery fruit peel” that separeted from the rest of
the fruit (vascular bundles and inner mesocarp) (Li et
al., 1999). It was unclear whether other Rhus species
had a the presence of friable exocarp and if this
separeted from the mesocarp.
In all of the species studied in these three genera, the
mesocarp was formed largely by parenchyma cells,
tannic idioblasts and secretory canals associated with
the vascular bundle. However, in Rhus lancea (Von
Teichman and Robbertse, 1986; Von Teichman,
1989), R. problematodes (Von Teichman and Van
Wyk, 1991), R. glabra and R. verniciflua (Brizicky,
1963; Li et al., 1999), the inner part of the mesocarp
was sclerified and could be a part of the endocarp. In
Lithraea molleoides, L. brasiliensis (Pienaar and
Von Teichman, 1998), Schinus terebinthifolius
(Carmello-Guerreiro and Paoli, 2002) and S. molle
(Soos and Hausknost, 1951), no sclerification of the
inner part of the mesocarp was observed..
The endocarp could be formed by the inner
epidermis of the ovary and its immediate derivates,
in which case it was referred to as sensu stricto; if
the endocarp also include layers of the mesocarp
then it was referred to as sensu lato (Roth, 1977). In
Lithraea molleoides, L. brasiliensis (Pienaar and
Von Teichman, 1998) and Schinus terebinthifolius
(Carmello-Guerreiro and Paoli, 2002) the endocarp
was of the sensu stricto type since was formed by
four layers fully derived from the inner epidermis
and consisted of an outermost crystalliferous layer
and three inner layers formed by sclereids in
palisad; the latter layers covered the locule.
In Rhus lancea (Von Teichman and Robbertse,
1986; Von Teichman, 1989), R. problematodes (Von
Teichman and Van Wyk, 1991), R. glabra and
R. verniciflua (Brizicky, 1963; Li et al., 1999), the
endocarp was sensu lato since the sclerified portion
of the mesocarp was part of the endocarp. Only in
R.
aromatica
was
the
inner
mesocarp
parenchymatous and the endocarp was defined as
sensu stricto (Li et al., 1999).
The inner part of the endocarp, or endocarp sensu
stricto, developed from the inner epidermis of the
ovary and its four-layered structure was very similar
among species of Lithraea and Schinus (CarmelloGuerreiro and Paoli, 2002; Pienaar and Von
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608
Carmello-Guerreiro, S. M. and Paoli, A. A. S.
Teichman, 1998; Soos and Hausknost, 1951). In
almost all species of Rhus studied by Copeland
and Doyel (1940), Brizicky (1963), Von
Teichman and Robbertse (1986), Von Teichman
(1989), Wannan and Quinn (1990) and Von
Teichman and Van Wyk (1991), the layer of
macrosclereids in contact with the locule had
wavy radial walls, except in R. glabra and R.
aromatica (Li et al., 1999). This feature was not
observed in any species of Lithraea or Schinus
studied so far.
The seeds of Rhus, Schinus and Lithraea were
considered to be partially pachychalazal (Von
Teichman, 1991; Carmello-Guerreiro and Paoli,
1999) since the chalazal part of the seed-coat was
smaller than the tegument part, and was
characterized by an endotegmen with a thickened,
lignified cell wall and bar-like or pitted
thickenings that prevent the collapse of the cells
(Piennar and von Teichman 1998). The partial
pachychalaza observed in these genera was easily
distinguished externally by that dark-brown color
seen in the seed-coat. A tanniferous hypostase
was also a common feature of these three genera and
of the Anacardiaceae in general (Von Teichman and
Van Wyk, 1994), as was the amphicribral vascular
bundle and crystalliferous cells of the raphe (Pienaar
and Von Teichman, 1998 and Carmello-Guerreiro and
Paoli, 1999).
The ovules of L. molleoides and R. problematodes
were basal but in Schinus they were apical (CarmelloGuerreiro and Paoli, 1999). Rhus and Schinus had an
anatropous ovule (McNair, 1921; Kelkar, 1958; Von
Teichman, 1991; Von Teichman and Van Wyk,
1991). L. molleoides also has an anatropous ovule,
but after fertilization the funicle grew, curves and
surrounded the tegument and embryo sac to give the
young seed a circinotropous-like shape. In addition,
the ovule of L. molleoides was unitegmic whereas in
the species of Rhus and Schinus mentioned above the
ovule was bitegmic.Pienaar and Von Teichman
(1998) described the ovule of L. brasiliensis as
bitegmic.
Table 1 - Comparison of the anatomical characters of the exo-, meso- and endocarp in Lithraea, Schinus and Rhus
species.
Exocarp
Mesocarp
Endocarp
Epi
Hyp
OM
IM
CL
OL
ML
IL
Lithraea molleoides
Lig*
__
ParSC-t
Par
Par
Scl
Scl
Scl
Lithraea brasiliensis
(Piennar and Von Teichman,
TW
__
ParSC-t
Par
Par
Scl
Scl
Scl
1998)
Schinus terebinthifolius
(Carmello-Guerreiro and Paoli,
Lig
Lig*
ParSC-t/c
Par
Par
Scl
Scl
Scl
1999)
Schinus molle
(Soos and Houknost, 1951)
Lig
Lig*
ParSC-t/c
Par
Par
Scl
Scl
Scl
Rhus glabra
(Li, Baskin and Baskin, 1999)
Pa
?
ParSC-t/c*
Scl-t
Par
Scl
Scl
Scl(w?)
Rhus aromatica
(Li, Baskin and Baskin, 1999)
Pa
?
ParSC-t/c*
Par
Par
Scl
Scl
Scl(w?)
Rhus problematodes
(Von Teichman and Van Wyk,
1991)
Rhus lancea
(Von Teichman and Robbertse,
1986; Von Teichman, 1989)
Rhus diversiloba
(Copeland and Doyel, 1940)
TWt
TWt
ParSC-scl
Scl-t
Par
Scl
Scl
Scl-w
TWt
TWt
ParSC-scl
Scl-t
Par
Scl
Scl
Scl-w
Pa*
?
ParSC-scl
Par
Par
Scl
Scl
Scl-w
Legend: (---) absent. (?) uncertain. (*) Exocarp detaches from the mesocarp. Exocarp: Epi=epidermis; Hyp=hypoderm;
Lig=lignified; Pa=papyriferous; TW=thickened wall; TW-t=thickened wall tanniferous. Mesocarp: OM=outer mesocarp;
IM=inner mesocarp; Par=parenchyma; SC-t/c/scl=tanniferous cells (t), crystalliferous cells (c), sclerenchyma cells (scl)
encircling the secretory canals. Endocarp: CL= crystalliferous layer; OL=outer layer; ML=median layer; IL=inner layer;
Scl=palisade sclerenchyma cells; Scl-w=palisade sclerenchyma cells with wavy walls.
Brazilian Archives of Biology and Technology
Anatomy of the Pericarp and Seed-coat of Lithraea molleoides
As shown for several species of Rhus (McNair,
1921; Kelkar, 1958; Von Teichman, 1991; Von
Teichman and Van Wyk, 1991) and for S. molle
(Soos and Hausknost, 1951; Copeland, 1959) and S.
terebinthifolius (Carmello-Guerreiro and Paoli,
1999), the ovules of Rhus and Schinus showed
greater similarity among themselves than do those
of Rhus compared to Lithraea. In Schinus, as in
Rhus, the ovule was bitegmic, with the outer
tegument being much longer than the inner one.
In L. molleoides, the bar-like thickenings or
pittings on the cell walls of the inner epidermis of
the testa characterized it as an endotestal seed, as
indicated by Corner (1976). This type of
thickening has been a very common feature of
different species of Anacardiaceae, in the
endotesta and endotegmen.
CONCLUSION
Lithraea and Schinus differed Rhus in the structure
of their endocarp. In the first two genera, the
endocarp was of the sensu stricto type and
consists of four layers of sclereids derived from
the inner epidermis of the ovary. In Rhus, the
endocarp was sensu lato type since it had layers of
the mesocarp as well as the four layers from the
inner epidermis. In addition to these differences,
the sclereids in contact with the locule had wavy
walls in Rhus and straight walls in Schinus and
Lithraea.
Further anatomical and taxonomic studies were
needed to solve persisting problems regarding the
generic limits in this family. In particular the types
of the ovules and the number of teguments need to
studied in detail in the three genera. Based on the
findings of this study, it was concluded that L.
brasiliensis should not be included in the genus
Rhus, contrary to the suggestion of Piennar and
Von Teichman (1998).
ACKNOWLEDGEMENTS
This work was supported by of CAPES and
FAPESP.
609
RESUMO
O fruto de Lithraea molleoides (Vell.) Engl. é uma
drupa globosa, branca-acinzentada, lisa, com
exocarpo friável e lignificado quando maduro. O
mesocarpo é parenquimático com grandes canais
secretores associados aos feixes vasculares. O
endocarpo é composto de quatro camadas: na
camada mais externa as células são poliédricas,
com cristais prismáticos de oxalato de cálcio, e nas
três camadas internas as células são esclereides em
paliçada. O envoltório da semente é membranáceo,
liso, amarelo-pálido com uma mancha marrom
escura. O óvulo é anátropo, unitegumentado,
crassinucelado, inserido em posição basal-lateral.
O funículo é crasso e cresce em direção à
micrópila formando o obturador funicular. Na
região calazal uma zona com células
parenquimáticas de conteúdo tanífero formam a
hipóstase. A semente em desenvolvimento
apresenta uma forma circinótropa, originada a
partir da curvatura do funículo crasso e longo que
circunda o tegumento e o saco embrionário. A
semente madura é endotestal com as paredes das
células da endotesta espessadas e lignificadas em
forma de barras ou pontuações.
REFERENCES
Barkley, F. A. (1962), Anacardiaceae: Rhoideae:
Lithraea. Phytologia, 8, 329-365.
Brizicky, G. K. (1963), The genera of Sapindales in
the southeastern United States. J. Arnold Arbor., 44,
462-501.
Carmello-Guerreiro, S. M. and Paoli, A. A. S. (1999),
Morfologia e anatomia da semente de Schinus
terebinthifolius
Raddi,
(Anacardiaceae),
em
desenvolvimento. Revta.brasil. Bot., 22, 91-98.
Carmello-Guerreiro, S. M. and Paoli, A. A. S. (2002),
Ontogeny and structure of the pericarp of Schinus
terebinthifolius Raddi (Anacardiaceae). Braz. Arch.
Biol. Tech., 45, 73-79.
Copeland, H. F. (1959), The reproductive structures of
Schinus molle (Anacardiaceae). Madrõno, 15, 14-24.
Copeland, H. F. and Doyel, B. E. (1940), Some features
of the structure of Toxicodendron diversiloba. Am. J.
Bot., 27, 932-939.
Corner, E. J. H. (1976), The Seeds of Dicotyledons.
Cambridge : Cambridge University Press. 2 v.
Engler, A. (1876), Anacardiaceae. In: Martius, C. P. F.
and Eichler, A. G. Flora Brasiliensis. Lipsiae : J.
Cramer. v.12. part II. pp. 367-418.
Brazilian Archives of Biology and Technology
610
Carmello-Guerreiro, S. M. and Paoli, A. A. S.
Gerrits, P. O. (1991), The application of glycol
methacrylate in histotechnology; some fundamental
principles.
Department of Anatomy and
Embryology, State University of Groningen,
Netherlands.
Johansen, D. A. (1940), Plant Microtechnique. New
York : McGraw-Hill.
Kelkar, S. S. (1958), Embryology of Rhus mysurensis
Heyne. J. Indian Bot. Soc., 37, 114-122.
Li, X.; Baskin, J. M. and Baskin, C. C. (1999), Pericarp
ontogeny and anatomy in Rhus aromatica Ait. and
Rhus glabra L. (Anacardiaceae). J. Torrey Botan.
Soc., 126, 279-288.
MacNair, J. B. (1921), The morphology and anatomy of
Rhus diversiloba. Am. J. Bot. 8, 179-191.
O'Brien, T. P.; Feder, N. and McCully, M. E. (1964),
Polychromatic staining of plant cell walls by
toluidine blue O. Protoplasma, 59, 368-373.
Pienaar, M. E. and Von Teichman, I. (1998). The
generic position of Lithraea brasiliensis Marchand
(Anacardiaceae): evidence from fruit and seed
structure. Bot. J. Linn. Soc., 126, 327-337.
Radford, A. E.; Dickinson, W. C.; Massey, J. R. and
Bell, C. R. (1974), Vascular Plant Systematics. New
York : Harper and Row.
Roth, I. (1977), Fruits of Angiosperms. Berlin :
Gebrüder Borntraeger.
Sass, J. E. (1951), Botanical Microtechnique. 3rd ed.
Ames : State Press.
Soos, E. and Hausknost, M. (1951), Die Früchte von
Schinus molle L., dem Pfeffestrauch (Anacardiaceen).
Scientia Pharmaceutica, 19, 213-219.
Spjut, R. W. (1994), A systematic treatment of fruit
types. Mem. N. Y. Bot. Gard., 70, 1-82.
Terrazas, T. and Chase, M. W. (1996), A phylogenetic
análisis of Anacardiaceae based on morphology,
anatomy and rbcL sequence data. Am. J. Bot., 83, 6,
suppl. 197.
Von Teichman, I. (1989), Reinterpretation of the
pericarp of Rhus lancea (Anacardiaceae). S. Afr. J.
Bot., 55, 383-384.
Von Teichman, I. (1991), Ontogeny of the seed-coat of
Rhus lancea L. fil., and pachychalazy in the
Anacardiaceae. Bot. J. Linn. Soc., 107, 35-47.
Von Teichman, I. and Robbertse, P. J. (1986),
Development and structure of the pericarp and seed
of Rhus lancea L. fil. (Anacardiaceae), with
taxonomic notes. Bot. J. Linn. Soc., 93, 291-306.
Von Teichman, I. and Van Wyk, A. E. (1991),
Taxonomic position of Rhus problematodes
(Anacardiaceae): evidence from fruit and seed
structure. S. Afr. J. Bot., 57, 29-33.
Von Teichman, I. and Van Wyk, A. E. (1994),
Structural aspects and trends in the evolution of
recalcitrant seeds in dicotyledons. Seed Sci. Res. 4,
225-239.
Wannan, B. S. and Quinn, C. J. (1990), Pericarp
structure and generic affinities in the Anacardiaceae.
Bot. J. Linn. Soc., 103, 225-252.
Brazilian Archives of Biology and Technology
Received: August 25, 2003;
Revised: May 25, 2004;
Accepted: November 26, 2004.