Acta Botanica Brasilica - 31(3): 319-329. July-September 2017.
doi: 10.1590/0102-33062016abb0287
Pericarp ontogeny of Tapirira guianensis Aubl.
(Anacardiaceae) reveals a secretory endocarp in young
stage
Elisabeth Emilia Augusta Dantas Tölke1*, Ana Paula Stechhahn Lacchia2, Diego Demarco3 and Sandra Maria
Carmello-Guerreiro1
Received: August 9, 2016
Accepted: October 6, 2016
.
ABSTRACT
Most species of Anacardiaceae have drupes containing secretory structures.. The substances produced by these structures
may have importance to industry and folk medicine, and may even cause allergenic effects. This work describes the
ontogeny of pericarp of Tapirira guianensis with an emphasis on the secretory structures present at different stages of
development. Ovary and fruits in various stages of development were collected, fixed and processed for studies using
light and scanning electron microscopy according to conventional techniques. Histochemical tests were employed to
identify the major metabolites present in the tissues. The fruit is a drupe formed by exocarp, mesocarp containing
secretory ducts and idioblasts, and endocarp with some lignified layers. Fruit growth occurs through the division
and elongation of cells. The secretory ducts produce mainly phenols and lipids and are active during all stages of
development. The secreted substances protect the fruit against pathogens and predators. In ripe fruits the cells of
the mesocarp accumulate starch. This study is the first report of the presence of a secretory endocarp in young fruits
of a species of Anacardiaceae. The substances produced by the endocarp in early developmental stages may play an
important role in seed dispersal and germination.
Keywords: cashew family, drupe, fruit, mucilages, secretory ducts
Introduction
Most species of Anacardiaceae have drupaceous fruits
(Wannan & Quinn 1990; Gonzalez & Vesprini 2010).
Wannan & Quinn (1990) studied fruits belonging to 29
genera of Anacardiaceae and recognized two basic types
of endocarp: (1) the Spondias type - consisting of a mass
of sclerenchyma with irregular orientation and (2) the
Anacardium type - characterized by a lignified inner
epidermis and a layered arrangement, including sclereids
in palisade. The first type occurs in Spondioideae tribe and
the second type in Anacardioideae tribe (Wannan & Quinn
1990; Pell et al. 2011).
Secretory structures are quite common in fruits of
Anacardiaceae (Von-Teichman 1987; Wannan & Quinn 1990;
Carmello-Guerreiro & Paoli 2000; 2002; 2005; Machado &
Carmello-Guerreiro 2001; Lacchia & Carmello-Guerreiro
2009; González & Vesprini 2010). The most frequent
structures are the ducts and cavities, both of which may
Programa de Pós-Graduação em Biologia Vegetal, Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas,
13083-970, Campinas, SP, Brazil
2
Departamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Estadual da Paraíba, campus I, 58429-600, Campina Grande,
PB, Brazil
3
Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil
1
*
Corresponding author: elisabeth.tolke@gmail.com
Elisabeth Emilia Augusta Dantas Tölke, Ana Paula Stechhahn Lacchia,
Diego Demarco and Sandra Maria Carmello-Guerreiro
produce resin, gum or a mixture of substances (Venning
1948; Metcalfe & Chalk 1950; Lacchia & Carmello-Guerreiro
2009). According to Barroso et al. (2007), the mesocarp of
the representatives of this family can be fleshy (Mangifera
and Spondias) or spongy with ducts or cavities (e.g.,
Anacardium, Astronium and Myracrodruon). In the latter,
the secretory system is quite developed, and the ducts
or cavities occupy almost the entire mesocarp (CarmelloGuerreiro & Paoli 2000). The substances produced may
have importance in industry and folk medicine and can
even cause allergenic effects (Dong & Bass 1993; Barroso
et al. 2007; Pell et al. 2011).
Idioblasts (Carmello-Guerreiro & Paoli 2005), glandular
trichomes (Li et al.1999) and pericarpial nectaries may also
occur (Wunnachit et al. 1992; Rickson & Rickson 1998).
These nectaries are already present in flowers and are
maintained in the fruits, improving the viability and seed
dispersal. None of these structures are exclusive to secreting
fruits but basically occur in the whole plant (Lacchia &
Carmello-Guerreiro 2009; Lacchia et al. 2016a; 2016b).
Tapirira belongs to tribe Spondioideae of Anacardiaceae
(Pell et al. 2011). This genus includes about eight species of
trees occurring mainly in tropical areas of America (Wendt
& Mitchell 1995; Tropicos 2016). Tapirira guianensis is
widely distributed throughout Brazil and other countries
of South and Central America (Tropicos 2016), especially
in areas of moist soil (Santana et al. 2009). It is a dioecious,
important species for logging, medicinal use and may be
employed in the recovery of degraded areas and riparian
forests (Lorenzi 2002; Lenza & Oliveira 2005; Santana et
al. 2009). The drupes of this species are greatly appreciated
by birds (Corrêa 1978). Von-Teichman (1990) conducted
an anatomical study of the ripe fruit of this species, which
is classified as Spondias type. However, despite describing
them, the author does not emphasize the secretory
structures.
Therefore, this study aimed to examine the ontogeny
of the pericarp of Tapirira guianensis with an emphasis
on secretory structures present in different stages of
development. Through histochemical tests the secretion
produced by different structures, in different stages of
development, was characterized. We also describe the first
case of a secretory endocarp in Anacardiaceae.
Materials and methods
Plant material
Anthetic female flowers and fruits at various
developmental stages of Tapirira guinanensis Aubl. were
collected in three areas in the state of São Paulo, Brazil:
the Itirapina experimental station (22°13’S; 47°51’W), the
Mogi Guaçu experimental station (22°10’S; 47°07’W) and an
additional area of cerrado (Brazilian savannah) in the District
of Sousas, Campinas (22°51’S; 46°57’W). The Itirapina
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experimental station includes vegetation of Cerrado and
Campo Cerrado, while the Mogi Guaçu experimental station
comprises sensu lato Cerrado vegetation, according to the
classification of Ribeiro & Walter (1998). Collections were
made from March to December 2011 and from January
to February 2012. Vouchers are deposited in the UEC
herbarium (UEC 182229).
Light microscopy (LM)
For anatomical studies the samples were fixed in FAA
(formaldehyde, acetic acid, 50% ethanol) for 24 h (Johansen
1940). The material was then dehydrated in an ethanol
series and embedded in hydroxyethyl methacrylate resin
(Historesin® Leica), according to Gerrits & Smid (1983).
Transverse and longitudinal sections 8 μm thick were
obtained using a Microm HM340E rotary microtome
and stained with 0.05% Toluidine Blue in sodium acetate
buffer with a pH of 4.7 (O’Brien et al. 1964). All slides
were mounted with water and the images captured with
an Olympus DP71 digital camera coupled to an Olympus
BX51 microscope.
Histochemistry
For the histochemical tests, the material was fixed in
FAA (for hydrophilic substances) for 24 h (Johansen 1940)
and in BNF (buffered neutral formalin, for lipophilic and
phenolic substances) for 48 h (Lillie 1965). The material was
then also dehydrated in an ethanol series and embedded
in hydroxyethyl methacrylate resin (Gerrits & Smid 1983).
Transverse and longitudinal sections 8 μm thick were
obtained using a Microm HM340E rotary microtome. The
treatments performed can be found in Table 1. The results
were recorded using an Olympus DP71 digital camera
coupled to an Olympus BX51 microscope.
Scanning electron microscopy (SEM)
For micromorphological analysis, samples fixed in FAA
were dehydrated in an ethyl series, critical point dried, and
sputter coated with gold. Observations were carried out
using a Jeol JSM 5800 LV scanning electron microscope
at 10 kV equipped with a digital camera.
Stages of development
Based on the anatomical changes that occur during fruit
development, the results were grouped into four stages: (i)
ovary of the anthetic flower, (ii) very young fruit (3-5 mm
in length), (iii) immature fruit with verified elongation or
cell growth (5.1-8 mm in length) and (iv) ripe fruit (8.1-10
mm in length) (Fig. 1). The pericarp is divided into three
clearly differentiated parts in all phases of development:
exocarp, mesocarp and endocarp.
Acta Botanica Brasilica - 31(3): 319-329. July-September 2017
Pericarp ontogeny of Tapirira guianensis Aubl. (Anacardiaceae)
reveals a secretory endocarp in young stage
Results
Stage I
The outer epidermis of the ovary is uniseriate (Fig. 2AB), composed of juxtaposed cells coated with a thick cuticle
and containing stomata (Fig. 2B). The ovary is covered with
glandular and tector trichomes (Fig. 2C-F). The glandular
trichomes contain a bicellular, uniseriate stalk while the
secretory head is multicellular and multiseriate (3-4 rows)
(Fig. 2E). The non-glandular trichomes are elongated,
multicellular and uniseriate with tapered apex and thick
wall (Fig. 2F). The ordinary epidermal cells and secretory
trichomes accumulate phenolic substances (Fig. 2G, Tab.2).
Furthermore, the trichomes showed a positive reaction to
lipids and polysaccharides (Tab.2).
The ovarian mesophyll can be divided into three regions
based on the size and arrangement of the cells. The outermost
region underlying the external ovarian epidermis consists
of parenchyma cells in an intense process of cell division
(Fig.2A). This region consists of eight to ten layers of cells
with evident nuclei and thin walls (Fig. 2A-B). Druses are
distributed throughout this region (Fig.2A). The middle
portion contains vascular bundles and secretory ducts
(Fig.2A). The secretory ducts have a one layered epithelium
(Fig. 2H) which releases a secretion into the lumen formed
by droplets and a more fluid portion composed of lipids,
phenolic compounds and mucilage (Tab.2). The internal
region of the ovarian mesophyll consists of 12-15 cell layers
of parenchyma in an intensive process of division (Fig. 2A)
with evident nuclei and thin cell walls.
The inner epidermis of the ovary is uniseriate, formed
by juxtaposed cells with evident nuclei in central position
(Fig. 2I). These cells undergo periclinal divisions forming
a biseriate inner epidermis (Fig. 2I).
Stage II
At this stage the increase of pericarp layers primarily
occurs. The exocarp, derived from the ovarian outer
epidermis, is quite similar to the previous stage (Fig. 3A),
except that a significant loss of trichomes occurs.
The mesocarp develops from the fundamental ovarian
tissue and is divided into three zones: outer, median and
Table 1. Histochemical tests used in the characterization of the substances.
Test
Substance detected
Sudan black B (Pearse 1980)
lipids
Nile blue (Cain 1947)
acidic and neutral lipids
Lugol’s reagent (Johansen 1940)
starch
Ferric chloride (Johansen 1940)
phenolic compounds
Wagner’s reagent (Furr & Mahlberg 1981)
alkaloids
Schiff’s reagent (PAS) (McManus 1948)
carbohydrates
Ruthenium red (Gregory & Baas 1989)
acidic mucilages
Tannic acid and ferric chloride (Pizzolato & Lillie 1973)
mucilages
Copper acetate and rubeanic acid (Ganter & Jollés 1969; 1970)
fatty acids
Aniline blue black (Fisher 1968)
proteins
Stage I
Stage II
Stage III
Stage IV
Figure 1. Stages of development of Tapirira guianensis fruit under stereomicroscope. Stage I: ovary of the anthetic flower, Stage II:
very young fruit (3-5 mm in length), Stage III: immature fruit with verified elongation or cell growth (5.1-8 mm in length) and Stage
IV: ripe fruit (8.1-10 mm in length).
Acta Botanica Brasilica - 31(3): 319-329. July-September 2017
321
Elisabeth Emilia Augusta Dantas Tölke, Ana Paula Stechhahn Lacchia,
Diego Demarco and Sandra Maria Carmello-Guerreiro
Table 2. Histochemical tests in Tapirira guianensis fruits at different stages of development.
Test
Sudan black B
outer epidermis/
epicarp
glandular
trichomes
outer
mesocarp
median
mesocarp
inner mesocarp
(idioblasts)
endocarp
secretory ducts
-
+ (I, II)
-
-
-
+ (II)
+ (I, II, III, IV)
Nile blue
-
+ (I, II)
-
-
-
+ (II)
+ (I, II, III, IV)
Lugol’s reagent
-
-
+ (IV)
+ (IV)
-
-
-
Ferric chloride
+ (I, II, III, IV)
+ (I, II)
-
-
+ (II, III)
-
+ (I, II, III, IV)
-
-
-
-
-
-
-
Schiff’s reagent (PAS)
-
+ (I, II)
-
-
-
+ (II)
+ (I, II, III, IV)
Ruthenium red
-
-
-
-
-
-
+ (I, II, III, IV)
Wagner’s reagent
Tannic acid and ferric chloride
-
-
-
-
-
-
+ (I, II, III, IV)
Copper acetate and rubeanic acid
-
-
-
-
-
-
-
Aniline blue black
-
-
-
-
-
-
-
Notes: I (stage I), II (stage II), III (stage III), IV (stage IV), + (positive reaction), - (negative reaction).
inner mesocarp (Fig. 3A). In the outer mesocarp, there is an
increased number of layers, which comprise about 20 layers
of parenchyma cells, which are still in the process of cell
division in several planes. In median mesocarp the secretory
ducts are distributed. In this phase the secretory ducts are
delimited by a one layered epithelium surrounded by a sheath
(2-3 layers) (Fig. 3B). The secretion responded positively
to lipids, total polysaccharides, phenolic compounds and
mucilage (Fig. 3C-F) (Tab.2). The epithelial cells degenerate
adding to part of the secretion (Fig. 3G), while the sheath
cells undergo periclinal divisions renewing the epithelium.
In the inner mesocarp, idioblasts with phenolic content
appear (Fig. 3H) (Tab.2). This region presents cell divisions
in several levels.
The endocarp, derived from inner ovarian epidermis,
consists of two layers of secretory cells (4A-D). Under SEM,
several drops of secretion were observed in the endocarp
(Fig. 4E), which were also observed on the developing seed
coat (Fig. 4F). The endocarp secretion responded positively
to lipids, mucilages and polysaccharides tests (Fig. 4A-D)
(Tab.2).
crystals (Fig. 5C). In the endocarp, the layer adjacent to the
inner mesocarp differs in elongated sclereids with the last
layer, in contact with the locule, remaining non-lignified (Fig.
5C). In this phase, the endocarp is not secretory; however,
secretions produced in the previous stage remain covering
the entire endocarp and seed coat.
Stage III
The fruit of T. guianensis is classified as a drupe since
the exocarp and mesocarp are fleshy and, the endocarp is
formed by several layers of sclerified cells (Von-Teichman
1990). In drupes, the exocarp acts as a protective outer
layer, the mesocarp is usually parenchymal and endocarp
is hard, with layers that protect the seed (Roth 1977; Spjut
1994). According to Roth (1977), the exocarp and the
endocarp may be formed by a single layer derived from the
outer and the inner ovarian epidermis, respectively. In this
case, they are called sensu stricto exocarp or endocarp. When
they also include derived mesocarp layers, they are called
sensu lato exocarp or endocarp. The exocarp of T. guianensis is
formed by the outer layer, derived from the outer epidermis
of the ovary, and by several layers of collenchymatous cells
formed from the outer mesocarp. Therefore, in this species
the exocarp is known as sensu lato, according to Roth (1977).
At this stage, all trichomes of the exocarp are lost.
The cells of the outer mesocarp present pectic-cellulosic
thickening becoming collenchymatous (Fig. 5A-B), the
thickest being close to the exocarp (Fig. 5B). The median
mesocarp increases the parenchyma cell layers between
the secretory ducts and the vascular bundles, now welldeveloped (Fig. 5A). In the inner mesocarp, the most
striking differences arise. Intercellular spaces become quite
conspicuous among the parenchyma cells (Fig. 5C). In the
last 3-4 layers, the vast majority of internal mesocarp cells
differentiates, forming elongated sclereids in longitudinal,
transverse and oblique directions (Fig. 5C). The cells that
do not lignify remain parenchymatic with many containing
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Stage IV
The most evident change in the ripe fruit exocarp is the
appearance of lenticels (Fig. 6A). The external and median
mesocarp cells accumulate starch (Fig. 6B-C) (Tab.2).
Parenchyma cells in the median mesocarp layers divide
and stretch in several directions (Fig. 6D). In the inner
mesocarp, some of the idioblasts that accumulated phenolic
compounds are now differentiated in sclereids (Fig. 6E). In
the endocarp, the layer in contact with the locule (which
was secretory) now also lignifies, forming sclereids (Fig. 6F).
Discussion
Acta Botanica Brasilica - 31(3): 319-329. July-September 2017
Pericarp ontogeny of Tapirira guianensis Aubl. (Anacardiaceae)
reveals a secretory endocarp in young stage
Figure 2. Structural and histochemical aspects of Tapirira guianensis ovary. (A) General aspect of the ovary in longitudinal-section.
Note the cells in intense process of division (arrows). (B) Outer epidermis of the ovary in cross-section. (C-D) Electron micrographs
of trichomes in the outer epidermis. (E) Glandular trichome in longitudinal section. Note the bicellular and uniseriate stalk and the
multicellular and multiseriate secretory head (F) Elongated, multicellular and uniseriate non-glandular trichome in longitudinal section.
(G) Outer epidermis showing positive reaction to ferric chloride. (H) Fundamental tissue in cross-section showing the secretory ducts
and vascular bundles still in development. The secretory ducts have an epithelium which releases a secretion into the lumen. (I) Inner
epidermis in cross-section showing the periclinal divisions (arrows). Abbreviations: ct, cuticle; dr, druse; ep, epithelium; ft, fundamental
tissue; ie, inner epidermis; lu, lumen; oe, outer epidermis; sd, secretory duct; st, stomata; vb, vascular bundle.
Acta Botanica Brasilica - 31(3): 319-329. July-September 2017
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Elisabeth Emilia Augusta Dantas Tölke, Ana Paula Stechhahn Lacchia,
Diego Demarco and Sandra Maria Carmello-Guerreiro
Figure 3. Structural and histochemical aspects of Tapirira guianensis pericarp in Stage II. (A) General aspect of the pericarp in crosssection. (B) Detail of the secretory ducts with uniseriate epithelium and multiseriate sheath. (C) Secretory duct showing positive reaction
to Schiff reagent. (D) Secretory duct showing positive reaction to Sudan black B. (E) Secretory duct showing positive reaction to ferric
chloride. (F) Secretory duct showing positive reaction to Nile blue sulphate. (G) Detail of the epithelium. Note the degeneration of cells,
eliminated together with the secretion, while the sheath cells undergo periclinal divisions renewing this epithelium. (H) Idioblasts
showing a positive reaction to ferric chloride Abbreviations: dr, druse; ec, exocarp; en, endocarp; ep, epithelium; id, idioblast; im,
inner mesocarp; mm, median mesocarp; om, outer mesocarp; vb, vascular bundle.
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Acta Botanica Brasilica - 31(3): 319-329. July-September 2017
Pericarp ontogeny of Tapirira guianensis Aubl. (Anacardiaceae)
reveals a secretory endocarp in young stage
Figure 4. Histochemical and SEM of the endocarp in Stage II. (A) Endocarp and idioblasts in Toluidine blue coloration. Note the
secretion droplets (*). (B) Endocarp and idioblasts showing positive reaction to Schiff reagent. (C) Endocarp showing positive reaction
to tannic acid and ferric chloride. (D) Endocarp and idioblasts showing positive reaction to Nile blue sulphate. Note the secretion
droplets (*). (E) Electron micrograph of secretion droplets (arrow) in endocarp. (F) Electron micrograph of secretion droplets (arrow)
in funicle. Abbreviations: en, endocarp; id, idioblast
Von-Teichman (1990), despite having studied just the ripe
fruit, also considers the exocarp of this species as sensu lato.
In this case the external mesocarp is considered part of
the exocarp due to their functional aspect (Roth 1977). In
general, the exocarp of the Spondioideae representatives,
a tribe belonging to T. guianensis, consists of small, thin
walled, tightly packed parenchyma cells, which may
develop thick cellulosic walls (Wannan & Quinn 1990). In
Anacardioideae, the exocarp may be sclerified, e.g., Lithraea
molleoides (Carmello-Guerreiro & Paoli 2005) and Schinus
terebinthifolius (Carmello-Guerreiro & Paoli 2002). The
ovarian epidermis and developing fruit are covered by
tector and glandular trichomes. This characteristic was
not observed by Von-Teichman (1990) since he studied
only the ripe fruits. The trichomes play an important role
in mechanical protection of the fruit in development, and
also act in protection against ultraviolet radiation (Roth
1977). This protection is enhanced by phenolic compounds
produced by the epidermis and the glandular trichomes
(Castro & Demarco 2008), these substances assist in
protection against herbivory (Fahn 1979; Calvo et al. 2010)
and against the microorganism proliferation (Calvo et al.
2010).
Secretory ducts are widely distributed in the median
region of the mesocarp. They play an important role
during all phases since they remain active during
Acta Botanica Brasilica - 31(3): 319-329. July-September 2017
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Elisabeth Emilia Augusta Dantas Tölke, Ana Paula Stechhahn Lacchia,
Diego Demarco and Sandra Maria Carmello-Guerreiro
Figure 5. Structural aspects of Tapirira guianensis pericarp in Stage III. (A) General aspect of the pericarp in cross-section. (B) Exocarp
and outer mesocarp in cross-section. Note the pectic-cellulosic thickening and druses. (C) Detail of inner mesocarp and endocarp. Note
intercellular spaces (*) and the formation of sclereids. The layer in contact with the locule, remaining non-lignified. Abbreviations: cr,
crystal; ct, cuticle; dr, druse; ec, exocarp; en, endocarp; id, idioblast; im, inner mesocarp; mm, median mesocarp; om, outer mesocarp;
pc, pectic-cellulosic thickening; sc, sclereid; st, stomata; vb, vascular bundle.
the whole fruit development. They produce the same
substances independent of the phase in which the fruit
is. In Anacardiaceae several studies have mentioned the
presence of resiniferous ducts in fruits, always associated
with vascular bundles (Von-Teichman 1987; 1990; Wannan
& Quinn 1990; Von-Teichman & Van-Wyk 1993; 1994;
1996; Carmello-Guerreiro & Paoli 2000; 2005; Machado
& Carmello-Guerreiro 2001; González & Vesprini 2010).
This is a constant feature for the family, regardless of the
tribe to which the species belong.
Lacchia & Carmello-Guerreiro (2009) closely studied the
formation of these ducts in T. guianensis fruit, as well as
the secretory mechanism. The authors concluded that the
formation of the ducts is schizogenous and the secretory
mechanism is eccrine. These ducts have a mixed secretion,
containing lipids, polysaccharides and phenolic substances.
It is possible to verify the disruption of the epithelium cells
and consequently extravasation of the secretion into the
326
lumen with cell debris with continuous replacement of
the epithelium by the meristematic activity of the sheath,
which characterizes the mode of secretion as holocrine.
The occurrence of a parenchymatous sheath surrounding
secretory ducts producing new epithelium cells has been
reported in several studies (Monteiro et al. 1995; 1999;
Machado & Carmello-Guerreiro 2001; Bennici & Tani 2004;
Rodrigues et al. 2011a; 2011b).
The large amount of phenolic substances found in T.
guianensis fruit, stored in ducts, exocarp and idioblasts,
is also found in other species of the family, referred to as
tanniferous substances (Von-Teichman 1987; Von-Teichman
& Van-Wyk 1993; 1994; 1996; Piennar & Von-Teichman
1998; González & Vesprini 2010). Von-Teichman (1990)
also report these substances in ducts and idioblasts of
T. guianesis fruits. However, it does not perform tests to
confirm the chemical nature of these substances. There
are several functions of the phenolic substances, among
Acta Botanica Brasilica - 31(3): 319-329. July-September 2017
Pericarp ontogeny of Tapirira guianensis Aubl. (Anacardiaceae)
reveals a secretory endocarp in young stage
Figure 6. Structural and histochemical aspects of Tapirira guianensis pericarp in Stage IV. (A) Lenticel formation in cross-section. (B)
Outer mesocarp showing positive reaction to Lugol. (C) Median mesocarp showing positive reaction to Lugol. (D) General aspect of
the fruit in cross-section. (E) Detail of inner mesocarp and endocarp. Note intercellular spaces (*) and the fact that some of the cells
that accumulated phenolic compounds now are differentiated sclereids (arrows). (F) Endocarp. Note that the layer in contact with
the locule now also lignifies. Abbreviations: ec, exocarp; el, elongated cell; en, endocarp; im, inner mesocarp; mm, median mesocarp;
om, outer mesocarp; sc, sclereid; vb, vascular bundle.
Acta Botanica Brasilica - 31(3): 319-329. July-September 2017
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Elisabeth Emilia Augusta Dantas Tölke, Ana Paula Stechhahn Lacchia,
Diego Demarco and Sandra Maria Carmello-Guerreiro
them chemical defense against pathogens, herbivory and
ultraviolet radiation (due to its antioxidant power) and
an aid in the dispersal by birds (inducing regurgitation)
(Roshchina & Roshchina 1993; Von-Teichman & VanWyk 1993; 1994; Aguilar-Ortigoza & Sosa 2004; Castro
& Demarco 2008).
Another important feature in mesocarp is the elongation
of cells located between the secretory ducts and the vascular
bundles. These elongated cells were also observed by VonTeichman (1990). The cell divisions that occur in this region
are responsible for the separation that occur between
the vascular bundles and the ducts. In young stages we
observe the secretory ducts and the vascular bundles very
close. Furthermore, these cells are the main site of starch
accumulation in the last stage of development, an energetic
substance demanded by dispersers (Roth 1977).
According to the organization of the endocarp, Wannan
& Quinn (1990) proposed a classification of two kinds
of pericarp for Anacardiaceae: (1) the Spondias type
with endocarp comprising a mass of sclerenchyma with
irregular orientation and (2) the Anacardium type with
endocarp in layers, comprising a lignified outer epidermis
and parenchyma arranged in layers, including sclereids
in palisade. Thus, the characteristics of the T. guianensis
endocarp fall under the Spondias type. Von-Teichman (1990)
studied the structure of the ripe fruit of T. guianensis and
found that the endocarp is not massive, but relatively
thin in comparison to another species of the same tribe,
i.e., Lannea discolor Engl. (Von-Teichman 1987). We not
report the presence of operculum, which agrees with the
observations of Von-Teichman (1990). Moreover, the T.
guianensis endocarp is considered sensu lato since the fully
developed fruit includes the sclerified layers derived from the
inner mesocarp. A novel aspect observed in T. guianensis is
the presence of a secretory endocarp in unripe fruits. The
production of hydrophilic mucilages by the endocarp may
facilitate seed hydration (Western 2012). In cases in which
the mucilage covers the seed, such as in Euphorbia species,
the mucilage may mediate germination under waterlogged
conditions, prevent seed predation by adherence to soil
and promote seed dispersal by attachment to animals
(Demarco & Carmello-Guerreiro 2011; Western 2012). These
mucilages are acids or neutral complex polysaccharides of
high molecular weight (Fahn 1979) that undergo substantive
swelling upon hydration (Western 2012). The production
of lipids may be an important chemical defensive against
fungi and other microorganisms (Fahn 1979). As described
for Heeria angentea (Von-Teichman & Wan-Wyk 1996), in
T. guianensis the parenchymatous cells of the endocarp is
replaced by a sclerenchymatous endocarp at the last stage of
fruit development. According to Von-Teichman (1990), the
endocarp hardening can be related to the seed protection for
seeds lacking a mechanical protective layer. The secretory
endocarp is naturally replaced by a sclerenchymatous
endocarp, once the seed has not a mechanical protective
layer (Von-Teichman 1990).
328
Conclusions
The results described herein suggest that fruits of
T. guianensis have several characteristics related to fruit
protection against pathogens and predators due to the
presence of ducts secreting gum-resin, idioblasts containing
phenolic substances and druses widely distributed in the
mesocarp. The substances produced by the endocarp in
young stages may play an important role in seed dispersal
and germination. The presence of a secretory endocarp is
first reported in the family.
Acknowledgements
We thank CNPQ (National Council for Scientific and
Technological Development) for the master’s scholarship
granted to Elisabeth E. A. Dantas Tölke during the first few
months of the development of this work and FAPESP (São
Paulo Research Foundation) for the master’s scholarship
and technical reserve (Process 2011/02293-0). We also
thank the FAPESP for their additional financial support
(FAPESP 01/12178-1, 03/13556-5, 14/18002-2, Biota/
FAPESP 96/12345-5, 00/12469-3).
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