CAMBIAL VARIANT IN THE STEM OF SERJANIA CORRUGATA (SAPINDACEAE) - Brill
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IAWA Journal, Vol. 27 (3), 2006: 269–280
CAMBIAL VARIANT IN THE STEM OF SERJANIA CORRUGATA
(SAPINDACEAE)
Gabriel U.C. Araújo and Cecilia G. Costa
Laboratório de Botânica Estrutural, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro,
Rua Pacheco Leão, 915, CEP 22460-030, Rio de Janeiro, RJ, Brazil
[E-mail: guc_araujo@yahoo.com.br]
SUMMARY
The establishment of the cambial variant and the development of the stem
of Serjania corrugata Radlk. (Sapindaceae) was analyzed. In the early
stages of development, the stem is lobed, with five lobes and five furrows
in cross section. Around the fourth internode, each lobe has a vascular arc
with one or two more developed central vascular bundles, two lateral bun-
dles and phloem in the interfascicular regions. Procambial strands are
also found in perimedullary position, producing only phloem elements.
At this stage, the beginning of the cambial activity can be seen in the cen-
tral vascular bundle in each lobe. This activity then extends to the lateral
vascular bundles and to the perimedullary phloem. Parenchymatic cells,
located between the vascular ring of the lobe and the perimedullary
phloem, dedifferentiate and initiate meristematic activity, uniting these
two regions. The development of xylem masses (one in each lobe) that
characterizes the adult stem results from this cambial activity. The devel-
opment of the cambial variant in S. corrugata is quite similar to that pre-
viously described in S. elegans Cambess.
Key words: Sapindaceae, Serjania, lianas, cambial variants, anomalous
secondary growth, divided xylem mass, development.
INTRODUCTION
Although lianas (woody climbers) are very common in tropical forests, anatomical
studies regarding them have been few (Bamber & Ter Welle 1994), and relatively little
attention has been paid to the cellular composition of the xylem in scandent plants as
well (Carlquist 1985). Lianas are an important source of studies regarding cambial
variants (also called anomalous secondary growth), since these occur less frequently
in self-supporting woody plants (Obaton 1960; Carlquist 1991). The different types of
cambial variants may have taxonomic and systematic importance (Obaton 1960; Met-
calfe 1983).
The diversity of cambial variants in Sapindaceae was initially described by Radlkofer
(1875, 1892, 1896) and Schenck (1893). Recently, Klaassen (1999) surveyed the wood
anatomy of Sapindaceae, including lianoid genera like Serjania and others. Around
226 species belong to the genus Serjania, and cambial variants occur in many of them
(Acevedo-Rodríguez 1993). Some types of cambial variants found in Sapindaceae, such
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as the divided xylem mass, are unique to Serjania (Metcalfe & Chalk 1950; Metcalfe
1983; Acevedo-Rodríguez 1991, 1993). The divided xylem mass is characterized by
five to seven radially disposed xylem masses that at maturity form separate cylinders
(Radlkofer 1892; Schenck 1893; Metcalfe 1983) and, up to the present day, has been
found only in the “S. paradoxa group”, composed by eight species of Serjania, including
S. corrugata Radlk. (Acevedo-Rodríguez & Somner 2001). Schenck (1893) described
the development of the divided xylem mass in the stem of S. elegans Cambess., and
Carlquist (2001) proposed a model for the development of this cambial variant in the
stem of S. corrugata. Our study clarifies how this variant develops, and shows some
differences from the speculative model of Carlquist (2001).
Most of the information about cambial variants is based on the mature structure,
and only a few developmental studies have been made (Nair 1993). The development
of the stem of S. corrugata is here reported, and the events leading to the formation of
the divided xylem mass are described and compared to literature data.
MATERIALS AND METHODS
Six specimens of S. corrugata were collected in two Atlantic rainforest areas – Tijuca
Forest and Morro das Andorinhas – located, respectively, in Rio de Janeiro city and
Niterói, RJ, Brazil. The vouchers are deposited at the herbarium of Jardim Botânico do
Rio de Janeiro (RB; accessions RB 402689, RB 402690, RB 402691 and RB 402692).
Samples from the internodes of the stems were fixed with FAA 50% and stored in 70%
aqueous ethanol (Johansen 1940). After dehydration with ethyl alcohol, the samples
from the young stems were embedded either in historesin, sectioned at 4 μm and
stained with toluidine blue 0.05% (Sakai 1973 cited in Kraus & Arduin 1997), or were
embedded in paraffin, sectioned at 10 μm and stained with astra blue-fuchsin (Roeser
1972, modified by Luque et al. 1997). Samples of the adult stem, some of which in-
cluded in polyethylenglicol (Gerlach 1984), were sectioned in transverse, radial and
tangential longitudinal planes with a sliding microtome, at a thickness of 14–18 μm,
and stained in astra blue-safranin (Bukatsck 1972, modified by Kraus & Arduin 1999).
Sections from fresh samples were stained with ferric chloride (Gahan 1984), Fehllingʼs
reagent (McLean & Cook 1958) iodine, barium hydroxide and potassium bichromate or
Sudan IV (Johansen 1940) in order to detect, respectively, phenolic substances, sugars,
starch, saponins and cutin. Polarization microscopy was used to identify crystals of
calcium oxalate, and fluorescence microscopy was used to identify lignin, using the
autofluorescence of the lignin under UV light.
RESULTS
Early stages of development and primary structure
Sequential transverse sections of the shoot apex reveal that the apical meristem
initially has a circular outline, and as the shoot develops, the progressive rise of lobes
in the stem surface can be seen. In the first internode below the shoot apex, the stem
presents five lobes, delimited by five well-defined furrows (Fig. 1). These furrows are
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Fig. 1–3. Transverse sections. – 1: First internode, showing five lobes and five deep furrows. –
2 & 3: Third internode. – 2: Detail of a lobe, showing lateral procambial groups (LP), a central
procambial group (CP) and the core of parenchyma cells (CO). – 3: Secretory cells (SC) in the
cortex; endodermis (EN); pericycle (PE). — Scale bar for 1 & 2 = 100 μm; for 3 = 50 μm.
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progressively attenuated throughout the development of the stem, so the adult stem
becomes slightly lobed or approximately cylindrical (Fig. 23). Developing glandular
trichomes are present (Fig. 1). Small groups of procambium occur in each lobe (Fig. 2).
The procambial activity is initiated in one or two central procambial groups, differ-
entiating protophloem at first, and then protoxylem. Then the two lateral procambial
groups, closer to the pith, also differentiate protophloem and protoxylem, while
the other procambial groups differentiate only protophloem. The core of each lobe
(Fig. 2) is connected to the pith and consists of parenchyma cells that store phenolic
substances.
In the third internode, the epidermal cells remain in active differentiation in the
regions of the furrows. Glandular trichomes are capitate, with uniseriate stalks. The
cortex has 2–4 layers of cells in the regions of the furrows and approximately 10 in the
lobes. Phenolic substances occur in the cortical cells and among these differentiating
secretory cells occur (Fig. 3). The secretory cells are bigger than the other cortical cells
and produce saponins. The inner cortical layer, the endodermis, is distinguished by
slightly bigger cells (Fig. 3) containing starch. No Casparian strips were observed in
these cells. The endodermis delimitates externally the pericycle, which has seven to
ten layers of cells (Fig. 3) and is delimited internally by a layer of primary phloem
cells with phenolic content.
In the fourth internode, unicellular non-glandular trichomes also occur in the epi-
dermis. Each lobe has its own vascular arch, with one or two central vascular bundles
and two lateral vascular bundles. In the interfascicular regions, only phloem elements
occur (Fig. 4). The vascular differentiation does not occur equally in each lobe, so dif-
ferences occur in the number of vascular bundles and in the stage of differentiation of
the vascular elements in each lobe. Procambium strands occur in perimedullary posi-
tion, producing only primary phloem (Fig. 6–7).
Establishment of cambial activity
Cambial activity begins in the central vascular bundles of the lobes (Fig. 5) and can
be observed from the fourth internode onwards. Between the fourth and the sixth
internode, the cambial activity is extended to the rest of the vascular arc of each lobe
(Fig. 10) and, last, to the perimedullary phloem. The epidermal cells are dome-shaped
(Fig. 8), and the stomata are located in a level slightly above them and have a small
substomatal chamber (Fig. 9). Only unicellular non-glandular trichomes occur in
the epidermis and their walls show signs of lignification (Fig. 11). In the cortex,
some layers differentiate into annular collenchyma. The pericycle becomes lignified
(Fig. 9), first in the regions of the furrows, and then also in the lobes (Fig. 11). In the
plants analyzed, the parenchyma cells that form the core of the lobes do not become
lignified, even in the oldest parts of the stem.
In the seventh internode, parenchyma cells of pericyclic origin, located between the
perimedullary phloem and the vascular arc of each lobe, dedifferentiate and initiate
meristematic activity, uniting the cambia of the two regions (Fig. 12 & 13). This aspect
can be better observed in later stages of the development (Fig. 14).
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Fig. 4 –9. Transverse sections. – 4 –7: Fourth internode; 8 & 9: Fifth internode. – 4: Vascular arc
of a lobe, with three vascular bundles (circles), one central and two lateral, and phloem (PH) in
the interfascicular regions. – 5: Detail of the central vascular bundle. Beginning of the cambial
activity (C), producing new vessel elements (NVE). ID = idioblasts in the primary phloem,
containing phenolic substances. – 6: Primary phloem (circle) in perimedullary position, close to
the pith (P). – 7: Detail of Fig. 6. – 8: Domed epidermal cells (arrow); secretory cell (SC) in the
cortex. – 9: Stoma (arrow) with a small substomatal chamber, endodermis (EN) and pericyclic
cells (PE) with lignified walls. — Scale bar for 4 & 6 = 50 μm; for 5, 7–9 = 25 μm.
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Formation of the xylem masses
From the seventh to the twelfth internode, cambial activity is fully established, con-
solidating the secondary structure of the stem. The epidermis and cortex are as described
above. In the pericycle, the complete differentiation of the fibers can be noted, forming
a continuous sclerenchyma ring (Fig. 15). In the lobes, the beginning of the formation
of the xylem masses can be seen. Initially, more parenchyma cells than vessel elements
and fibers are produced. The vessel elements initially formed have smaller diameters
than those formed later (Fig. 15 & 17). In the region of the furrows, the cambium is
unidirectional, producing only externally a small amount of phloem. Parenchyma cells of
pericyclic origin fill up the region between the small xylem masses (Fig. 17). Periclinal
divisions of these cells expand this tissue radially, so in later stages the furrows become
less distinct (Fig. 23).
In the twelfth internode, the cambium almost completely circles the xylem of the
lobes, except in the regions that connect the core of the lobes with the pith (Fig. 16).
These connections may persist in old stems. As a consequence of the production of
vascular tissues, the cells of these connections show intense cellular division, in order
to remain connected with the pith of the xylem masses.
In two of the samples analyzed, a fragmentation of the cambium, in the region of
the furrows, was observed. This fragmentation results in one or more separated circular
cambial strands that circle a small amount of phloem (Fig. 18). However, no continuity
to these strands was found in subsequent internodes. Starch is abundantly present in
most of the cells of the core of the lobes and in the parenchyma cells of the secondary
xylem. Some cells of the pith also store starch, but in smaller quantities.
Rupture of the sclerenchyma ring
At this stage, the xylem masses are well-developed, each with its own pith (Fig. 20).
The epidermis, the cortex and the pericycle undergo structural changes, as a conse-
quence of the production of the vascular tissues. The epidermis is still present, although
interrupted at some points by lenticels, originating by a phellogen that arises in the
cortical layers below the stomata (Fig. 19). The sclerenchyma ring breaks at some points,
since these cells are not capable of dividing, and these points are filled with cortical
parenchyma cells (Fig. 20). These cells may become sclerified (Fig. 21). Prismatic crys-
tals of calcium oxalate, isolated or juxtaposed, occur in the parenchyma of the cortex,
pith, xylem and phloem.
Each xylem mass is almost completely surrounded by its own cambium. In certain
regions of each cambium, large parenchyma rays are formed. When these rays occur
close to the connection between the pith of the xylem masses and the central pith, the
xylem masses become separated, generating smaller xylem masses (Fig. 22).
Starch is abundantly present in the axial parenchyma cells of the secondary xylem.
→
Fig. 10–15. Transverse sections. – 10 & 11: Fifth internode; 12 & 13: Seventh internode; 14 &
15: Tenth internode. –10: Cambium (C) in a lateral vascular bundle. PH = phloem; VE = vessel
elements. – 11: Fluorescence microscopy, showing that the lignification of the pericycle occurs
more intensely in the regions of the furrows (FU) than in the region of the lobes (LO). The non-
glandular trichomes also show signs of lignification (TR). – 12 & 13: Parenchyma cells between
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the cambium of the lobe (COL) and the cambium of the perimedullary phloem (COP) show
meristematic activity, uniting these two cambia and resulting in a single cambium (C). PMP =
perimedullary phloem. – 14: Same region as shown in Fig. 12 & 13, where the consolidation of
cambium (C) can be observed. – 15: Detail of a lobe, showing the pericyclic sclerenchyma ring
(PE), and the difference between the diameter of first-formed (FV) and later-formed (LV) vessel
elements. — Scale bar for 10, 12–14 = 25 μm; for 11 & 15 = 100 μm.
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Fig. 16–21. Transverse sections. – 16–17: Twelfth internode. – 16: Persistence of the connection
(CON) between the pith (P) and the core of a lobe. C = cambial strand. – 17: Parenchyma tis-
sue (PA) of pericyclic origin between the recently formed xylem masses (XM). The difference
between the diameter of the first-formed (FV) and later-formed vessel elements (LV) can be
noted. – 18: Sixteenth internode. Separate cambial strand, enveloping phloem tissue. – 19: Ori-
gin of a phellogen (PHE) below a stoma (ST). – 20: Rupture of the sclerenchyma ring at some
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Establishment of the periderm
At this last stage of development, the five xylem masses are fully developed, each sur-
rounded completely or almost completely by secondary phloem and cambium, forming
five vascular cylinders. The intermediate zones between the xylem masses are composed
Fig. 22–24. Transverse sections. – 22: Small xylem mass formed between the wide parenchyma
ray (WPR) and the connection (CON) between the pith of the xylem mass (PXM) and the pith. –
23: Adult stem of Serjania corrugata, with five xylem masses (XYL) and the intermediate
zones (IZ) composed of phloem and parenchyma of pericyclic origin. Note the attenuated fur-
rows (*). – 24: Wavy periderm (PE) caused by extension of the phellogen activity to cellular
layers below the primary sclerenchyma ring (PE). — Scale bar for 22 = 200 μm; for 23 = 2 mm;
for 24 = 100 μm.
←
points (RU), due to expansion of the vascular tissues. These points are filled with cortical parenchy-
ma cells. XYL = xylem mass; PXM = pith of the xylem mass. – 21: Sclerification of parenchyma
cells in the points of rupture (SC). PE = pericyclic fibers. — Scale bar for 16, 17 & 20 = 200 μm;
for 18 & 19 = 25 μm; for 21 = 150 μm.
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of cambia, secondary phloem and wide parenchyma rays. The shape of the stem in trans-
verse section is slightly lobed, or almost cylindrical, since the vascular activity resulted
in the attenuation of the furrows (Fig. 23).
Fragments of the primary sclerenchyma ring may still be present adjoining the cor-
tex (Fig. 24). The lenticels occur in greater proportion, and the periderm is well estab-
lished, developing from a subepidermal phellogen. At some points, more deep-seated
phellogens arise that link up with the subepidermal phellogen, resulting in a locally
wavy periderm (Fig. 24). Sclerenchyma is formed below the primary (pericyclic) scler-
enchyma ring, in the secondary phloem, and in the parenchyma that separate the xylem
masses.
Starch is abundantly present in axial and radial parenchyma cells of the secondary
xylem.
DISCUSSION
The storage of starch in the stem of Serjania corrugata is remarkable, as it is present
abundantly in different stages of development. According to Mooney and Gartner
(1991), the main feature of the vining habit is the potential for rapid growth, since these
plants may allocate the carbon that would be used in structural molecules to storage sub-
stances, such as starch. According to Carlquist (1985, 1991, 2001) and Mooney and
Gartner (1991), starch could be used to obtain energy for growth fluxes and repair of
injured tissues. Also, some authors suggest that starch may be hydrolyzed into sugar
that, if carried into the vessels, increases the osmotic pressure, pulling water into them;
this mechanism might be used to recover embolised vessels (Carlquist 1985, 2001,
Mooney & Gartner 1991).
Schenck (1893) and Haberlandt (1928) suggested that the “anomalous” disposition
of secondary tissues (cambial variants) might increase the flexibility of the stem, aug-
menting its resistance to mechanical damage caused by twisting. Biomechanical ex-
periments conducted by Putz and Holbrook (1991), comparing stems of Puerto Rican
tree saplings and lianas, showed that the latter are more flexible and tougher (withstand
larger deformations without losing function), and, according to the authors, these prop-
erties appear to be closely related to the internal structure. The cambial variant found
in the stem of S. corrugata is characterized by compartimentalized xylem separated
by soft tissues (wide parenchyma rays and secondary phloem), resulting in a cable-like
structure that, according to Obaton (1960) and Putz and Holbrook (1991), increases stem
flexibility. According to Schenck (1893), all different types of cambial variants found
among the Sapindaceae result in this cable-like structure. The divided xylem mass may
also contribute to recovering from injuries, since cambial variants allow the stem to be
longitudinally segmented instead of transversally broken (Fisher & Ewers 1991).
The results observed in the present study show differences from the theoretical model
proposed by Carlquist (2001). According to this model, in younger stages of devel-
opment of the stem of S. corrugata, the stem itself and the pith are round in cross
section; also, the vascular system forms a complete ring. In our study the stem is lobed
in the early stages of development, which supports Schenckʼs (1893) observation that
the lobed stem is an early stage in the development of the divided xylem mass. The
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pith has projections that extend into the lobes (the core of the lobes) and each lobe has
its own vascular arch, disconnected from each other.
The development of the divided xylem mass in the stem of S. corrugata is very similar
to the development of the same cambial variant in the stem of S. elegans, except that
in the latter fibers are formed in the pith of older stems. According to Schenck (1893),
the formation of these fibers in the pith occurs only in S. elegans. The formation of
fibers below the pericyclic fibers and in the tissue between the xylem masses present
in S. corrugata was observed by Radlkofer (cited by Schenck 1893) in other species.
ACKNOWLEDGEMENTS
The authors would like to express their appreciation to the National School of Tropical Botany (ENBT),
the Atlantic Rainforest Program (PMA), CNPq, CAPES and Fundação Botânica Margaret Mee
for grants and sponsoring. We also thank Dr. P. Baas, Dr. J.B. Fisher, Dr. C.H. Callado, Dr. C.F. Barros,
Dr. G.V. Somner, Dr. K. De Toni, C.W. Oliveira, N. Tamaio, J. Benchimol, A. Penha, E. Zózimo,
P. Dias and R. Figueiredo for their valuable contributions to the improvement of this study.
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