979
Vol.50, n. 6 : pp.979-988, November 2007
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 Underground System in Vernonia
grandiflora Less. and V. brevifolia Less. (Asteraceae)
Adriana Hissae Hayashi1 and Beatriz Appezzato-da-Glória2*
1
Seção de Anatomia e Morfologia; Instituto de Botânica; SP; C. P. 3005; 01061-970; São Paulo - SP - Brasil.
Departamento de Ciências Biológicas; Escola Superior de Agricultura “Luiz de Queiroz”; Universidade de São
Paulo; bagloria@esalq.usp.br; C. P. 9; 13418-900; Piracicaba - SP - Brasil
2
ABSTRACT
This work dealt with the anatomy of the underground system in Vernonia grandiflora Less. and V. brevifolia Less.
(Vernonieae; Asteraceae), two perennial geophytes, to elucidate their ability to sprout in the Brazilian Cerrado
conditions. V. grandiflora, a subshrubby species, possessed a thickened underground system constituted by a
xylopodium and many tuberous roots. The xylopodium had stem and root structure and its buds were axillary or
originated from the cortical parenchyma proliferation. The tuberous roots produced by this organ were adventitious
and accumulated inulin-type fructans mainly in the cortical parenchyma. The thickened underground system of V.
brevifolia, an herbaceous species, was a tuberous primary root whose buds originated from the proliferated
pericycle. The occurrence of these bud-forming underground systems, which stored reserve compounds, enabled
these plants to survive throughout unfavourable environmental conditions in the Cerrado, such as dry season and
frequent fires in the winter.
Key words: Bud, tuberous root, xylopodium, fructan, Cerrado
INTRODUCTION
The Brazilian Cerrado covers approximately 2
million km2, representing about 23% of the area of
the country (Ratter et al., 1997). Its flora contains
a large part of the tropical biodiversity (Felfili et
al., 1998) and, like that of all savannas, it is fireresistant and shows all the usual adaptations
(Ratter et al., 1997), such as thick corky bark,
tunicate leaf-bases in grasses, bud-forming
underground organs etc (Coutinho, 1990; Jeník,
1994; Ratter et al., 1997).
The presence of underground systems, which
produce buds and accumulate reserve compounds,
is one of the several adaptive strategies in plants
exposed to harsh conditions (Figueiredo-Ribeiro et
*
al., 1986; Pate et al., 1990; Bowen and Pate, 1993;
Bell et al., 1996). In plants from the Cerrado, the
high fructan content and its variation in
composition and content throughout the
phenological cycle, mainly during sprouting,
flowering and frutification, suggest that this
carbohydrate is a reserve compound which
contributes to adaptive features in plants subjected
to unfavourable environmental conditions
regarding to the soil, water and temperature
(Carvalho and Dietrich, 1993; Figueiredo-Ribeiro
et al., 1991).
The Asteraceae (Compositae) is the family more
represented in this vegetation after the
Leguminosae, that is, it is the second one with the
major number of species (Mendonça et al., 1998).
Author for correspondence
Brazilian Archives of Biology and Technology
980
Hayashi, A. H. and Appezzato-da-Glória, B.
Several representatives of this family and of others
have thickened underground systems (FigueiredoRibeiro et al., 1986; Tertuliano and FigueiredoRibeiro, 1993) and due to the scarce information
about their morphology and anatomy, the
designation of these organs is confused (Rizzini
and Heringer, 1961; Appezzato-da-Glória and
Estelita 2000).
The genus Vernonia (tribe Vernonieae) contains
about 500 species distributed in North and South
America, tropical Africa, Madagascar and tropical
Asia (Bremer, 1994). Vernonia grandiflora Less.
and V. brevifolia Less. are subshrubby and
herbaceous perennial geophytes, respectively,
found in the Brazilian Cerrado. The objective of
the present work was to study the anatomy of the
underground system of these two species to
elucidate the structural nature of these organs and
also the origin of their buds relating these features
to the survival of these species under Cerrado
conditions.
MATERIALS AND METHODS
Plant materials were collected from natural
populations in the Cerrado areas of São Paulo
State, Brazil. Vernonia grandiflora Less. was
collected at Fazenda Palmeira da Serra, in Pratânia
(22o48’S; 48o44’W), in December 2001, and V.
brevifolia Less. at Reserva Biológica e Estação
Experimental de Mogi Guaçu, in Mogi Guaçu
(22o18’S; 47o11’W), in May 2001. Voucher
specimens were deposited in the Herbarium of
Escola Superior de Agricultura “Luiz de Queiroz”,
Universidade de São Paulo (São Paulo State,
Brazil), under the numbers ESA 82474 (V.
grandiflora) and ESA 81071 (V. brevifolia).
Four individuals of V. grandiflora and two of V.
brevifolia were examined. For the anatomical
study, underground systems were fixed in FAA 50
(Johansen, 1940), dehydrated in a graded ethylic
series and then embedded in glycol methacrylate
resin. Serial sections (5-7 µm thick) were cut on a
rotary microtome (Sass, 1951) and stained with
toluidine blue O (Sakai, 1973). Freehand crosssections were also cut and stained with astra blue
and basic fuchsin (Roeser, 1972) and then
dehydrated in a graded ethylic series, and 50 and
100% butyl acetate, respectively. Permanent slides
were mounted in synthetic resin.
For the histochemical tests, freehand crosssections were cut from fresh material and treated
with Sudan IV to detect lipidic substances (Jensen,
1962). To identify the inulin-type fructans,
samples were fixed in 70% ethanol and sectioned
freehand. Inulin crystals were visualized under
polarized light and the presence of these crystals
was confirmed by a treatment with thymolsulphuric acid reagent (Johansen, 1940).
Photomicrographs were taken with a Nikon
Labophot microscope or a Nikon SMZ-2T
stereomicroscope.
RESULTS
The thickened underground system of V.
grandiflora was formed by a xylopodium and
many tuberous roots (Fig. 1A). The xylopodium
was an organ with a woody consistency and
formed by a vertically oriented axis in the soil.
This organ produced several buds distributed
along the axis (Fig. 1A-E) that might develop into
aerial stems. The adventitious tuberous roots were
originated from this xylopodium (Fig. 1A-B).
The anatomical analyses showed that the
xylopodium had a complex structure, according to
the sectioning levels indicated in Fig. 1A: natural
self-grafting of the bases of the stem axes at level
A (Fig. 2A), stem structure (endarch xylem) at
level B (Fig. 2C), transition region localized 574
µm above of the level C (Fig. 2D), and root
structure (exarch xylem) at level C (Fig. 2E). The
periderm covered the organ surface and enclosed
the cortex and vascular cylinder (Fig. 1C). The
innermost layer of the cortex, the endodermis, was
conspicuous with larger cells than the cortical
parenchyma cells (Fig. 2A-B). The buds originated
from the self-grafting region had an axillary origin
and the vascular trace reached the pith (Fig. 2A),
while the buds below of this region were
originated from the cortical parenchyma
proliferation (Figs. 1C and 1E).
Brazilian Archives of Biology and Technology
Anatomy of the Underground System in Vernonia grandiflora Less. and V. brevifolia Less
981
1 cm
AS
TR
B
A
PD
TR
PR
TR
RT
A
D
C
SX
E
Figure 1 - Vernonia grandiflora Less. A. General view of the xylopodium showing several buds
and tuberous roots. The letters (A, B, C) indicate the sectioned regions which are
shown in Fig. 2. B. Detail of the previous figure showing the buds (arrows). C-E.
Cross-sections of the xylopodium showing the buds (arrow in Fig. C) originated from
the cortical parenchyma proliferation. Bars = 200 µm (C); 870 µm (D, E). AS = aerial
stem, PD = periderm, PR = cortical parenchyma proliferation, RT = root trace, SX =
secondary xylem, TR = tuberous root
Brazilian Archives of Biology and Technology
Hayashi, A. H. and Appezzato-da-Glória, B.
982
E
SA
SA
E
A
C
D
B
C
E
Figure 2 - Vernonia grandiflora Less. A-E. Cross-sections of the xylopodium with the sectioned
regions shown in Fig. 1A. A. Natural self-grafting of the bases of two stem axes at
level A. Note the conspicuous endodermis and one axillary bud (arrow) with vascular
trace reaching the pith. B. Detail of the endodermis. C-E. Central region of the
vascular cylinder. C. Stem structure at level B. D. Transition region. E. Root structure
at level C. Note the exarch protoxylem (arrows). Bars = 760 µm (A-B); 35 µm (C-E).
E = endodermis, SA = stem axis
Brazilian Archives of Biology and Technology
Anatomy of the Underground System in Vernonia grandiflora Less. and V. brevifolia Less
EP
EP
P
CP
B
C
SP
SX
A
E
PX
E
PE
SX
D
E
SX
E
PX
F
Figure 3 - Vernonia grandiflora Less. A-F. Cross-sections of the tuberous root. A. General view
of the tuberous root showing the well developed cortical parenchyma. B. Formation of
the phellogen from the subepidermal layers. C. Sclereids among cortical parenchyma
cells. D. Endodermis with Casparian strips (arrows). E. Lipidic substances in the
endodermis. F. Inulin crystals accumulated mainly in the cortical parenchyma. Bars =
200 µm (A, F); 35 µm (B-D); 75 µm (E). CP = cortical parenchyma, E = endodermis,
EP = epidermis, P = phellogen, PE = pericycle, PX = primary xylem, SP = secondary
phloem, SX = secondary xylem
Brazilian Archives of Biology and Technology
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Hayashi, A. H. and Appezzato-da-Glória, B.
984
SA
A
SA
SA
B
PP
CP
SX
PD
E
PX
SP
C
D
A
CP
SX
PD
SP
E
E
E
E
PP
PP
CP
SP
E
PP
F
SP
SX
G
SX
PX
Figure 4 - Vernonia brevifolia Less. A. General view of the tuberous root. The letters (A, B) indicate
the sectioned regions which are shown in Fig. 4B-C. Note a contracted area (arrow). B-C.
Cross-sections of the underground system. B. Natural self-grafting of the bases of three
stem axes and the presence of one axillary bud (arrow) at level A. C. Root structure at
level B. D. Detail of the endodermis (arrows). E. Longitudinal section of the tuberous
root. Note the contracted area shown in Fig. 4A (arrow) with a reduced number of
proliferated pericycle and cortex layers. F-G. Cross-sections of the tuberous root. F.
Lipidic substances in the cortical parenchyma, endodermis, proliferated pericycle, and
parenchyma of secondary vascular tissues. G. Bud originated from the proliferated
pericycle. Bars = 450 µm (B); 200 µm (C-G). CP = cortical parenchyma, E = endodermis,
PD = periderm, PP = proliferated pericycle, PX = primary xylem, SA = stem axis, SP =
secondary phloem, SX = secondary xylem
Brazilian Archives of Biology and Technology
Anatomy of the Underground System in Vernonia grandiflora Less. and V. brevifolia Less
The adventitious tuberous roots produced by the
xylopodium were covered by the epidermis (Fig.
3A-B) and the phellogen was produced through
divisions of the subepidermal layers (Fig. 3B). The
cortical parenchyma was well developed and
constituted by many cell layers (Fig. 3A).
Sclereids occurred among these parenchymatic
cells (Fig. 3C). The endodermis presented
conspicuous Casparian strips (Fig. 3D) and its
cells were filled with lipidic substances (Fig. 3E).
The vascular cylinder was formed by the uniseriate
pericycle, and the secondary and primary vascular
tissues (Figs. 3A and 3D). The protoxylem had six
poles and centripetal maturation (exarch xylem).
Besides lipidic substances, these tuberous roots
also accumulated inulin-type fructans mainly in
the cortical parenchyma (Fig. 3F).
V. brevifolia developed a vertical, fleshy primary
root as thickened underground system (Fig. 4A).
This tuberous organ was contractile and its surface
was irregular showing wrinkles and contraction
areas (Figs. 4A and 4E). Aerial stems were
produced by the upper region of the underground
system and thin lateral roots were originated
throughout this organ (Fig. 4A). The upper region
of this thickened underground system was formed
by natural self-grafting of the bases of the stem
axes (Fig. 4B) between the levels A and B as
indicated in Fig. 4A, and root structure (exarch
xylem) (Fig. 4C) below of the level B. The
periderm covered the organ surface, followed
internally by the cortical parenchyma (Figs. 4C
and 4E-F). In the root structure, the endodermis
possessed larger cells than the cortical parenchyma
cells (Fig. 4C-G) and they were filled with lipidic
substances (Fig. 4F). The vascular cylinder
consisted of a proliferated pericycle and secondary
and primary vascular tissues (Fig. 4C).
The centre of the organ was occupied by the
exarch xylem that had two protoxylem poles. As
this root became thicker due to the vascular
cambium activity, the cortical parenchyma and
proliferated pericycle cells divided periclinally and
anticlinally according to the increased diameter of
the underground organ (Fig. 4C). In the contracted
areas, there was a reduced number of proliferated
pericycle and cortex layers (Fig. 4E), causing
surface wrinkling (Fig. 4A), when compared with
the non-contracted areas (Fig. 4E). Histochemical
tests indicated the presence of lipidic substances in
the cortical parenchyma, endodermis, proliferated
985
pericycle, and parenchyma of secondary vascular
tissues (Fig. 4F).
The buds originated from the upper region of the
underground system (level A) had an axillary
origin (Fig. 4B) because they were formed from
the bases of the self-grafting of the stem axes,
while in the root region the buds were originated
from the proliferated pericycle (Fig. 4G).
DISCUSSION
The underground system of V. grandiflora
consisted of a xylopodium and many adventitious
tuberous roots while in V. brevifolia it was a
tuberous primary root. According to Rizzini and
Heringer (1961), the xylopodium has a hard and
dry consistency with predominance of woody
tissues while the tuberous root has a watery soft
consistency with predominance of storage
parenchyma as verified in both studied species. In
other representatives of the genus Vernonia, the
underground systems consisted of rhizophores,
that is, underground stems (cotyledonary bud
origin) in association with the aerial stems
(plumule origin) (Menezes et al., 1979; Sajo and
Menezes, 1986; Hayashi and Appezzato-daGlória, 2005). Therefore, three types of
underground organs could be identified in the
same genus and tribe of the Asteraceae, showing
their morphological diversity.
The occurrence of xylopodia has been recorded in
Brazilian Cerrado species belonging to different
taxa (Appezzato-da-Glória and Estelita, 2000;
Milanez and Moraes-Dallaqua, 2003), including
Asteraceae representatives (Paviani, 1987, 1977).
In some species, the lower portion of the
xylopodium is joined to the upper portion of the
tuberous root, as in Mandevilla illustris, M.
velutina (Appezzato-da-Glória and Estelita, 2000),
and Pachyrhizus ahipa (Milanez and MoraesDallaqua, 2003). As xylopodia are situated
superficially in the driest soil part, they must
necessarily be provided with water and food
reserves in order to survive in dry seasons and to
produce the aerial stems during the rainy seasons
(Rizzini and Heringer, 1961). This must be the
reason for which the tuberous roots were
associated with the xylopodium in V. grandiflora
as well as to the three species previously
mentioned.
Brazilian Archives of Biology and Technology
986
Hayashi, A. H. and Appezzato-da-Glória, B.
The main characteristics of a xylopodium are
woody consistency, ability to sprout and complex
structure because of its nature (stem, root or both)
(Rizzini and Heringer, 1961; Appezzato-da-Glória
and Estelita, 2000). This structural complexity is
also related to the process of self-grafting of stem
axes (Appezzato-da-Glória and Estelita, 2000) as
verified in V. grandiflora.
The xylopodium formation is a response to severe
environmental conditions and also may be a
genetically determined structure as in a tuberous
root (Rizzini and Heringer, 1961). When the aerial
parts of the plant are damaged by fire or die in the
dry season, the underground shoot buds of the
xylopodium that are well protected against
overheating by the soil layer repeatedly sprout
(Jeník, 1994). Thus, during the life cycle of the
plant, these buds develop into aerial stems and
their bases undergo self-grafting as observed in V.
grandiflora.
The underground system of V. brevifolia was
constituted predominantly by a tuberous primary
root with small participation of stem structure
(self-grafting of the bases of the stem axes). This
tuberous organ showed contractile activity due to
fewer number of cell layers of proliferated
pericycle and cortex in contracted areas than in
non-contracted areas. However, in Chlorogalum
pomeridianum roots, cells of the inner and middle
cortex
underwent radial expansion and
longitudinal shortening following contraction.
Cells of the outermost cortex became distorted and
collapsed whilst the stele remained relatively
straight and undistorted (Jernstedt, 1984). In
Trifolium repens, the root contraction was caused
by the change in maturing phloem tissue, that is,
there was a large proportion of air space, the fibres
were shorter and distorted and the parenchyma
cells were larger and more numerous in contracted
area than in non-contracted area (Cresswell et al.,
1999). In V. brevifolia the contraction pulled the
tuberous root and its buds deeper into the ground,
a process that is an adaptive mechanism to adverse
environmental conditions as fire and drought in the
Cerrado.
In V. brevifolia the buds were originated from the
proliferated pericycle of the tuberous root whilst
the buds of V. grandiflora were originated from
the cortical parenchyma as described to Brasilia
sickii (Asteraceae) by Paviani (1987). In Vernonia
spp. (Menezes et al., 1979; Sajo and Menezes,
1986; Hayashi and Appezzato-da-Glória, 2005)
and Smallanthus sonchifolius (Machado et al.,
2004) the rhizophores (cauline structure) had
axillary buds.
In the tuberous roots of V. grandiflora and V.
brevifolia, the presence of lipidic substances was
demonstrated through histochemical tests. Hayashi
and Appezzato-da-Glória (2005) also verified
these substances in rhizophores of V. herbacea and
V. platensis. In addition, fructans were also stored
in the tuberous roots of V. grandiflora as showed
in the present work. According to Tertuliano and
Figueiredo-Ribeiro (1993), total fructans as a
proportion of dry mass were 2.4% in V. brevifolia
and less than 20% in V. grandiflora and in other
species analysed in tribe Vernonieae.
Fructans have been found in thickened
underground systems of Vernonia and of other
Asteraceae species from the Brazilian Cerrado
(Figueiredo-Ribeiro et al., 1986; Tertuliano and
Figueiredo-Ribeiro, 1993; Asega and Carvalho,
2004). These carbohydrates are generally found in
plants from temperate regions and then it states
that fructans are related to drought tolerance (Vijn
and Smeekens, 1999) and low temperature
(Hendry, 1987; Vijn and Smeekens, 1999).
Besides
being
considered
as
reserve
carbohydrates, fructans may also act as osmotic
regulators due to their rapid polymerization and
depolymerization (Figueiredo-Ribeiro, 1993).
V. grandiflora and V. brevifolia are well adapted
species to the Cerrado conditions because the
reserve compounds in the underground organs
enable the development of new shoots when the
aerial parts are damaged by fire or lost during
dormancy stage of the plant. These characteristics
are ecologically important for the survival of these
plants exposed to unfavourable conditions and this
knowledge enables a suitable management of these
species mainly in the disturbed areas in the
Cerrado.
ACKNOWLEDGEMENTS
We thank FAPESP (Process 00/12469-3) for the
financial support, CAPES and CNPq for the
grants. We also thank Dr. M. M. Pinto, a scientific
researcher at Reserva Biológica e Estação
Experimental de Mogi Guaçu, Instituto de
Botânica da Secretaria de Estado do Meio
Ambiente - SP, for the permission granted to
collect plant material for this work as well as for
the field assistance. This work is part of a PhD
thesis of Adriana Hissae Hayashi (Biologia
Brazilian Archives of Biology and Technology
Anatomy of the Underground System in Vernonia grandiflora Less. and V. brevifolia Less
Vegetal, Instituto de Biologia, Universidade
Estadual de Campinas, Brazil).
RESUMO
Este trabalho teve como objetivo estudar a
anatomia dos sistemas subterrâneos de Vernonia
grandiflora Less. e V. brevifolia Less.
(Vernonieae; Asteraceae), duas geófitas perenes, a
fim de esclarecer sua capacidade para brotar em
condições de Cerrado. O sistema subterrâneo
espessado de V. grandiflora, uma espécie
subarbustiva, é constituído pelo xilopódio e por
várias raízes tuberosas. O xilopódio possui
estrutura mista (radicular e caulinar) e suas gemas
são de origem axilar ou se originam a partir da
proliferação do parênquima cortical. As raízes
tuberosas produzidas por este órgão são
adventícias e acumulam frutanos do tipo inulina,
principalmente no parênquima cortical. Em V.
brevifolia, uma espécie herbácea, o sistema
subterrâneo espessado é constituído pela raiz
primária cujas gemas são originadas a partir do
periciclo proliferado. A ocorrência destes sistemas
subterrâneos
gemíferos,
que
armazenam
compostos de reserva, permite que estas plantas
sobrevivam às condições desfavoráveis do
Cerrado, tais como a estação seca e os freqüentes
incêndios durante o inverno.
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Received: November 11, 2005;
Revised: July 25, 2006;
Accepted: March 12, 2007.
Brazilian Archives of Biology and Technology