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Plant anatomy: history and future directions
The anatomy of neotropical galls and the untold lessons
about the morphogenetical potentialities of plants
Rodriguésia 75: e01542023. 2024
http://rodriguesia.jbrj.gov.br
DOI: http://dx.doi.org/10.1590/2175-7860202475007
Abstract
Plant anatomists perceive the plant body as the dynamic result of complex developmental processes which may
deviate during gall development. Gall development involves local responses forming a morphophysiological
continuum with the host plant organ, which can be addressed by anatomical studies. We revisited the history
of galls in Brazil, as well as their morphogenetical potentialities and integration with entomological, chemical,
physiological, and ecological approaches. The Fabaceae, Myrtaceae, Melastomataceae, and Asteraceae are
the main hosts of the Brazilian gall morphotyes, which can be classified according to their three-dimensional
shapess. Anatomical tools have been used to map cell and tissue fates in gall morphotypes, revealing the
potential of plant tissue systems to overexpress or inhibit standard plant development. In-depth anatomical,
cytological, histochemical, and immunocytochemical techniques have greatly expanded the knowledge of gall
traits and plant cell responses. The new structures of galls hosted on leaves, stems, roots, and reproductive
organs show consistent tissue specialization regarding the dermal and ground tissue systems, with the gall’s
vascular system being connected to preexisting or newly formed bundles of the host plant. Due to the diverse
stressors imposed on plant tissues, gall anatomy reveals adaptive responses that can be addressed from several
perspectives, including citizen science initiatives.
Key words: cell fates, ontogenesis, structure and function.
Resumo
Anatomistas vegetais percebem o corpo da planta como resultado de processos dinâmicos e complexos que
podem ser desviados ao longo do desenvolvimento da galha. Este desenvolvimento envolve respostas locais,
mas em um continuum morfofisiológico com o órgão hospedeiro, o que pode ser estudado do ponto de vista
anatômico. Revisitamos a história das galhas no Brasil, suas potencialidades morfogenéticas e integração com
abordagens entomológicas, químicas, fisiológicas e ecológicas. No Brasil, espécies de Fabaceae, Myrtaceae,
Melastomataceae e Asteraceae são as principais hospedeiras de diversos morfotipos de galhas classificados
com base em suas formas tridimensionais. Ferramentas anatômicas usadas para mapear o destino de células
e tecidos nas galhas revelam o potencial dos sistemas de tecidos vegetais para superexpressar ou inibir o
desenvolvimento vegetal padrão. Técnicas anatômicas, citológicas, histoquímicas e imunocitoquímicas
aprofundadas expandiram o conhecimento das características das galhas e das respostas das células vegetais.
As galhas hospedadas em folhas, caules, raízes e órgãos reprodutivos têm especialização tecidual consistente
nos sistemas de tecido dérmico e fundamental, com o sistema vascular das galhas conectado àqueles da planta
hospedeira. Devido a diversos estressores impostos aos tecidos vegetais, a anatomia das galhas revela respostas
adaptativas que podem ser abordadas por diversas perspectivas, incluindo iniciativas de ciência cidadã.
Palavras-chave: destinos celulares, ontogênese, estrutura e função.
Rosy Mary dos Santos Isaias1, Jane Elizabeth Kraus2, Elaine Cotrim Costa3
& Renê Gonçalves da Silva Carneiro4,5
1 Universidade Federal de Minas Gerais, Inst. Ciências Biológicas, Depto. Botânica, Pampulha, Belo Horizonte, MG, Brazil. ORCID: <https://orcid.org/0000-
0001-8500-3320>.
2 Universidade de São Paulo, Inst. Biociências, Depto. Botânica, Cidade Universitária, São Paulo, SP, Brazil. ORCID: <https://orcid.org/0009-0002-6925-9187>.
3 Universidade Federal do Rio Grande, Inst. Ciências Biológicas/Botânica, Campos Carreiros, Rio Grande, RS, Brazil. ORCID: <https://orcid.org/0000-0001-
6625-7595>.
4 Universidade Federal de Goiás, Inst. Ciências Biológicas, Depto. Botânica, Campus Samambaia, Goiânia, GO, Brazil. ORCID: <https://orcid.org/0000-0002-
4766-3851>.
5 Author for correspondence: renecarneiro@ufg.br
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Introduction
Plant anatomy is a crucial component of plant
biology, and plant anatomists are the researchers
who best understand the plant body as a dynamic
structure shaped by continuous and complex
processes. All plant cells, tissues, and organs go
through such processes, resulting from metabolic
interactions responsive to abiotic and biotic factors
of the environment (Mauseth 1988). Among the
biotic factors, there are organisms that induce galls
and influence plant development, resulting in the
diverse shapes of galls found in nature (Ferreira
et al. 2019), known as gall morphotypes (Isaias
et al. 2013).
Gall development involves cell hypertrophy
and hyperplasia processes, as well as cell
redifferentiation in the host plant organ, culminating
in the formation of new organs with specialized
tissues (Mani 1964). For example, the typical
nutritive tissue and the sclerenchyma are common
anatomical features of the Diptera, Hymenoptera,
and Lepidoptera galls (Ferreira et al. 2017, 2019;
Guedes et al. 2023a). In contrast, a nutritive-like
tissue occurs in some Hemiptera galls (Ferreira et
al. 2019). Plant morphologists and physiologists
may explore galls as models for the understanding
of plant developmental programs (Shorthouse
& Rohfritsch 1992) based on the premise that
the anatomical examination of galls showcases
how plants, under specific stimuli, can undergo
reprogramming to grow atypical structures.
The structural and metabolic patterns of these
atypical organs can deviate significantly from
the typical course of plant development (Isaias
et al. 2014b; Ferreira et al. 2019; Guedes et al.
2023a). Moreover, the restricted cellular changes
observed in galls underlie the focus on structural
and physiological studies (Carneiro et al. 2017),
although according to an integrative perspective
(Jorge et al. 2018), since the connection between
the gall tissues and the non-galled tissues of the host
plants are part of a morphophysiological continuum
(Mani 1964; Isaias et al. 2014b).
Brazil stands out as the epicenter of scientific
production in Cecidology, the study of galls.
Historical records date back to the early 20th century
when Tavares (1909) published the first data on the
host plant-galling insect systems in the Brazilian
flora. From the early 1980’s onwards, the first
anatomical diagnoses of galls described how cells
and tissues involved in the development of different
gall morphotypes are reprogrammed toward the
expression of new phenotypes (Arduin et al. 1989,
1991; Arduin & Kraus 1995, 2001) repetitively
found in nature (Isaias et al. 2013, 2014a). From
the perspective of the influence of the gall inducers’
taxa (Bronner 1992; Rohfritsch 1992), many galls
from Brazil have been found to fit previously
described patterns of Nearctic and Palearctic
galls. However, as diverse as the Brazilian flora is,
many peculiarities, herein understood as host plant
morphogenetical constraints and potentialities,
have been reported as novelties due to in-depth
anatomical investigations (cf. Arduin et al. 1991,
2005; Ferreira et al. 2019; Teixeira et al. 2022).
Anatomical traits, together with histochemical
profiles, have been used as diagnostic features of
the new functions assumed by plant cells and
tissues at the sites of gall development. In contrast
to the plant’s structural modules specialized for
photosynthesis, storage of water and metabolites,
and support of other organs, the physiological
processes of plants aim at the maintenance of new
tissue homeostasis, enabling the development and
maintenance of galls as ectopic new organs (Mani
1964) such as the horn-shaped gall on Copaifera
langsdorffii Desf. (Fabaceae) leaves (Carneiro et
al. 2017). The physiological demands imposed by
gall tissues have been interpreted as a complex set
of metabolic pathways that guarantee the balance
of reactive oxygen species (ROS), which ends up
triggering the first steps of gall induction (Isaias et
al. 2015). Furthermore, consistent data about the
anatomical development of galls are crucial for a
better elucidation of the genetic dynamics involved
in this interaction (Schultz et al. 2019). From the
first descriptive steps to the functional approaches
about gall structure, Brazilian cecidology has
progressed from understanding gall anatomy to
addressing functional traits. On this basis, we
review here the history of gall anatomy in Brazil
and its integration with entomological, chemical,
physiological, and ecological approaches, and we
point out future perspectives regarding the focus
of this line of research.
The 20th Century and the rst studies
on gall anatomy in Brazil
After the initial records of the presence of
galls in Brazil reported by Tavares (in 1909),
several studies on gall anatomy were undertaken
over the years, with emphasis on graduate programs
on Botany (Fig. 1) at the University of São Paulo
(USP) under the regency of Jane E. Kraus. In the
1980’s, as mentioned above, the first consistent
descriptive studies on the morphoanatomy and
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the ontogenesis of Neotropical galls generated the
first results, which were published during the next
decade and at the beginning of the 21st century
(Arduin et al. 1989, 1991, 2005; Arduin & Kraus
1995, 2001; Kraus et al. 1993, 1996, 1998, 2002;
Souza et al. 2000).
The 21th Century: Brazil stands out as
the epicenter of scientic production
in Cecidology
By the end of the 2000’s, the establishment
of a research group on the Structure, Chemistry,
and Physiology of Neotropical Galls at the Federal
University of Minas Gerais (UFMG), registered
in the “Conselho Nacional de Desenvolvimento
Científico e Tecnológico” - CNPq (Brazilian
National Council for Research) and headed by Rosy
M. S. Isaias (CNPq 2023), promoted a higher level
of the study of galls. The richness and diversity of
galls in the Neotropical region are well known,
and Fabaceae, Myrtaceae, Melastomataceae,
and Asteraceae are the main host plant families
reported in gall inventories of the Brazilian flora
(Isaias et al. 2021). In this scenario, particularly
important is the analysis of the inventories of
gall diversity and richness reported during the
period from 1990 to 2010. However, this analysis
reveals a profusion of confusing data regarding
the morphological terminology used to describe
the galls. Similar shapes were often referred to by
different, inaccurate names, thus making any type
of comparative analysis very difficult due to many
inconsistencies (Isaias et al. 2014a). The solution
came from the initiative of using names of standard
tridimensional forms to refer to gall morphotypes,
facilitating the recognition of galls and host plants
in nature. The recognition of host plants on the basis
of gall morphology is a trustworthy and efficient
taxonomic tool since each host plant-gall inducer
system has a peculiarly associated morphotype
(Isaias et al. 2013, 2014a). Despite the variety of
shapes, the development of galls involves a similar
functionality based on the search for a buffered
environment that ensures increased protection of
gall-inducing organisms against adverse biotic
and abiotic environmental conditions, as well as
higher-quality nutrition compared to free-living
herbivores, as demonstrated by comprehensive
empirical data and tests of hypotheses (Price et
al. 1987).
The effort to improve the terminology used for
gall shapes resulted in an illustrated and annotated
checklist of Brazilian gall morphotypes (Isaias et
al. 2013), which provides the standardization of
gall shapes by dividing 43 referenced shapes into
seven morphotypes. Among the tridimensional
standard shapes (Figs. 2-3), the globoid (Figs.
2a; 3a), lenticular (Figs. 2b; 3b), and conical
morphotypes (Figs. 2c; 3c) were found to be the
most common (Isaias et al. 2013). In addition to
providing a standardized terminology, this effort
also helps overcome problems generated by the
lack of taxonomic identity of the gall inducers and
enables comparative analyses of the data presented
in the inventories of gall richness and distribution
in Brazil (Isaias et al. 2014a) and worldwide.
The organization of gall tissues -
from the host organ
to the new structure
In terms of developmental pathways, galls
can be useful models for morphogenetic studies.
Mapping cell and tissue fates in different galls
reveals the potential of the three plant tissue systems
to express neoformations, which are also linked
to new physiological traits. The developmental
anatomy of galls in the Neotropics reveals that the
gall inducer stimuli may be balanced by the host
plant morphogenetical constraints (Isaias et al.
2014b; Ferreira et al. 2019), as demonstrated in
the Cecidomyiidae galls on Baccharis reticularia
(Asteraceae) and in the Calophya mammifex galls
on Schinus polygama (Anacardiaceae) (Guedes
et al. 2018). With non-galled tissues as control
samples, the analysis of gall tissues can indicate
Figure 1 – Time line illustrating the areas of contribution
to the research line on galls in the Brazilian flora.
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the origin and fates of the differentiated cells along
cecidogenesis, so that many of these silenced and
stimulated effects can be revealed (Fig. 4).
Prominent changes in the three plant tissue
systems usually indicate various degrees of
overexpression of preexisting traits, but the
differentiation of sclereids interspersed within the
gall parenchyma is not observed in non-galled
leaves of other species, such as Aspidosperma
spruceanum (Apocynaceae) (Formiga et al. 2011).
On the other hand, an example of an impaired
developmental feature of galls is the pericycle,
a cell layer adjacent to procambial derivatives
whose meristematic potential can be fundamental
for gall development since it is responsible for the
differentiation of fibers lining the vascular system,
forming a protective layer. Impaired lignification of
pericycle cell walls is relatively common in galls
(Meyer & Maresquelle 1983), as observed in several
leaf galls on B. concinna and B. dracunculifolia-
Cecidomyiidae (Diptera) (Arduin & Kraus 2001),
Ficus microcarpa (Moraceae)-Gynaikothrips
ficorum (Thysanoptera) (Souza et al. 2000),
Piptadenia gonoacantha (Fabaceae)-Cecidomyiidae
(Diptera) (Arduin & Kraus 1995), and Struthanthus
vulgaris (Loranthaceae)-Hymenoptera (Kraus et al.
2002). This is particularly evident in galls induced
by sap-sucking organisms, whose main feeding sites
are neoformed vascular bundles around the gall
chamber. These vascular bundles are surrounded
by parenchymatous cells near the phloem and
the xylem, instead of being covered by pericyclic
fibers (Carneiro et al. 2015; Ferreira et al. 2019).
In addition, the sclerenchyma in triozid-induced
galls (Fig. 3a) and other insect-induced galls often
differentiates from ground tissues and not from the
pericycle (Carneiro et al. 2014; Ferreira et al. 2019;
Guedes et al. 2023b).
The numerous plasmodesmata in living
sclereids indicate the possible translocation of
substances toward the feeding site of the inducer
or related to the maintenance of cecidogenesis
(cf. Meyer & Maresquelle 1983; Hori 1992).
This is also observed in neotropical galls (Kraus
et al. 1993; Oliveira et al. 2010) and in plants in
general, whose sclerenchyma cells (both fibers
and sclereids) may not be dead at maturity (Evert
2006). More recently, the lignification process has
been acknowledged as a pathway that scavenges
free radical molecules, representing a physiological
defense mechanism against excessive oxidative
stress (Oliveira et al. 2017), as further considered
in the present text.
In galls without a typical nutritive tissue
around the larva chamber, anatomical and
cytological investigations have shown the presence
of nutritive-like cells differentiated from the
vascular and perivascular parenchyma (most
probably, the pericycle), which are the feeding
sites of the gall inducers, in this case, triozid
phloem-feeders (Carneiro & Isaias 2015). Vascular
neoformation is quite important for the redirection
of metabolites toward the gall developmental sites.
In most galls, the neoformed vascularization is
connected to the vascular system of the host organs
(Meyer & Maresquelle 1983), but vascular cells
can have different origins. For instance, in leaf
galls on the Guarea macrophylla (Meliaceae)-
Figure 2 – a-c. Main gall morphotypes reported in the Brazilian flora – a. globoid gall on Psidium laruotteanum
Cambess. (Myrtaceae) induced by Nothotrioza acuminata Burckhardt 2022 (Hemiptera, Triozidae); b. lenticular gall
on Piper sp. (Piperaceae) by an unidentified inducer; c. conical gall on Byrsonima sp. (Malpighiaceae) induced by
an unidentified Cecidomyiidae (Diptera). Scale bars = 1 cm.
a b c
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Cecidomyiidae (Diptera) system (Kraus et al.
1996), the vascular system differentiates directly
from procambial cells, whereas in other galls the
vascular systems may derive from the vascular
parenchyma of preexisting vascular bundles or
from the ground parenchyma cells in the cortical
region of the developing gall (Carneiro & Isaias
2015; Bragança et al. 2021).
The vascular parenchyma cells may also be
hyperplastic, separating the conductive elements of
the xylem from the phloem, which appear as isolated
bundles immersed in the gall parenchyma, as
observed in the Cecidomyiidae galls on S. vulgaris
(Arduin et al. 1991). Changes in cell number, area,
and developmental patterns particularly occur in
some host plant-gall inducer systems, where the
phloem portion of the vascular bundles can be
wider than the xylem portion, and vessel elements
with helical thickening can predominate (Kraus
et al. 1993). Also, the differentiation of tracheids
where only procambial cells should be found, as
in the root galls of Cattleya guttata (Orchidaceae),
Figure 3 – a-c. Diagrams of the anatomical profiles of
the main gall morphotypes reported in the Brazilian flora
– a. globoid gall of Nothotrioza myrtoidis (Hemitera,
Triozidae) on Psidium myrtoides (Myrtaceae) leaves
- Adapted from Carneiro et al. (2014); b. lenticular
gall of Cecidomyiidae (Diptera) on Inga ingoides
(Fabaceae) leaves - Adapted from Bragança et al.
(2021); c. conical gall of Cecidomyiidae (Diptera) on
Byrsonima variabilis (Malpighiaceae) leaves - Authors’
archive, demonstrating tissue organization. Scale bars:
3a = 2 mm; 3b = 100 µm; 3c = 2 mm.
Figure 4 – a-b. Diagrams of the cell lineages (origins
and fates) in the tissues of mature leaves (NGL)
and hypothetical mature galls (MG) – a. diagrams
demonstrating that dermal, ground, and vascular
tissue systems of NGL originate by the differentiation
of leaf meristematic tissues (protoderm, ground
meristem, and procambial strands), while the dermal,
ground, and vascular tissues of MG originate from the
redifferentiation of epidermal and parenchyma leaf
cells; b. diagram of the MG in continuum with the
NGL lamina, showing the epidermis (yellow), vascular
bundles (pink and blue), the dorsiventral mesophyll
with palisade (light green) and spongy parenchyma
(purple) in NGL; and the epidermis (yellow), common
storage tissue (purple and light green), vascular bundles
(pink and blue), sclerenchyma layer (dark pink), and
typical nutritive tissue (dark green) in MG.
a
b
c
a
b
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indicates that gall induction may lead to the
premature differentiation of the vascular system
(Kraus & Tanoue 1999).
The new organogenesis alters
the ordinary patterns of the host plants
Any plant organ can host galls induced by
several taxa of organisms; most galls associate
with eudicotyledons, but, more rarely, they may
also be found in association with monocotyledons
and ferns. While, indeed, monocotyledons seem
to rarely host galls, ferns seem to be a neglected
group of plants in terms of gall studies, especially
when the first inventories of gall occurrence in
the Brazilian flora are analyzed (Farias et al.
2020). Consequently, few papers deal with the
morphological data of galls induced on ferns. Initial
records have reported anatomical changes caused
by a micromoth on the stems of Microgramma
squamulosa (Polypodiaceae) (Kraus et al. 1993),
whose inducer was then described as Tortrimosaica
polypodivora (Lepidoptera: Tortricidae) (Brown
et al. 2004). Recently, more accurate searches
in field trips have revealed many ferns hosting
diverse gall morphotypes (Santos & Maia 2018)
and new anatomical studies have been conducted
on fern galls. The structure of galls induced by T.
polypodivora has been revisited since complex
galls of this type are also induced on M. vaccinifolia
(Martins et al. 2023) and on M. mortoniana in
addition to M. squamulosa. Additionally, galls on
Niphidium crassifolium, another Polypodiaceae
species, have been recently studied anatomically
and biogeographically based on herbaria records,
with their anatomical characteristics showing that
such galls are induced by Diptera: Cecidomyiidae
in plants occurring across a wide geographical
range (Bragança et al. 2023).
Despite the taxonomical identity, all gall
hosts are stimulated by their associated inducers
in different ways that determine gall shape, size,
and functions (Mani 1964; Rohfritsch 1992).
Nevertheless, even though gall morphology is
considered to be the extended phenotype of its
inducer, the sites of oviposition (Formiga et al.
2011; Carneiro et al. 2015; Teixeira et al. 2022),
i.e., the plant organs, influence gall development.
Leaves are galled the most, but stems, roots, and
reproductive plant organs may also host galls, with
tissue specialization following a simple general
pattern involving the three tissue systems. The
dermal system assumes a protective role (when
covering the outer surface) or a nutritive role (when
lining the larval chamber); the ground system
constitutes a storage parenchyma with interspersed
sclereids and/or a sclerenchymatic sheath around
the innermost parenchyma layers that form nutritive
tissues; and the vascular system is formed either
by preexisting or neoformed bundles which
supply water and nutrients to both the gall and the
inducer (See Figs. 3-4). Such general anatomical
characteristics are common to most galls, but
peculiarities attributed to galls occurring in specific
organs may also occur.
Galls on roots are less frequent either owing to
a reduced number of gall inducers living in the soil
or to lack of information due to poor sampling. As
orchids usually have aerial roots, the visualization
of their root galls is easier, rendering them good
models for identifying some anatomical aspects of
root anatomy manipulation by the gall inducers.
In root galls induced by Hymenoptera on Cattleya
guttata (Orchidaceae), the velamen and the central
vascular cylinder remain unchanged, except for
their displacement toward the root apex. The
overdifferentiation of cortical parenchyma cells is
the most prominent feature in this root gall, and the
non-differentiation of the root cap cells highlights
an impairment of root standard anatomy (Kraus
& Tanoue 1999). These impairments have also
been reported for non-galled root galls on Ansellia
gigantea (Orchidaceae) under dry winter conditions
(Noel 1974), demonstrating a convergent structural
response of the roots of Orchidaceae species to both
abiotic and biotic stressors. Another peculiarity of
the root galls on C. guttata is the differentiation of
tracheoidal cells surrounding the larval chamber
(Kraus & Tanoue 1999). Tracheoidal cells are a
common structural trait of Orchidaceae (Burr &
Barthlott 1991) that provides further mechanical
support and aid to water-retention mechanisms
in non-galled orchid organs (Olatunji & Nengim
2008), a characteristic that may also apply to the
context of gall structure.
Additionally, the ontogenesis of root galls
on C. guttata reveals the presence of a group of
meristematic cells formed in an atypical region
of the plant body such as the parenchyma. The
formation of meristematic centers is well-known
in plant tissue culture (Kruglova et al. 2023), with
these areas being crucial for the development of new
morphological plant structures such as the galls.
Gall induction usually stimulates cell divisions
and growth in existing meristems or in totipotent
tissues such as the parenchyma, and may lead to the
differentiation of ectopic meristems, as observed
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in the horn-shaped galls on Copaifera langsdorffii
(Fabaceae) (Carneiro et al. 2017), in the bud
rosette galls on Guapira opposita (Nyctaginaceae)
(Fleury et al. 2015), and in the amorphous galls
on Miconia spp. (Melastomataceae) (Ferreira et
al. 2017). The formation of meristematic centers
shows that cecidogenesis affects processes of
cell differentiation, including dedifferentiation,
confirming that galls are new plant organs (Mani
1964).
Galls on stems and leaves commonly lead
to the most marked changes in the ground tissue
system, whose cell fates can be altered not only
toward parenchyma cells accumulating water
and primary and secondary metabolites, but also
toward the differentiation of new cell types. As
far as the development of stem galls is concerned,
the host stem structure is affected to different
degrees depending on the site of oviposition and
on the taxa of the gall inducer. When the adult’s
ovipositor or a recently hatched larva enters the
stem tissues, usually near the stem apex, shoot
elongation may be compromised, as observed for
the galls induced by Tortrimosaica polypodivora
(Lepidoptera, Tortricidae) on Microgramma
mortoniana (Polypodiaceae) (Lehn et al. 2020)
and on M. squamulosa (Kraus et al. 1993). When
the entry of T. polypodivora larvae does not
compromise the apical cell at the shoot apex, the
elongation of the stem is not affected, as is the
case for the Lepidoptera galls induced on Marcetia
taxifolia (Melastomataceae) (Ferreira & Isaias
2013) and for the Neolasioptera sp. (Diptera,
Cecidomyiidae) galls induced next to the stem apex
of Eremanthus erythropappus (Asteracae) (Jorge et
al. 2022a), whose stems continue to grow above the
site of gall development.
The development of globoid stem galls in
the Neolasioptera sp.-E. erythropappus system
involves a change in vascular cambium activity.
The anatomical consequences are the production
of less numerous but larger vessel elements and
the overproduction of vascular parenchyma cells.
In functional terms, the vascular traits of the
Neolasioptera sp. stem galls on E. erythropappus
result in increased water flow that supplies both
the galls and the non-galled portions of the stems
which continue to grow above the galls, allowing
the maintenance of shoot development even after
gall infestation (Jorge et al. 2022a). The similar
atypical activity of the vascular cambium is also
observed in Peumus boldus (Monimiaceae) due
to the development of Dasineura sp. stem galls.
In this case, the differentiation of the xylem is
detrimental to the phloem, with overproduction of
xylem parenchyma cells with poorly lignified cell
walls that can store water and nutrients, while the
differentiation of the phloem is inhibited (Guedes
et al. 2022, 2023b). In these two systems, changes
in the activity of the vascular cambium do not
affect xylem conductivity or the activity of the
shoot apical meristem (Jorge et al. 2022a; Guedes
et al. 2023b).
As an example of the importance of the
site of oviposition, galls on stem internodes may
develop due to the ability of the female inducers
to oviposit through leaf gaps, in the stem cortex
or in axillary buds, but also due to the ability of
the gall-inducing larvae to dig through the stem
cortex toward the pith parenchyma, as described
for Calophya rubra stem galls on S. polygama in
Chile (Guedes et al. 2018). The access through
leaf gaps avoids lignified tissues such as pericyclic
fibers and xylem and favors the establishment of
galls in stems, which are naturally harder than
leaves. As the first instar nymphs establish and
begin to feed, cell hypertrophy and hyperplasia
in the parenchyma pith is stimulated to generate
the gall (Guedes et al. 2018). In the C. rubra stem
galls, as well as in other stem galls (Ferreira &
Isaias 2013; Ferreira et al. 2022; Jorge et al. 2022a,
b), phellogen activity confers further protection to
the gall inducers by the production of additional
cork (phellem) layers on the outer surface of the
galls in a process similar to the cork production
in non-galled stems in secondary growth. Further
meristematic activity in stem galls reveals that the
activity of cambium-like meristems in the gall
cortex results in a complex, thickened and vastly
reinforced structure, as observed for the galls
induced by Eucecidoses minutanus (Lepitoptera)
on the buds of Schinus engleri (Anacardiaceae),
whose shoots are transformed into galls (Ferreira
et al. 2022). Thus, the meristematic activity of galls
should be further explored as a potential source
of many structural novelties, especially if studied
using the ontogenetical approach.
Galls on leaves involve the redirection of the
structure, standardly adapted to photosynthesis,
toward supporting the life cycle of the inducers,
providing food, shelter, and a buffered
microenvironment (Stone & Schönrogge 2003).
The chlorophyllous parenchyma (spongy and
palisade) is often the tissue most modified by cell
hypertrophy and/or hyperplasia. Notably, these
changes primarily occur in the spongy parenchyma,
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whose cells respond more quickly to the outer stimuli
than the palisade parenchyma, with the loss of
intercellular spaces. Such responses of parenchyma
homogenization have been reported in the galls
induced by distinct insects on S. vulgaris (Arduin
et al. 1991; Kraus et al. 2002), Guarea macrophylla
(Meliaceae) (Kraus et al. 1996), and Psidium
myrtoides (Myrtaceae) (Carneiro et al. 2014, 2015).
The loss of dorsiventrality in leaf laminas hosting
galls is another important consequence of gall
development, which was elegantly diagnosed in
leaf folding galls induced by Thysanoptera on Ficus
microcarpa (Moraceae) (Souza et al. 2000) and
Myrcia splendens (Myrtaceae) (Jorge et al. 2018).
Changes of parenchyma cell fates, as in the
case of galls induced by Diptera (Cecidomyiidae),
Lepidoptera, and Hymenoptera, result in the
formation of highly specialized nutritive tissues. The
cytoplasm of nutritive cells is rich in metabolites
(see ahead), fragmented vacuoles, hypertrophied
nuclei and nucleoli, and abundant organelles
(Bronner 1977, 1992; Meyer & Maresquelle 1983;
Rohfritsch 1992; Ferreira et al. 2019). In general
terms, typical nutritive tissues are characterized
by the accumulation of starch, lipids, or proteins
and form one or more continuous layers around
the larval chamber (Ferreira et al. 2017). The
accumulated nutrients form specific gradients
depending on the inducer’s taxon and on the stage
of development (Oliveira et al. 2010; Carneiro
et al. 2014, 2015; Carneiro & Isaias 2015). The
presence of an active inducer is necessary to initiate
and maintain the cytohistochemical characteristics
of the nutritive tissue; in the absence of the larva
(death by predation or parasitoidism), the nutritive
cells lose their metabolic and ultrastructural
characteristics (Bronner 1992). Even though
classical works refer to Lepidoptera galls typically
having no nutritive tissue, a recent review has
indicated that the formation of a typical nutritive
tissue is a common anatomical trait of Lepidoptera
galls (Guedes et al. 2023b). The nutritive cells of
these galls are located around the larval chamber,
have an abundant cytoplasm and large nuclei
with one or more nucleoli, and are in intense
division, being smaller in size than the surrounding
parenchyma. Thus, they have characteristics similar
to those described for the nutritive tissues of galls
induced by other groups of insects, with lipids
as the main storage reserve. The gall-inducing
Hymenoptera and Lepidoptera (Motta et al. 2005;
Vieira & Kraus 2007), as is true for other chewing
insects, stimulate the accumulation of lipids in the
nutritive cells of their galls, which may be tested
by the reaction with one of the Sudan’s reactives
(Vieira & Kraus 2007; Rezende et al. 2019).
Peculiar cases of gall anatomy
regarding the taxa of the inducers
The Diptera: Cecidomyiidae-induced galls
are the most common in the Brazilian flora, with
265 of them having been described (Maia 2021),
while the Hymenoptera and Thysanoptera galls
are not so commonly reported in the inventories
(Maia 2012). Thysanoptera-induced galls may
not be formed by specialized tissues; instead, they
may be characterized by necrotic spots, sites of cell
hypertrophy, and hyperplasia in the ground system.
Thus, for instance, the ordinary functionality of
the leaves for photosynthesis and respiration is
altered toward protecting and nurturing the colony
of Gynaikothrips ficorum (Thysanopera) on F.
microcarpa (Souza et al. 2000).
An intriguing characteristic is that gall
shapes and sizes are usually constant, but sexually
dimorphic galls may occur, as is the case for
Eriococcid-induced galls, whose male-induced
galls are smaller and simpler than the large, more
complex, galls induced by females (Gonçalves et
al. 2005). This sexual dimorphism results from
the differences in chemical signalers (Gullan et
al. 2005), which make the Eriococcid galls good
models for determining the origin of gall shapes
and their cytological potentialities. In the Annona
dolabripetala (= Rollinia laurifolia) (Annonaceae)-
Pseudotectococcus rolliniae (Hemiptera) system,
female-induced galls have a longer life cycle and
consequently higher stimuli for the development
of parenchyma cells than male-induced galls
(Gonçalves et al. 2005, 2009). The anatomy of the
the Pseudobombax grandiflorum (Malvaceae)-
Eriogalococcus isaias (Hemiptera) system shows
less evident differences between male- and
female-induced galls regarding the shape of the
gall chamber and cell wall lignification in a wider
area on top of the chamber of the galls induced by
E. isaias females (Magalhães et al. 2015). In this
case, the gall morphotype is the same independently
of the sex of the inducers, but the mapping of the
cell origin and fate has been used to support the
different determination of gall induction by females
and males. In the other taxonomic groups of insect-
induced galls, the shapes rarely vary according to
sex, as surprisingly observed in Cecidomyiidae-
induced galls on Matayba guianensis (Sapindaceae)
(Gonçalves et al. 2022).
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Gall anatomy elucidates
gall functional traits
Together with a greater investment
in anatomical studies, histochemical,
immunocytochemical, and cytological analyses
have expanded the knowledge of gall functional
traits, revealing potential cell responses in each
plant tissue system. The dermal system is the
first line of contact of the gall inducer with its
host plant, where oviposition and the feeding
activity of the larvae occur. Salivary secretions
may induce increasing cell divisions, which may
indicate the return of the epidermal cells to the
meristematic condition. Also, changes in the
patterns of determination of cell origin and fates
in the epidermal cell mosaic (Glover 2000) result
in the overexpression or impairment of trichome
and stomata differentiation, with these structures
being less dense or malformed. Trichomes may
buffer the environmental abiotic factors, and their
overdifferentiation, hyperplasia and/or hypertrophy
are anatomical traits used to distinguish different
morphospecies of Cecidomyiidae galls on Mimosa
gemmulata (Fabaceae) (Costa et al. 2022a) and
Croton floribundus (Euphorbiaceae) (Teixeira
et al. 2022). Stomata malformation indicates the
incapacity of the leaf lamina to photosynthesize
and to perform cellular respiration, as observed
in leaf galls on F. microcarpa (Souza et al. 2000),
and Aspidosperma spp. (Lemos-Filho et al. 2007).
In addition, the larger stomata of Clinodiplosis
profusa (Diptera, Cecidomyiidae) and Eugenia
uniflora (Myrtaceae) galls may allow higher gas
exchange rates and tissue aeration in galls than
in host leaves (Castro et al. 2023). Periderm
can replace epidermis as the protective outer
layer, expressing an unusual program in leaf
development, but observed on leaf galls on S.
vulgaris (Arduin et al. 1989; Kraus et al. 2002) and
Guarea macrophylla (Kraus et al. 1996).
The galls induced by different organisms on
superhosts of galling herbivores reveal the potential
of each parasite to drive cecidogenesis in particular
ways (Cornell 1983), with the superhosts of galling
herbivores thus representing adequate models for
addressing hypotheses about plant potentialities.
Their associated gall inducers may cohabit not
only the same plant individual, but in some cases
the same plant organ, as observed in Copaifera
langsdorffii-Cecidomyiidae (Diptera) systems,
requiring seasonal syndromes in order to share
the same plant potentialities over a one-year time
(Oliveira et al. 2013). The different anatomical
profiles of the gall morphotypes on C. langsdorffii
indicate different impacts and constraints regarding
the same plant potential (Oliveira et al. 2008).
The study of galls on Lonchocarpus
muehlbergianus (Fabaceae) has provided a new
understanding of gall anatomy and histochemistry
since its gall inducer, Euphalerus ostreoides
(Hemiptera, Psyllidae) was previously considered
incapable of inducing the differentiation of
nutritive cells (Oliveira et al. 2006). However,
this understanding began to change when these
galls were found to have peculiar ultrastructural
characteristics in the cells that accumulate
carbohydrates. Carbohydrates were already known
to accumulate in the tissues of galls induced by E.
ostreoides (see Oliveira et al. 2006), but no cellular
or subcellular characteristics of such galls had
been previously described. Further investigations
of these galls by Isaias et al. (2011) demonstrated
that the ultrastructural features of cells where
the carbohydrates accumulate and where the
gall inducer feeds were similar to those of true
nutritive tissues formerly described by Bronner
(1992) for Cecidomyiidae (Diptera) and Cynipidae
(Hymenoptera) galls. This was the first time that
histochemical profiles and ultrastructural analyses
were used together to describe a nutritive-like
tissue, i.e., a tissue that is similar in structure and
function to those described in the classical literature
for other insects, but does not fully fit the concept
of “true nutritive tissues” described by Bronner
(1992). The fact that nutritive-like tissues were
reported for galls induced by a sap-sucking insect,
classically believed to induce non-nutritive galls,
was considered a paradigm shift.
Further investigations on the “nutritive
nature” of hemipteran galls have shown the
accumulation of primary metabolites and highly
specialized ultrastructure of cells in galls induced
by Nothotrioza myrtoides and N. cattleyani
(Hemiptera, Triozidae) on P. myrtoides and P.
cattleyanum (Myrtaceae) (Carneiro et al. 2014,
2015), when the terminology “nutritive-like
cells” and “nutritive tissues” was used for the
first time to describe cell types of galls induced
by sap-sucking insects. Beyond the nutritional
aspects concerning plant cell manipulation, the
analyses of L. muehlbergianus galls demonstrated
the accumulation of oxonium salts, a novelty
for flavonoidic derivatives described in galls,
highlighting the ability of the gall inducer to
manipulate the chemical profile of the plant
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(Oliveira et al. 2006). The phenolic derivatives
mediate plant-herbivore interactions along several
pathways and, as the investigations on gall anatomy,
histochemistry and immunocytochemistry have
evolved, the association of phenolics with plant
growth regulators and as ROS scavengers for
the maintenance of tissue homeostasis has been
discussed.
The role of metabolites -
from chemical defenses
to signalers of gall development
More than being astringent molecules that
turn plant tissues unpalatable and deter herbivore
attacks, phenolics interact with other molecules
taking part in crucial steps of gall development.
The effects of the fluctuation in the levels of
phenolics in plant and gall tissues may influence
gall metabolism and the maintenance of tissue
homeostasis (Isaias et al. 2015). In galls, the
phenolic compounds contribute to absorbing and
neutralizing free radicals, which seem to be one of
the main roles of these compounds in gall tissues
(Detoni et al. 2010, 2011; Isaias et al. 2015).
Phenolic compounds have been related to the
defensive role against parasites and/or parasitoids
(Harborne 1980), fungi or other agents in galls.
Later, they were suggested to be involved in
hormonal regulation, inhibiting indole-3-acetic
acid (IAA) oxidases, thus indirectly increasing
the accumulation of auxins (Hori 1992), which are
phytohormones responsible for cell hypertrophy
(Cleland 1995). As naturally phenolic-rich
structures, galls are good models demonstrating
the interaction of phenolics and phytohormones
due to the increased and local cell hypertrophy and
hyperplasia. Histochemical tests were used for the
detection of this interaction (Leopold & Plummer
1961), with the Ehrlich’s reagent revealing the
accumulation of IAA together with catechol,
chlorogenic acid or caffeic acid by the development
of different colors. By the application of this reagent,
the double accumulation of phenolic compounds
and IAA could be detected in the parenchyma of
Cecidomyiidae galls on P. gonoacantha (Bedetti et
al. 2017, 2018). Curiously, the sites with the most
intense staining of the phenolics-IAA complex are
also the sites with the highest cell hypertrophy,
thus supporting the growth-promoting effect
of phenolic accumulation in galls (Hori 1992).
Analyses of the horn-shaped galls on C. langsdorffii
(Carneiro et al. 2017), for example, demonstrated
that the distribution of phytohormones along
the developmental process is crucial for the
determination of the gall bizarre shape. Together
with auxins, cytokinins in gall tissues were
histochemically and immunocytochemically
detected at hyperplastic sites, confirming the role
of these two phytohormones in the determination
of gall shapes (Bedetti et al. 2017, 2018). Galls
have been used for proposing hypothetical models
of plant organogenesis involving ROS-phenolics-
IAA-cytokinins based on empirical evidence. These
proposals are valuable for the understanding of
possible plant responses to a wide variety of biotic
and abiotic stressors.
Gall responses to environmental
conditions
Environmental conditions such as water
availability, light intensity, and temperature
variations have effects on the diversity of gall
structures (Stone & Schönrogge 2003), as
documented in galls in the restrictive coastal
environments of the Brazilian Restinga (Isaias et
al. 2017; Arriola et al. 2018; Costa et al. 2022b).
The effects of water availability and light intensity
on gall structure have been recently investigated,
demonstrating a high investment in water-storage
parenchyma, a site of ion accumulation, in leaf
galls on Avicennia schaueriana (Acanthaceae)-
Meunieriella sp. (Diptera, Cecidomyiidae)
system. In these galls, salt excess is removed by
epidermal salt glands, favoring internal ion balance
(Nobrega et al. 2021), a specific environmental
adaptation to the variable salinity and flooding
of mangrove environments. In the case of the
Mimosa tenuiflora (Fabaceae) - Lopesia mimosae
(Diptera, Cecidomyiidae) system, cell wall porosity
mediated by methyl-esterified homogalacturonans
seems to favor water flux toward the storage
parenchyma, favoring gall development in the
Caatinga environment (Nogueira et al. 2022).
The hyperplasia and cell hypertrophy of the
ground tissue system are also influenced by light
conditions, with effects on sun and shade galls of
C. profusa on E. uniflora (Castro et al. 2023).
In addition to abiotic factors, the diverse
guild of organisms associated with galls such as
parasitoids, inquilines, predators, and successors
(Luz & Mendonça-Júnior 2019) can affect gall
structure. The attack by these organisms may
cause the collapse of nutritive cells, the loss of
cell membrane integrity (Rezende et al. 2019),
and precocious gall senescence (Costa et al.
2022c). In contrast to the effect of parasitoids, the
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Rodriguésia 75: e01542023. 2024
additional feeding stimuli of inquilines may induce
an increase in gall tissue thickness (Rezende et al.
2019, 2021). The successors, such as ants, may
occupy post-senescent galls, and, interestingly,
their movements when entering and exiting the
gall seem to reactivate cambium activity and
stimulate the differentiation of an ectopic phellogen
lining the larval chamber, as demonstrated for E.
erythropappus stem galls (Jorge et al. 2022a). This
post-senescence case of activity in gall tissues has
been used to raise the interest of young students
in nature and science using storytelling strategies
(Jorge et al. 2022b, 2023).
Studies of gall anatomy based on the
histochemistry, immunocytochemistry, cytology,
physiology, and chemistry of Brazilian host plant-
gall inducer systems are progressing towards the
interpretation of structural and functional traits not
only at the species-specific level but also in terms
of environmental bases since gall development
is a highly multifactorial phenomenon (Fig. 5).
Thus, we propose that gall development should be
interpreted as the result of taxon-dependent changes
caused by the different galling organisms, but also
by the various constraints and potentialities peculiar
to each plant species and to each plant organ. As
a product of complex ecological phenomena, gall
structure should also be considered in terms of
biotic and abiotic factors (Fig. 5) since galls are not
parasite-free and are found across different biomes
in Brazil and worldwide. Based on this perspective,
plant anatomists have adhered to the open field of
interdisciplinary research that is still growing and
innovating. From a broader perspective, data of
gall occurrence in Brazilian phytophysiognomies
is of paramount importance for the progression of
gall studies toward understanding functional traits,
adaptive anatomical features under current and
future scenarios of climate changes.
Acknowledgements
The authors thank Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq;
304535/2019-2), Fundação de Amparo à Pesquisa
do Estado de Minas Gerais (FAPEMIG), and
Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior (CAPES), for financial support.
Data availability statement
In accordance with Open Science
communication practices, the authors inform that
all data are available within the manuscript.
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Area Editor: Dr. João Paulo Basso-Alves
Received on August 31, 2023. Accepted on February 27, 2024.
This is an open-access article distributed under the terms of the Creative Commons Attribution License.
