The mechanism of plant gall induction by insects: revealing clues, facts, and consequences in a cross-kingdom complex interaction

Abstract

Galls are defined as modifications of the normal developmental design of plants, produced by a specific reaction to the presence and activity of a foreign organism. Although different organisms have the ability to induce galls in plants, insect-induced galls are the most elaborate and diverse. Some hypotheses have been proposed to explain the induction mechanism of plant galls by insects. The most general hypothesis suggests that gall formation is triggered by the action of chemical substances secreted by the gall inducer, including plant growth regulators such as auxins, cytokinins, indole-3-acetic acid (IAA), and other types of compounds. However, the mode of action of these chemical substances and the general mechanism by which the insect could control and manipulate plant development and physiology is still not known. Moreover, resulting from the complexity of the induction process and development of insect galls, the chemical hypothesis is very unlikely a complete explanation of the mechanism of induction and morphogenesis of these structures. Previous and new highlights of insect gall systems with emphasis on the induction process were analyzed on the basis of the author’s integrated point of view to propose a different perspective of gall induction, which is provided in this article. Due to the extraordinary diversity of shapes, colors, and complex structures present in insect galls, they are useful models for studying how form and structure are determined at the molecular level in plant systems. Furthermore, plant galls constitute an important source of material for the study and exploration of new chemical substances of interest to humans, due to their physiological and adaptive characteristics. Considering the finely tuned control of morphogenesis, structural complexity, and biochemical regulation of plant galls induced by insects, it is proposed that an induction mechanism mediated by the insertion of exogenous genetic elements into the genome of plant gall cells could be involved in the formation of this kind of structure through an endosymbiotic bacterium.

Full text

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The mechanism of plant gall induction by insects: revealing clues,
facts, and consequences in a cross-kingdom complex interaction
Omar Gätjens-Boniche
Laboratorio de Biología Molecular, Escuela de Ciencias Naturales y Exactas, Campus Tecnológico Local San Carlos,
Instituto Tecnológico de Costa Rica. Santa Clara, San Carlos, Alajuela, Costa Rica; ogatjens@itcr.ac.cr,
ogatjensboniche@gmail.com
Received 07-XI-2018. Corrected 28-V-2019. Accepted 23-IX-2019.
Abstract: Galls are defined as modifications of the normal developmental design of plants, produced by a spe-
cific reaction to the presence and activity of a foreign organism. Although different organisms have the ability
to induce galls in plants, insect-induced galls are the most elaborate and diverse. Some hypotheses have been
proposed to explain the induction mechanism of plant galls by insects. The most general hypothesis suggests
that gall formation is triggered by the action of chemical substances secreted by the gall inducer, including
plant growth regulators such as auxins, cytokinins, indole-3-acetic acid (IAA), and other types of compounds.
However, the mode of action of these chemical substances and the general mechanism by which the insect
could control and manipulate plant development and physiology is still not known. Moreover, resulting from the
complexity of the induction process and development of insect galls, the chemical hypothesis is very unlikely
a complete explanation of the mechanism of induction and morphogenesis of these structures. Previous and
new highlights of insect gall systems with emphasis on the induction process were analyzed on the basis of the
author’s integrated point of view to propose a different perspective of gall induction, which is provided in this
article. Due to the extraordinary diversity of shapes, colors, and complex structures present in insect galls, they
are useful models for studying how form and structure are determined at the molecular level in plant systems.
Furthermore, plant galls constitute an important source of material for the study and exploration of new chemi-
cal substances of interest to humans, due to their physiological and adaptive characteristics. Considering the
finely tuned control of morphogenesis, structural complexity, and biochemical regulation of plant galls induced
by insects, it is proposed that an induction mechanism mediated by the insertion of exogenous genetic elements
into the genome of plant gall cells could be involved in the formation of this kind of structure through an endo-
symbiotic bacterium.
Key words: insect galls, inductor insect, induction mechanism, plant morphogenesis, effectors.
The term plant gall has been applied to
different systems, and although there is no
consensus about the definition of the term,
the same has been used as a generalized
expression more than a precise scientific term
or concept (Williams, 1994). Nonetheless, in
general terms, galls could be defined as devia-
tions in the normal plant development pattern,
produced by a specific reaction to the presence
and activity of a foreign organism (Shorthouse
& Rohfritsch, 1992; Inbar et al., 2009; Huang
et al., 2015). Gall-inducing insects, also called
gall inducers, gall makers, or simply gallers,
live within the plant tissue, which supplies
food, low levels of potentially harmful chemi-
cal substances, protection against unfavorable
Gätjens-Boniche, O. (2019). The mechanism of plant gall induction by insects: revealing clues,
facts, and consequences in a cross-kingdom complex interaction. Revista de Biología
Tropical, 67(6), 1359-1382.
SPECIAL ARTICLE

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environmental factors (Nogueira, Costa, Silva,
& Isaias, 2018), and shelter against natural
enemies (Mani, 1992; Ananthakrishnan, 1998;
Raman, Schaefer, & Withers, 2005; Tooker
& De Moraes, 2008; Tooker, Rohr, Abraham-
son, & De Moraes, 2008; Huang et al., 2015;
Isaias et al., 2018).
The meaning of the adaptive value of galls
and the kind of biological interaction existing
between gall-inducing insects and their host
plants is the subject of a continuous debate
among the different groups of researchers that
work in the field (Nyman & Julkunen 2000;
Stone & Schönrogge, 2003). Some groups
established that galls originated as a mecha-
nism of defense developed by insects against
attack by their natural enemies. Moreover, the
main function of the gall is to give shelter and
food to the larvae of the galling insect; how-
ever, this and other related ideas are still the
target of extensive debate (Ananthakrishnan,
1998; Stone & Cook 1998; Price, Waring &
Fernández, 1986; Stone & Schönrogge, 2003;
Tooker et al., 2008; Giron, Huguet, Stone, &
Body, 2016). Different lines of thought relate
galls with processes of pathogenesis, symbio-
sis, and defense mechanisms in plants (Hart-
nett & Abrahamson, 1979; Price et al., 1986).
Regardless of the type of specific interaction
between gall-inducing insects and their host
plants, natural selection consequently operates
on the insect to stimulate the development of
protective and/or nutritive tissues in the plant;
on the other hand, in the plant, natural selec-
tion acts to resist the stimulus generated by the
insect (Ananthakrishnan, 1998).
Hymenoptera and Diptera are two orders
with a particularly large number of gall induc-
ers, but great diversity can also be found in
galls formed by thrips, aphids, and insects from
other orders (Ananthakrishnan, 1998; Han-
son & Gómez-Laurito, 2005). A large number
and diversity of plant gall morphotypes and
inducing insects have been reported world-
wide (Espírito-Santo & Fernandes, 2007). New
species of inducing insects are periodically
described, while other studies on the abundance
and diversity of gall morphotypes, as well as
their corresponding inducers, has helped to
broaden the existing knowledge in this field
(Shorthouse & Rohfritsch, 1992; Williams,
1994; Ronquist & Liljeblad, 2001; Hanson &
Gómez-Laurito, 2005; Dalbem & Mendonça,
2006; Güçlü, Hayat, Shorthouse, & Göksel,
2008; Coelho et al., 2009; Maia, Fernandes,
Magalhãcs, & Santos, 2010a; Maia, Fleury,
Soares, & Isaias, 2010b; Medianero, Paniagua,
& Castaño-Meneses, 2010; Maia & Oliveira,
2010; Santos, Almeida-Cortez & Fernandes,
2011; Sano, Havil, & Ozaki, 2011; Maia, 2014;
Santos de Araújo, 2017; Martins dos Santos,
Pereira Lima, Souza Suares, & Calado, 2018).
Besides insects, plant galls are also
induced by a great variety of organisms such as
bacteria, fungi, nematodes, and mites (Leitch,
1994; Williams, 1994; Ananthakrishnan, 1998,
Raman, 2011). Galls induced by insects are
distinct from those induced by fungi and bacte-
ria in their form, organization, and complexity.
More complex and diverse galls are induced
by insects such as those of the Cynipidae and
Cecidiomyiidae families, which show extreme
examples of radial symmetry, belonging to the
orders Hymenoptera and Diptera, respectively
(Raman, Cruz, Muniappan, & Reddy, 2007;
Sinnott, 1960; Raman, 2011). A general scheme
for the structural complexity of plant galls
and the taxonomic groups of their inducers
is proposed by the author from the reviewed
literature (Fig. 1) (Rohfritsch & Shorthouse,
1982; Mani, 1992; Davey, Curtis, Gartland, &
Power, 1994; Gómez & Kisimova-Horovitz,
1997; Williams, 1994; Valentine, 2003; Sá
et al., 2009; Raman 2011; Álvarez, Molist,
González-Sierra, Martínez, & Nieto-Nafría,
2014; Formiga, Silveira, Fernandes, & Isaias,
2015; Muñoz-Viveros et al., 2014; Guimarães,
Neufeld, Santiago-Fernandes, & Viera, 2015;
Hernández-Soto et al., 2015; Suzuki, Morigu-
chi, & Yamamoto, 2015; Mellah, Enhassaïni, &
Álvarez, 2016; Oliveira et al., 2016; Richard-
son, Body, Warmund, Schultz, & Appel, 2016;
Ferreira, Álvarez, Avritzer, & Isaias, 2017;
Palomares-Rius, Escobar, Cabrera, Vovlas, &
Castillo, 2017; Cotrim Costa, Gonçalves da
Silva Carneiro, Santos Silva, & Isaias, 2018;

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Nogueira, Costa, Silva, & Isaias, 2018); how-
ever, a consensus on this approach does not
exist, and substantial variation can be observed
within each group.
The fact that different groups of insects
possess the capacity to form galls in a wide
variety of plants has motivated a great number
of investigations attempting to elucidate the
mechanism of induction of this type of struc-
ture. Nevertheless, considering the importance
of galls as models for understanding a series of
fundamental processes in the development of
plants, the induction mechanisms and the evo-
lutionary context of this type of structure is still
poorly understood (Stone & Schönrogge, 2003,
Raman, 2011; Oates, Denby, Myburg, Slippers,
& Naidoo, 2016).
The aim of this paper is to provide an
updated general description of plant galls
induced by insects, focused on the induc-
tion process as well as how, according to an
integrated interpretation by the author, the
associated characteristics of these structures
and the biological processes they regulate
could be the basis for an alternative induction
hypothesis mediated by the insertion of exog-
enous genetic elements into the plant gall cells
through some endosymbiotic bacteria originat-
ing from the insect.
Plant gall development and diversity
of plant gall-inducing insects
The association between galls and their
inducing organisms has likely been recognized
since the study of these systems began (Mani,
1992). However, it was not until the 17th cen-
tury that Malpighi described, in the Western
World, that the growth and development of
these structures was correlated to the activity of
feeding, oviposition, and particular nutritional
requirements of the inducing insect (Fagan,
1918; Hough, 1953).
Gall morphogenesis is a complex phe-
nomenon, which involves reorientation of the
Fig. 1. Proposed general scheme for the structural complexity of plant galls and the taxonomic groups of gall inducers. Images
show some examples of galls. Bacteria crown gall found on Pittosporum sp. (Pittosporaceae), induced by Agrobacterium
tumefaciens. Fungus gall on Satyria warszewiczii (Ericaceae), induced by Exobasidium emeritense. Nematode gall induced
by Meloidogyne incognita on Solanum lycopersicum (tomato, Solanaceae). Mite gall induced on Acnistus arboresens
(Solanaceae). Insect gall induced on Cissus fuliginea (Vitaceae) by an unknown diptera Cecidomyiidae and on Hirtella
racemosa (Chrysobalanaceae) by an unknown diptera Cecidomyiidae. Taxonomic identification of host plants of insect galls
was performed by Roberto Espinoza, and inductor insects were identified by Paul Hanson. Photo credit: taken from Patrick
Roper (bacteria crown gall), Omar Gätjens-Boniche (fungus gall, nematode gall, mite gall and insect galls).

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plant’s development by the inducing insect
(Ananthakrishnan, 1998; Raman, 2011; Oates,
Külheim, Myburg, Slippers, & Naidoo, 2015;
Agudelo et al., 2018). The degree to which
the insect manipulates the plant’s growth to
form the gall varies considerably and involves
changes ranging from the induction of cell
proliferation (Agudelo et al., 2018) to the for-
mation of a complex structure that the plant
does not produce under normal conditions.
Just like normal plant organs and structures,
galls induced by insects present anatomic and
histologic characteristics of their own, which
vary greatly in their diversity and degree of
complexity (Fig. 2) (Nyman & Julkunen, 2000;
Mani, 1992; Ananthakrishnan, 1998; Stone &
Schönrogge, 2003; Oliveira & Isaias, 2010;
Raman, 2011; Oliveira, Carneiro, Magalhães,
& Isaias, 2011; Oliveira et al., 2016). Tissues
near the inducing insect show cytological and
morphological changes that benefit its feed-
ing process and development. This tissue, also
known as “nutritive tissue”, commonly pres-
ents high concentrations of sugar (Nogueira et
al., 2018), lipids, proteins, nitrogen, and other
nutrients that provide a continuous source of
food for the insect and show intense phospha-
tase activity (Miles, 1968; Rohfritsch & Short-
house, 1982; Shorthouse & Rohfritsch, 1992;
Raman, 2011, Oliveira & Isaias, 2010; Oliveira
et al., 2011; Nabity, Haus, Berenbaum, &
Delucia, 2013; Huang et al., 2015; Oates et al.,
2016; Ferreira et al., 2017; Isaias et al., 2018).
Typical nutritive cells show a dense cytoplasm
with abundant cell organelles, fragmented vac-
uoles, a hypertrophied nucleus and nucleolus,
and dedifferentiated plastids clustered around
the nucleus, as well as chloroplasts modified
Fig. 2. Some plant galls from Costa Rican flora. A) Gall induced on Pisonia macranthocarpa (Nyctaginaceae) by an
unidentified insect species (Diptera, Cecidomyiidae). B) Gall induced on Vitis tiliifolia (Vitaceae) by an unidentified insect
species (Diptera, Cecidomyiidae). C) Gall induced on Hirtella racemosa (Chrysobalanaceae) by an unidentified insect
species (Diptera, Cecidomyiidae). D) Gall induced on Semialarium mexicanum (Hippocrateaceae) by an unknown inducer.
Taxonomic identification of the host plants was carried out by Roberto Espinoza, and the inductor insects were identified by
Paul Hanson. Photo credit: Omar Gätjens-Boniche (A, C, and D) and Gregorio Dauphin (B).

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to varying degrees and modified cell walls
(Shorthouse & Rohfritsch, 1992; Raman, 2011;
Carneiro & Isaias, 2015). Ferreira et al. (2017)
compared six gall systems with different levels
of structural complexity (aphids, mites, and
Nematoda), using histometric and histochemi-
cal analyses. Based on the types of storage
tissue, the authors proposed a classification of
three types of storage tissues: typical nutritive
tissues (TNT), common storage tissues (CST),
and nutritive-like tissues (NLT). TNT and NLT
present cells with a dense cytoplasm and a large
nucleus; TNT serve as a direct food source for
gall inducers. CST have vacuolated cells, and
may store starch and other types of energy-rich
molecules, as do the cells of NLT. Likewise,
several studies have demonstrated that insects
generally feed on a reduced area of the gall
(Nyman & Julkunen, 2000).
The inducing insect can modify the expres-
sion of genes within restricted areas of the host
plant, thereby producing new developmental
events in the tissues under its influence. Gall
morphogenesis occurs in a relatively short
time; however, this fact apparently does not
influence the complexity observed in such mor-
phological entities (Ananthakrishnan, 1998,
Nabity et al., 2013; Oates et al., 2015).
In many kinds of abnormal growth or
deviation from normal organismal develop-
ment, there are alterations in the mechanisms
that regulate cell proliferation and differentia-
tion. Within this context, “crown galls” induced
by the genus Agrobacterium are an example of
structures formed due to the proliferation of
cells with a low level of differentiation; hence,
they are considered the simplest and least
derived plant gall within the wide variety of
these structures found in Nature. On the other
hand, galls induced by insects are very well-
organized structures showing different degrees
of differentiation, the reason why they are
considered as the most complex and derived
structures. Nonetheless, in spite of the clear dif-
ferences between these two extremely diverse
groups of plant galls, they show important
similarities. For instance, both systems require
a previous state of “conditioning” towards
the development of the structure. In the case
of insect galls, the “conditioner” is the insect
itself, which modulates the tissue that will
form the structure through mechanical action
and the secretion of chemical substances. In
crown galls the conditioning factor is given by
a series of metabolic events prior to the genetic
transformation of plant cells by the bacterium
(Rohfritsch & Shorthouse, 1982; Davey et al.,
1994; Piñol, Palazón, Cusidó & Serrano, 1996;
Valentine, 2003; Suzuki et al., 2015).
In a similar manner as in so-called “tumor
cells” of crown galls, cells from insect-induced
galls acquire a certain autonomy and indepen-
dence from their normal tissue development
pattern. From the induction process, cell devel-
opment is redirected due to the influence of
the inducing stimulus. However, unlike insect
galls, crown galls have an unlimited capacity to
grow without a defined pattern of development.
After the initial stimulus, cell proliferation in
both systems develops in a different way; in
the case of bacteria-induced crown galls, cell
proliferation occurs in an uncontrolled way
and does not require the continuous presence
of bacteria once the process is initiated. In con-
trast, for adequate and complete development
of galls induced by insects, in general, the con-
tinuous, active presence of the insect is required
(Rohfritsch & Shorthouse, 1982; Davey et al.,
1994; Valentine, 2003; Suzuki et al., 2015).
According to Rohfritsch & Shorthouse
(1992), Arduin & Kraus (1995), and Sá et al.
(2009), plant galls present four basic stages
of development, but significant differences
between gall inducers can occur. These stages
of development involve the processes of ini-
tiation, growth and differentiation, maturation,
and finally, dehiscence (Fig. 3). The state of
growth and development is a continuous pro-
cess of cell division and differentiation that
generally depends on the feeding activity of the
larva, which in turn is mainly responsible for
molding the shape of the gall’s inner chamber.
After the nutritive tissue is formed around the
inner chamber, a mass of cells binds the vas-
cular tissue of the gall to the plant. Frequently,
sclerenchymatous tissue is also formed around

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the inner chamber and near the vascular tis-
sue of the gall, which causes its separation
into internal and external regions. The inter-
nal region is considered to be influenced by
the activity of the larva, whereas the external
region or outer cortex of the gall is under the
influence of the plant. The opening and dehis-
cence of galls occurs towards the end of the
maturation stage and represents the period of
greatest chemical and physiological change
in the tissues that comprise it. Not only has it
been demonstrated that the meristematic tissues
react to the stimuli but also that young stems of
various species of plants can be stimulated and
modified to make these structures.
Shorthouse & Rohfritsch (1992) separate
the morphogenesis of galls induced by insects
into two processes. The first is a permanent
effect, which remains even when the corre-
sponding insect is removed or dies. A second
process implies that the effect is generated
through continuous stimulation by the induc-
ing insect, which disappears if the insect is
removed from the gall or if it dies.
Several authors have tried to classify galls
according to a series of morphological criteria
that have, in spite of being arbitrary, estab-
lished the groundwork for the development
of a great number of studies. Shorthouse &
Rohfritsch (1992) and Williams (1994) dis-
tinguished two basic types of galls: organoids
and histoids. The first one results from organ
proliferation or modification, maintaining the
basic organ structure. Histoid galls, in contrast,
originate from the proliferation of modified
cells leading to the formation of new tis-
sue. Plant galls are also classified according
to more strict morphological criteria. Galls
called “kataplasmic” are irregular in size and
shape, presenting an irregular growth pattern
Fig. 3. General scheme for the life cycle of insect-induced galls. This figure is based on the gall induced by the Cecidomyiidae
Latrophobia brasiliensis in Manihot esculenta Crantz (Cassava). The scheme was synthesized from the reviewed literature.
Photo credit: Omar Gätjens-Boniche.

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with little differentiation in their tissues. On
the other hand, “prosoplasmic” galls are more
complex and differentiated and are formed as
a result of the formation of a new structure
(Miles, 1968; Williams, 1994). Nonetheless, it
is important to emphasize that any attempt at
classification turns into a difficult task, mainly
because of the great quantity of existing inter-
mediate states and shapes among the different
gall morphotypes. Therefore, the shape and
structure of galls depends on a large number
of factors, including the species to which the
host plants belong, the species of the inducing
insects, the type of organ attacked, the state of
development of the plant and, in some cases,
even the sex of the insect. According to Raman
(2011), about 90 % of all the known galls show
bilateral or radial symmetry. As reported by
the same authors, in the specific case of galls
formed by insects belonging to the families
of Cecidomyiidae (Diptera) and Cynipidae
(Hymenoptera), they show surprising levels of
radial symmetry. Moreover, some factors that
affect gall size include the number of larvae
present, the structural diversity of the galls, the
percentage of tissue infected, the physiological
state of the host plant, environmental condi-
tions, and the genotype of the plant (Mani,
1992; Ananthakrishnan, 1998; Stone & Schön-
rogge, 2003; Raman, 2011).
Some galls are simply “swellings”—undif-
ferentiated cell masses or those with a low
level of differentiation, while others show a
surprisingly high degree of differentiation,
organization and specialization within their
cells and tissues, frequently with characteristics
exclusively associated with the gall from which
they originate. Based on the above, this last
type of gall, called “prosoplasmic”, presents an
anatomy and histology very characteristic of
its own. Prosoplasmic galls induced by some
families of insects are, due to their high degree
of complexity and organization, the ones that
generate a higher interest (Mani, 1992).
The order Hymenoptera includes the most
complex and organized galls described so
far for the Class Insecta. In this group, gall-
inducing insects are classified in the Suborder
Symphyta, family Tenthredinidae and the
Suborder Apocrita, with two Superfamilies:
Chalcidoidea, which includes the families
Pteromalidae, Eurytomidae, and Agaonidae
and the superfamily Cynipoidea, represented
by the family Cynipidae. Gall-inducing Hyme-
noptera species present a wide distribution over
several areas of the planet and can be found in
various groups of dicotyledonous plants and
even in monocotyledonous plants, especially in
gramineous species (Shorthouse & Rohfritsch,
1992). According to Rohfritsch & Shorthouse
(1982) and Shorthouse & Rohfritsch (1992),
Cynipidae contains the main gall inducers of
the order Hymenoptera, and they can cause
the development of different kinds of galls in
distinct organs of the plant. Most representa-
tives of this family induce the formation of
galls in leaves, sprouts, stems, and roots.
Females lay eggs on the surface of the tissue,
and the egg itself induces an initial gall, even
though the larvae of these insects are the main
inducing agents of these structures. Cynipidae
eggs have a lytic effect on the cells that sur-
round them, which leads to the formation of a
chamber that protects the young larva. Larvae
have mouth structures that allow them to break
the plant cell wall to suck on the contents of
the nutritive cells. Many species of Cynip-
ids are characterized by complex life cycles,
commonly accompanied by an alternation of
generations. Individuals of both generations
can attack the same organ or different types of
organs in the plant, resulting in the formation
of radically different galls, and in some cases,
even the individuals of the two generations are
morphologically different. The surface of the
galls formed by the Cynipids can be coated by
trichomes, scales, thorns, or other types of out-
growths. Nevertheless, one of the most impor-
tant characteristics of these structures is the
formation of concentric areas of differentiation
and an area of sclerenchymatous cells around
the larval chamber.
The order Diptera grouped in the subor-
der Nematocera, which includes the family
Cecidomyiidae (gall midges), and the suborder
Brachycera, which includes Tephritidae (fruit

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flies) and Agromyzidae. Gall inducers belong-
ing to this order present a broad global dis-
tribution, and in contrast to other orders of
gall- inducing insects, they can also be found in
monocotyledonous plants, especially grasses.
Nonetheless, the majority of arthropod-induced
galls occur on dicotyledons, and at least 66
% of the dicotyledon families harbor galls
(Shorthouse & Rohfritsch, 1992; Hanson &
Gómez-Laurito, 2005). Hanson & Gómez-
Laurito (2005) suggested that possibly more
than 90 % of dicotyledon species in all major
biogeographic regions harbor gall-inducing by
cecidomyiids. Around 80 % of plant galls
induced by insects from the Neotropical region
are induced by the Cecidomyiidae family, and
new species of inducing insects belonging
to this family are constantly being described
around the world. Moreover, according to Han-
son & Gómez-Laurito (2005), about 70 % of
the gall-inducing arthropods in Costa Rica are
Cecidomyiidae.
Galls formed by Diptera, especially those
induced by individuals of the family Cecido-
myiidae, are characterized by a high degree
of tissue differentiation; on the other hand, the
insects are characterized by the complexity of
their life cycles. Another important character-
istic present in gall-inducing Diptera species is
their capacity to pupate inside the gall. In the
family Cecidomyiidae only the larvae have the
capacity to induce galls; these have a poorly
developed mouth structure and feed by sucking
on fluids exuded from the gall cells, without
causing any damage or necrosis (Rohfritsch &
Shorthouse, 1982; Shorthouse & Rohfritsch,
1992). In those galls, nutritive tissue is present
throughout the development of the structure. At
the same time, for the development and main-
tenance of nutritive tissue, the active presence
of the larva of the inducing insect is necessary
(Ananthakrishnan, 1998).
Galls induced by the orders Thysanop-
tera and Hemiptera appear as small bumps or
abnormal growths, whose tissues are essential-
ly made of parenchymatous cells. Some species
can also cause a leaf roll accompanied by cellu-
lar hypertrophy. In the case of the hemipterans,
they induce a variety galls types, which vary
from simple forms to very sophisticated com-
plex structures. Several species of coleopteran
gall-inducing larvae produce tunnels in differ-
ent parts of the plants, and the eggs are placed
in the interior of cavities prepared by insect
females. Although plant galls induced by Cole-
optera have been described as characterized
by the absence of nutritive tissue (Shorthouse
& Rohfritsch, 1992), there are descriptions
detailing the presence of this type of tissue
or nutritive-like tissue in coleopteran galls
(Raman et al., 2007; Barnewall & De Clerck-
Floate, 2012). Nevertheless, little is known
about gall-inducing Coleoptera, especially in
tropical ecosystems (Korotyaev, Konstanti-
nov, Lingafelter, Mandelshtam, & Volkovitsh,
2005). Many galls formed by Lepidoptera do
not develop nutritive tissue, and larvae of these
insects are fed by chewing the tissue that sur-
rounds the internal chamber, producing a large
amount of detritus (Rohfritsch & Shorthouse,
1982; Shorthouse & Rohfritsch, 1992). Howev-
er, recent studies on lepidopteran-induced galls
suggest that these structures may also present
nutritive tissue and are not as simple as they
have traditionally been described. For example,
a true nutritive tissue that showed metabolite
concentration gradients, which seem to be spe-
cific for lepidopteran galls, was described by
Ferreira & Isaias (2013). Nutritive tissue was
described in Bauhinia ungulata L. (Fabaceae)
by Bedetti, Ferreira, de Castro, and dos Santos
Isaias (2013). Moreover, nutritive cells in the
galls induced on the leaves of Tibouchina pul-
chra (Cham.) Cogn. (Melastomataceae) have a
large amount of rough endoplasmic reticulum,
ribosomes, polyribosomes, and mitochondria,
which are evidence of the high metabolic status
of these cells. Likewise, vascular cambium-
like, with high protein synthesis and lipid stor-
age, are characteristic of that nutritious tissue.
The nutritive cells are stimulated by the activity
of galling larvae, consequently generating a
new tissue type (Vecchi, Menezes, Oliveira,
Ferreira, & Isaias, 2013).

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The induction mechanism of plant galls
by insects: What do we know?
The capacity of a large number of insects
to form galls in different groups of plants has
motivated a great deal of research with the aim
of elucidating the mechanism of induction of
this type of structure. Hori (1992) describes
four main hypotheses that could explain the
formation of plant galls. The first of these
hypotheses suggests the injection of a fluid
from the insect during the oviposition process,
which would mediate gall induction. A second
hypothesis proposes that gall formation is the
result of mechanical irritation due to the pres-
ence of a foreign body on the plant tissue. An
extension of this hypothesis suggests that galls
are induced at a “reactive site” with particular
traits of available meristematic regions by the
action of the inductor insect, probably in stem
cell areas (Weis, Waltonanand, & Crego, 1988;
Abrahamson & Weis, 1997; Espírito-Santo,
Neves, Andrade-Neto, & Fernandes, 2007;
Silvia & Connor, 2017). The third hypothesis
proposes that the formation of galls is induced
by the secretion of active components from the
saliva of the insect. Finally, a fourth hypothesis
purports that the formation of galls is medi-
ated by the excretion of metabolic products
from the insect.
For simplicity, the morphogenic process of
plant gall induction by insects can be divided
into three main phases. The first one involves
“conditioning” of the cells of the corresponding
plant tissue by the insect, to make them more
susceptible and suited to its action as induc-
tor. In the following phase, induction of the
gall as such takes place, whereby cell division
and elongation results in the formation of a
“primary” gall. The final phase consists of gall
maturation, in which the primary gall grows
to complete its morphogenesis (Shorthouse &
Rohfritsch, 1992; Raman, 2011).
As mentioned above, in the plant gall
induction process, plant cells should be con-
ditioned to produce a particular physiological
state (Raman, 2011). In this respect, different
studies have mentioned that the amino acids
present in the salivary secretions of gall-induc-
ing insects, essentially lysine, histidine, and
tryptophan, could function as “precondition-
ers” for gall induction. It seems that these
amino acids could cause major plasticity and
would increase the sensitivity of the plant tis-
sue to the action of the corresponding induc-
ing insect. Although the presence of pectinase
in the saliva of insects has not been corre-
lated with gall induction, such enzymes could
degrade the cell walls and in turn contribute
to tissue preconditioning to the action of the
insect. Likewise, it has been speculated that
polyphenol oxidase (PPO), also present in the
saliva secretions of insects and the phenolic
compounds derived from its enzymatic action,
could increase plant tissue sensitivity to the
stimulus of the inductor insect. It has also been
suggested that the complex interaction between
the host plant tissue and polyphenol oxidase
might be of fundamental value in gall forma-
tion (Miles, 1968; Hori, 1992; Ananthakrish-
nan, 1998; Saltzmann, Giovanini, Zheng, &
Williams, 2008). In this respect, Miles (1968)
indicated that interactions and the balance
between insect polyphenol oxidase and the host
plant could determine whether the “attack” of
an insect causes injury (necrosis) or gall devel-
opment. Moreover, the modulation of redox
potential has been related to gall initiation and
establishment, especially concerning the accu-
mulation of reactive oxygen species (Isaias,
Oliveira, Moreira, Soares, & Carneiro, 2015).
Different studies have reported that indole-
acetic acid (IAA) could be a powerful gall-
inducing agent, and it has also been speculated
that this compound could interact with other
plant growth regulators, like cytokinins and
gibberellins, or in a synergistic way with other
chemical substances, to promote the induction
and maturation of these structures (McCalla,
Genthe, & Hovanitz, 1961; Miles, 1968; Hori,
1992; Leitch, 1994; Ananthakrishnan, 1998;
Mapes & Davies, 2001; Stone & Schönrogge,
2003; Raman, 2011, Tooker, & Helms, 2014;
Bartlett & Connor, 2014; Bedetti, Modolo,
& dos Santos, 2014; Bailey, Percy, Hefer, &
Cronk, 2015). However, the mechanism of

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action through which these substances act to
promote the development of plant galls is very
poorly understood and is currently a subject
of discussion. This scenario becomes more
complicated in the case of prosoplasmic galls,
like the ones formed by insects of the Cecido-
myiidae and Cynipidae families, because of the
complexity of their development and structure.
Symbiotic relationships between gall-
inducing insects and microorganisms have
been hypothesized to be involved in plant
gall development (Hansen & Moran, 2014;
Tooker and Helms, 2014). Several studies
have demonstrated the presence of a great
number of endosymbiotic bacteria in different
insect groups (Degnan, Lazarus, & Werne-
green, 2005; Kikuchi, Meng & Fukatsu, 2005;
Delmotte, Rispe, Schaber, Silva, & Moya,
2006; Fukatsu et al., 2007; Jaenike, Polak,
Fiskin, Helou, & Minhas, 2007; Goto, Anbutsu,
& Fukutsa, 2006; Xi, Gavotte, Xie, & Dobson,
2008; Toft, Williams, & Fares, 2009; Gutz-
willer, Dedeine, Káiser, & Giron, 2015; Kraw-
czyk, Szymańczyk, & Obrępalska-Stęplowska,
2015; El-Sayed & Ibrahim, 2015; Campbell et
al., 2015), as well as bacteriocytes (Nikoh &
Nakabachi, 2009; Braendle et al., 2009). Some
of these symbiont microorganisms are mutu-
alistic and contribute to the viability of their
hosts, while others are parasites, which tend
to affect their corresponding hosts in a nega-
tive way. Insect-associated microorganisms
could be important mediators of interactions
between insects and plants (Sugio, Dubreuil,
Giron, & Simon, 2015; Hammer & Bowers,
2015, Wielkopolan & Obrępalska-Stęplowska,
2016). Some researchers have reported that
simultaneous infection with different species of
endosymbionts in the same host organism is a
common phenomenon in several insect groups
(Thao et al., 2000; Thao, Gullan, & Baumann,
2002; Russell et al., 2003; Ishii, Matsuura,
Kakizawa, Nikoh, & Fukatsu, 2013; Krawc-
zyk et al., 2015; El-Sayed et al., 2015; Ghosh,
Bouvaine, & Maruthi, 2015; Brentassi et al.,
2017). Different tissues in the body of the same
host constitute different microenvironments
for endosymbiont organisms. Some tissues
could be, for instance, nutritionally favorable,
immunotolerant, or simply easy to colonize
(Mouton, Henri, Bouletreau, & Vavre, 2003;
Kondo, Shimada, & Fukatsu, 2005; Koga,
Meng, Tsuchida, & Fukatsu, 2012; Hansen &
Moran, 2014; Sugio et al., 2015).
In recent years, a growing interest has
emerged regarding the reproductive biology
of endosymbiont parasites that are transmitted
through the mother and manipulate the repro-
duction of their host organism. Accumulated
evidence shows that many species of arthropod
are infected by different kinds endosymbiont
organisms transmitted from the mother through
vertical transmission, which have a great influ-
ence on the biology of their hosts. Some of
these endosymbiont microorganisms include
Wolbachia, Spiroplasma, Rickettsia, Arseno-
phonus, and Cardinium, among others (Weeks,
Velten & Stouthamer, 2003; Zchori-Fein &
Perlman, 2004; Goto et al., 2006; Casper-
Lindley et al., 2011; Goodacre & Martin, 2012;
Kageyama, Narita, & Watanabe, 2012; Koga et
al., 2012; Kremer et al., 2012; Herren, Paredes,
Schüpfer, & Lemaitre, 2013; Ma, Vavre & Beu-
keboom, 2014; Boivin et al., 2014; Ma et al.,
2015; Sugio et al., 2015; Brentassi et al., 2017;
Mariño, Verle Rodrigues, & Bayman, 2017; Ma
& Schwander, 2017).
Many galling insects are known to have
microbial associates that may be involved in
gall development or could facilitate herbivory,
such as Ambrosia gall midges associated with
fungal symbionts, but studies exploring the
role of microbial associates in the lifecycles
of insect gallers are scarce (Hansen & Moran,
2014; Tooker & Helms, 2014; Huang et al.,
2015). Bacteria of the genus Wolbachia have
been associated with green-island formation
by the apple leaf-mining moth Phyllonorycter
blancardella, a similar phenomenon to the one
observed in some types of plant galls induced
by insects (Kaiser, Huguet, Casas, Commin,
& Giron, 2010; Gutzwiller et al., 2015). Their
results suggest that bacteria impact green-
island induction by manipulating cytokinin
levels. In addition, secretions of phytohor-
mones, such as cytokinins, by endosymbiotic

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microorganisms have also been associated with
the plant–galling insect interaction (Spíchal,
2012). Likewise, Bartlett and Connor (2014)
hypothesized that the inducing insects obtained
their ability to induce galls via endosymbiotic
microbes, which have acquired the biosynthetic
pathways to produce IAA and trans-zeatin fam-
ily cytokinins from plants. It is not surprising
then that the control of cytokinins constitutes
an important selection factor for arthropods and
pathogens because of the importance of these
phytohormones in the regulation of plant mor-
phology, senescence, and defense, especially
with regard to the mobilization of nutrients in
each of these processes (Giron, Frago, Gleva-
rec, Pieterse, & Dicke, 2013; Tooker & Helms,
2014; Naseem, Wölfling, & Dandekar, 2014;
Giron et al., 2016).
It has been proposed that galling insects
acquired genes from symbiotic microorgan-
isms through horizontal gene transfer (Giron
& Glevarec, 2014; Bartlett & Connor, 2014).
Horizontal gene transfer (HGT) is the move-
ment and transference of genetic informa-
tion between different organisms, and it is a
common phenomenon between pathogens of
animals and plants, and between symbionts
and pathogens (De la Cruz & Davies, 2000;
Suzuki et al., 2015). Indirect evidence sup-
porting the previous hypothesis is provided by
works such as those carried out by Nikoh et al.
(2008). Molecular analyses performed by these
authors in Wolbachia, one of the most abundant
intracellular bacteria described in arthropods,
as well as nematodes, suggested that approxi-
mately 30 % of Wolbachia genes are present
in the nuclear genome of host insects. In this
study, through fluorescence in situ hybridiza-
tion techniques, they located the transferred
genes of Wolbachia in the proximal region of
the short arm of the insect X chromosome.
The collected evidence indicated that this pro-
cess of horizontal gene transfer was probably
generated from an individual event. In another
study, it was determined that the genome of
Wolbachia pipientis contains high levels of
repetitive sequences of DNA and also mobile
genetic elements (Wu et al., 2004). In spite of
its wide distribution and the effects of Wolba-
chia on the biology of its hosts, little is known
about the molecular mechanisms that mediate
the interaction between this bacterium and its
invertebrate hosts (Wu et al., 2004; Chrostek &
Teixeira, 2015).
Therefore, under the previous scenario,
horizontal gene transfer (HGT) could play a
fundamental roll in plant gall induction and
evolution. In recent years, more evidence has
shown that the molecular mechanisms involved
in the different processes of symbiosis and
pathogenesis present a series of common path-
ways which have revealed existing similarities
in the modulation and interactions between
pathogens and symbionts with their hosts (De
la Cruz & Davies, 2000; Hentschel, Steiner, &
Hacker, 2000; Rankin, Rocha, & Brown, 2011;
Suzuki et al., 2015). Furthermore, the informa-
tion generated by microbial genome sequenc-
ing studies has demonstrated that horizontal
transference of genes is an important process
and widely distributed within the evolution-
ary scenario of prokaryote organisms (Nikoh
& Nakabachi, 2009; Jayaprakashvel, Bhrathi,
Muthezhilan, & Hussain, 2017).
In addition to chromosomes, prokary-
otes possess mobile genetic elements, such as
genomic islands, plasmids, transposons, inser-
tion sequences or bacteriophages, which allow
them to induce structural and physiological
changes, as well as the acquisition or loss of
genomic regions. Moreover, the fact that a great
number of pathogenic and symbiotic determi-
nants are located in mobile genetic elements
allows a source of permanent variation to be
generated within these organisms. In addition,
some authors have suggested that the acquisi-
tion and incorporation of plasmids into bacteria
could constitute a key process to the adaption
of these microorganisms to new ecological
niches and to their development as symbionts
or pathogens (Vivian, Murillo, & Jackson,
2001; Suzuki et al., 2015; Jayaprakashvel et
al., 2017). Genetic variability plays a very
important role by generating the conditions that
allow the evolution of new types of interactions
among organisms, thus HGT between different

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species could represent a powerful mechanism
through which the final result of the interaction
between a pathogen or symbiont and its host
could be altered permanently (Hentschel et al.,
2000; Suzuki et al., 2015; von Wintersdorff et
al., 2016; Porse, Schou, Munck, Ellabaan, &
Sommer, 2018).
Not only is HGT responsible for speciation
and subspeciation in bacteria; it also constitutes
an important mechanism in eukaryote organ-
isms. There are sufficient information related
to the role of conjugation processes in the
transference of genetic information from bac-
teria to eukaryote cells. Such eukaryote cells
include yeasts, filamentous fungi, and plant
cells (De la Cruz & Davies, 2000; Rankin et
al., 2011; Suzuki et al., 2015). For example,
the mechanism through which Agrobacterium
tumefaciens transfers genes from the bacterium
to plant cells is well known: it occurs through
the action of the T-DNA segment present in the
Ti plasmid (Suzuki et al., 2015). Stable natural
transgenic plants of sweet potato containing
Agrobacterium T-DNA sequences with their
foreign genes expressed at detectable levels in
different tissues were reported by Kyndt et al.
(2015). Likewise, the work of Diao, Freeling,
& Lisch (2006), provides evidence of HGT
through the transposons of superior plants.
In this regard, some bacteria, retroviruses,
and DNA viruses constantly integrate different
kinds of genetic elements into the chromosomes
of animal and plant cells through mechanisms
such as conjugation and transformation (De la
Cruz & Davies, 2000, Oliver et al., 2006; Klas-
son, Kambris, Cook, Walter, & Sinkins, 2009;
Nikoh & Nakabachi, 2009; Suzuki et al., 2015).
Moreover, the mechanism by which eukaryotes
acquire genes from distantly related organisms
remains obscure (Suzuki et al., 2015).
Although, in general terms, it has been
accepted that some kind of “chemical stimuli”
(very likely a phytohormone) from the insect is
involved in the induction and morphogenesis
of galls (McCalla et al., 1961; Miles, 1968;
Rohfritsch & Shorthouse, 1982; Hori, 1992;
Leitch, 1994; Ananthakrishnan, 1998; Raman,
2011; Yamaguchi et al., 2012; Connor et al.,
2012; Erb, Meldau & Howe, 2012; Giron et
al., 2013, Tooker & Helms, 2014; Bailey et al.,
2015; Oates et al., 2016, Giron et al., 2016), up
to now it has not been possible to determine
with certainty whether insects could synthe-
size phytohormones. However, Yamaguchi et
al. (2012) found abnormally high concentra-
tions of a type of zeatine in the glands of the
“sawfly” Pontania sp. (Hymenoptera, suborder
Symphyta) which, according to these research-
ers’ criteria could be strong evidence that
this insect can synthesize cytokinins as well
as IAA. Likewise, Shih, Lin, Huang, Sung,
and Yang (2018) found evidence that gall
induction could be related to the secretion of
phytohormones like cytokinin and auxin, as
well as Brassinosteroids (steroids hormones),
from the inductor insect. In a similar direction,
Bartlett & Connor (2014) showed evidence
consistent with the hypothesis that exogenous
cytokinins, in combination with IAA from the
gall-inducing insect, lead to gall induction.
Additionally, Brütting et al. (2018) demonstrat-
ed, using 15N-isotope labeling, the transference
of the cytokinin N6-isopentenyladenine (IP)
from the free-living herbivore and non-galling
insect Tupiocoris notatus to Nicotiana attenu-
ata plants via their oral secretions.
On the other hand, the possibility of a
molecular induction mechanism in insect-
induced plant galls that involves the transfer-
ence of genetic elements has neither been
considered nor explored extensively. Cornell
(1983) suggested the possibility that the gall-
inducing insect could insert some genetic ele-
ments, mutualistic viroid, or virus into the plant
genome, which would regulate and control
the process of gall formation. However, this
author did not offer any evidence that could
support this statement. The molecular basis of
the induction of plant galls by insects is still
unknown (Stone & Schönrogge, 2003; Raman,
2011; Oates et al., 2016; Bailey et al., 2015;
Giron et al., 2016). Moreover, the physiologi-
cal nature of the stimuli given by the inducing
insect and the influence of its own genomic
constitution, as well as the reaction generated

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by the plant, are questions that remain com-
pletely open.
Stone & Schönrogge (2003) mentioned
three great problems or challenges in identify-
ing the molecules responsible for the process
of gall formation. First is the difficulty of
establishing an appropriate assay for the plant
tissues involved in the process of induction.
Second, the possible inducing molecules used
by insects could be chemically similar to those
normally present in the plant. Third, since it
is expected that the signals coming from the
insect generate a cascade of responses in the
plant, it would be very difficult to separate the
first morphogenetic impact originated by the
inductor from the secondary responses gener-
ated by the plant.
In the particular case of gall-inducing
insects belonging to Cecidomyiidae, it has been
reported that either the egg or the ovipositing
female could generate the initial stimulus and
that the larva, by secreting substances that
promote the growth of plant tissue under its
action, could cause the formation of the gall
(Hori, 1992).
Regarding the family Cynipidae (Hyme-
noptera), different studies have associated both
auxins and cytokinins with the processes of
gall induction and morphogenesis. Moreover,
the morphogenesis and induction of these
structures have been correlated with the activ-
ity of oviposition of the female, secretions of
the insect egg, and the activity and secretion
of chemical substances from the larva (Miles,
1968; Hori, 1992, Shorthouse & Rohfritsch,
1992; Raman, 2011). As with the galls formed
by insects from the family Cecidomyiidae, the
mechanism of morphogenesis of galls formed
by cynipids cannot be explained simply by
the action of plant phytohormones. Neverthe-
less, Boysen-Jensen (1952) and Miles (1968)
support the hypothesis of chemical induction,
arguing that the larva moves instinctively and
secretes regulatory substances in the proper
locations of the “attacked” tissue at specific
times, thereby generating a suitable environ-
ment that favors the development of the gall.
“Omics” is an informal term that refers
to fields of study in biology ending in -omics,
such as genomics, proteomics, or metabolo-
mics, among others. Emerging work conducted
with new omics technologies is expanding
our understanding of some relevant aspects
relating to plant gall induction and morpho-
genesis. In a recent paper regarding the iden-
tification of the galling effector repertoires
of the Hessian fly, it was shown that around
7 % of its genome encodes putative effector
proteins, which include the secreted salivary
gland protein (SSGP)-71, a known member
of an arthropod protein family (Zhao et al.,
2015). Moreover, these authors showed that
although SSGP-71 lacks sequence homology
with other proteins, its structure resembles both
ubiquitin E3 ligases from plants and E3-ligase-
mimicking effectors from plant pathogenic
bacteria. Protein analyses indicate that the
mature SSGP-71 protein contains a cyclin-like
F box domain near the N-terminus and a series
of leucine-rich repeats (LRRs). F box domains
are frequently associated with LRRs, and both
domains mediate protein-protein interactions,
according to Ho, Tsai, and Chien (2006). These
types of proteins are associated with the trans-
fer of ubiquitin to target proteins destined for
degradation in the proteasome. In addition,
they play essential roles in phytohormonal sig-
naling, plant development, and plant immunity.
Zhao et al. (2015) also proposed that SSGP-71
proteins are a novel class of F-box-LRR mim-
ics that enable the insect to hijack the plant
proteasome in order to directly produce nutri-
tive tissue and additionally defeat basal plant
immunity. These authors further propose that
their results prove that these effectors are the
agents responsible for arthropod-induced plant
gall formation. Likewise, Shih et al. (2018)
demonstrated, by using transcriptome analy-
sis, the modification of normal plant tissue to
form galls. Moreover, they indicated that the
manipulation of genes related to gall formation
might be induced by auxin, cytokinin, and even
steroid hormones (Brassinosteroids) secreted
by gallers of Hemiptera, Lepidoptera, and
Diptera. Similarly, other transcriptomic and

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genomic studies provide evidence leading to
altered gene expression in galled plant tissues.
These altered genes and effector proteins could
be involved in several aspects of gall insect
biology, including feeding, metabolic altera-
tions, suppression of defense responses, and
developmental manipulation of the host plant
tissue (Rawat, Neeraja, Nair, & Bentur, 2012;
Hearn, 2013). Even more interesting, Hearn
(2013) also determined that genes expressed
in gall wasp genomes encode plant-cell-wall-
degrading enzymes that could originate from
plant pathogenic bacteria. Pawłowski, Staszak,
Karolewski, and Giertych (2017), using a pro-
teomic approach to compare the galls induced
by three oak gall species, Cynips quercusfolii,
Cynips longiventris, and Neuroterus quercus-
baccarum, with non-gall plant tissue in the host
plant Quercus robur, described several proteins
that could potentially be related to plant gall
formation. On the other hand, for non-insect
galls, a transcriptomic approach by Olszak et
al. (2018) showed evidence that galls induced
by Plasmodiophora brassicae in Arabidopsis
reprogram critical steps of the host cell cycle.
That distortion leads to initial cell hyperplasia,
which increases the number of cells, followed
by overgrowth of cells colonized by the patho-
gen. The authors showed that P. brassicae
infection stimulates the formation of the E2Fa/
RBR1 complex and upregulation of MYB3R1,
MYB3R4, and A- and B-type cyclin expres-
sion. Those cell cycle factors were previously
described as important regulators of the G2-M
cell cycle checkpoint.
An interesting survey in nematode galls
(Meloidogyne incognita), using high through-
put sequencing for small non-coding RNAs,
identified siRNA clusters that were differential-
ly expressed in infected roots of Arabidopsis
thaliana. Those siRNAs were overrepresented
in infected tissue, with a size 23 - 24 nt, cor-
responding to heterochromatic siRNAs (hc-
siRNAs), which are known to regulate the
expression of transposons and probably genes
at the transcriptional level, by an RNA-direct-
ed DNA methylation (RdDM) pathway that
induces the silencing of transposable elements
(Medina et al., 2018).
Insect-induced plant galls
and phytochemistry
An interesting aspect of some plant galls
is the particular or even radical phytochemis-
try between these structures and normal plant
tissues. Research conducted on galls of dif-
ferent species of plants have revealed that the
composition and concentration of chemical
substances in these structures can differ from
those of other plant tissues and organs (Tooker
& de Moraes, 2008; Saltzmann et al., 2008;
Giron & Huguet, 2011; Huang et al., 2015;
Oates et al., 2015; Hall, Carrol, & Kitching,
2017; Kot, Jakubczyk, Karaś, & Złotek, 2017).
Tissues near the outside of the gall frequently
accumulate high levels of tannins and other
chemical compounds related to the process of
defense of the gall and, in consequence, of the
insect (Ananthakrishnan, 1998; Li et al., 2017;
Chen et al., 2018; Nogueira et al., 2018). A
study by Vereecke et al. (1997) revealed that
the chemical composition of ethanol and aque-
ous extracts of galls produced in the leaves
of Nicotiana tabacum differs drastically from
that of non-infected plant tissue extracts. It has
been reported that the concentrations of some
carbohydrates such as hemicellulose, xylose,
and arabinose increase during gall develop-
ment in the tree Zelcowa (Yeo, Chae, So, Lee,
& Sakurai, 1997). Other authors have also
reported differences in the concentrations of
certain secondary compounds as well as certain
types of phytohormones in plant gall tissue
(Kraus & Spiteller, 1997; Pinkwart, Diettrich,
& Luckner, 1998). Kot et al. (2017), Li et al.
(2017) and Hall et al. (2017) demonstrated that
galls induced by cynipid species and the wasp
Leptocybe invasa (Hymenoptera: Eulophidae),
respectively, contain high levels of phenolic
compounds compared with control tissues.
Moreover, increased production of waxes in
the gall induced by the insect Baccharopelma
spp. (Hemiptera: Psyllidae) in leaves of Bac-
charis spicata (Lam) Baill has been related

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to a protective function against desiccation by
Agudelo et al. (2018).
Several authors have reported high con-
centrations of certain nutritive substances in
gall tissues; some of those substances include
sugars, proteins, phosphates, lipids, and nitro-
gen compounds (Tooker et al., 2008; Giron
& Huguet, 2011; Huang et al., 2015; Li et
al., 2017). In contrast, some researchers have
described that galls can present low lev-
els of certain chemical compounds related
to the processes of plant defense, such as
some phenolic compounds (Price et al., 1986;
Agudelo et al., 2018).
Due to the fact that many galls present high
quantities of certain nutrients and low levels of
other chemical substances that are damaging
to insects, a hypothesis has been proposed
related to the galler being able to manipulate
the development of its host plant by generating
a tissue with a higher nutrient value (nutritional
hypothesis). Nevertheless, several studies con-
ducted with the goal of proving this hypoth-
esis revealed that the concentrations of certain
chemical compounds considered as defensive
in plants are higher in the gall tissues, which
is contrary to the above-mentioned hypothesis
and suggests the need for a reconsideration of
the same (Nyman & Julkunen, 2000).
Taking into consideration studies such as
the those carried out by Nyman & Julkunen
(2000), Tooker & De Moraes (2008), Tooker et
al. (2008), Giron & Huguet (2011), Huang et al.
(2015), Oates et al. (2015), Li et al. (2017), Kot
et al. (2017), Chen et al. (2018), and Agudelo
et al. (2018), comparing the chemical composi-
tion of galls with that of normal plant tissue, the
conclusion would be that gall-inducing insects
could control some the chemical properties of
these structures.
CONCLUSIONS AND PERSPECTIVES
Although the chemical induction hypoth-
esis has been accepted with some discretion
and questioning as the general mechanism of
plant gall induction, there are, so far, no related
studies on a putative induction mechanism
involving exogenous genetic elements in the
process of insect gall formation. Moreover, lit-
tle has been speculated in relation to this topic.
A possibility exists that the control of induction
and morphogenesis of insect galls could be
under strict genetic control, possibly mediated
by the insertion of mobile genetic elements
into the genome of plant gall cells. Likewise,
that process could be mediated by means of an
endosymbiotic bacteria from the insect. Thus,
due to the demonstrated ability of the inductor
to manipulate the process of morphogenesis in
insect galls, the galling insect should be able to
control the regulation and expression of those
exogenous insertion sequences at different
levels. Consequently, under this hypothetical
scenario, the insertion sequences would func-
tion as mediators of the molecular interaction
between animal and plant systems. Genes
contained in these possible insertion sequences
could be those related to the control of the host
cellular machinery and analogous phytohor-
mones genes to those present in the host plant,
among others. Virtually no work has been con-
ducted in this direction, probably because of
insufficient knowledge and the complexity of
insect-plant-gall system relationships.
On the other hand, if a relatively simpler
plant gall induced by Agrobacterium species
involves a complex interaction between the
inductor organism and its host plant, which is
mediated by the insertion of genetic elements
into the genome of the host cells, why is it
not then assumed that a similar or even more
complex mechanism exists for the induction
of more complex plant galls, which could also
be induced by the delivery of genetic elements
from the cecidogenic organism? We could also
rephrase the question as follows: is cellular
self-proliferation an essential requirement or
condition for the genetic transformation of
plant cells, as occurs in the case of “crown
galls” induced by Agrobacterium?
It is essential to conduct studies to under-
stand, at the molecular level, the mechanism
of induction and morphogenesis of plant galls
induced by insects, exploring the presence of
any possible symbiotic organism and some

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kind of external genetic element to the plant
gall cells, associated with any of the symbi-
onts. With this goal in mind, an appropriate
gall induction model system should be chosen.
The choice of an insect–plant gall system to
be used as an experimental model should take
into account gall diversity and morphologic
complexity in order to include, in the same
plant species, prosoplasmic and kataplasmic
gall types. The next step would be to compare
the similarities and differences at the molecular
level, among different kinds of galls and how
these could affect the extraordinary morpholo-
gy and diversity observed in nature. Due to the
diversity of shapes, colors, and complex struc-
tures displayed by insect galls, these systems
could constitute ideal models to study how
form and structure are determined at the molec-
ular level in biological systems, more specifi-
cally, taking as a parameter plant morphology.
Due to their physiological and biochemi-
cal particularities, the identification of chemi-
cal substances or even specific genes in plant
galls that could be of interest or have practical
applications, according to the genetic transfor-
mation hypothesis postulated in this article,
could result in these tissues becoming real
germplasm sources, which may have a great
impact on conservation policies and offer a
promising background for the development of
applied biotechnologies. Considering all the
above information, it is clear that plant galls
represent an important germplasm sink and a
promissory gene bank that should be explored,
used, and preserved as an authentic treasure of
our biodiversity.
RESUMEN
El mecanismo de inducción de agallas de plantas
por insectos: revelando claves, hechos y consecuencias
en una interacción compleja entre reinos. Las agallas
se definen como modificaciones del diseño y desarrollo
normal de las plantas debido a una reacción específica a
la presencia y actividad de un organismo foráneo. Aunque
diferentes grupos de organismos tienen la habilidad de
inducir agallas en plantas, las agallas inducidas por insectos
son las más elaboradas y diversas. Algunas hipótesis han
sido propuestas para explicar el mecanismo de inducción
de las agallas de insectos. La hipótesis más general sugiere
que la formación de las agallas es disparada por la acción
de sustancias químicas secretadas por el insecto inductor,
incluyendo reguladores de plantas como auxinas, cito-
quininas, ácido-3-indolacético (AIA) o bien otros tipos
de compuestos. No obstante, el modo de acción de estas
sustancias químicas y el mecanismo general por medio del
cual el insecto podría controlar y manipular el desarrollo y
fisiología de la planta es aún desconocido. Más aún, como
resultado de la complejidad del proceso de inducción y
desarrollo de las agallas de plantas inducidas por insectos,
la hipótesis química es una explicación insuficiente e
incompleta en relación con el mecanismo de inducción y
morfogénesis de estas estructuras. Previas y nuevas evi-
dencias relacionadas con el sistema de agallas de insectos,
con énfasis en el proceso de inducción, fueron analizadas
desde un punto de vista integral del autor para proponer en
este artículo una perspectiva diferente sobre la inducción
de este tipo de estructuras. Debido a la extraordinaria diver-
sidad de formas, colores y estructuras complejas presentes
en las agallas de insectos, las mismas constituyen modelos
útiles para estudiar cómo la forma y la estructura son
determinadas a nivel molecular en los sistemas vegetales.
Además, las agallas de plantas son un importante origen de
material para el estudio y exploración de nuevas sustancias
químicas de interés humano, debido a las características
fisiológicas y adaptativas que presentan. Considerando el
control fino del proceso de morfogénesis, regulación bio-
química y complejidad estructural de las agallas de insec-
tos, se propone que un mecanismo de inducción mediado
por la inserción de elementos genéticos exógenos dentro
del genoma de las células de la planta que forman la agalla
podría estar involucrado en la formación de este tipo de
estructuras, vía una bacteria endosimbiótica.
Palabras clave: agallas de insectos, insecto inductor,
mecanismo de inducción, morfogénesis vegetal, efectores.
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