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Desnitskiy, A.G.; Chetverikov, P.E.; Ivanova, L.A.; Kuzmin, I.V.; Ozman-Sullivan, S.K.; Sukhareva, S.I. Gall Formation Induced by Mites and Insects. Encyclopedia. Available online: (accessed on 10 December 2023).
Desnitskiy AG, Chetverikov PE, Ivanova LA, Kuzmin IV, Ozman-Sullivan SK, Sukhareva SI. Gall Formation Induced by Mites and Insects. Encyclopedia. Available at: Accessed December 10, 2023.
Desnitskiy, Alexey G., Philipp E. Chetverikov, Larissa A. Ivanova, Igor V. Kuzmin, Sebahat K. Ozman-Sullivan, Sogdiana I. Sukhareva. "Gall Formation Induced by Mites and Insects" Encyclopedia, (accessed December 10, 2023).
Desnitskiy, A.G., Chetverikov, P.E., Ivanova, L.A., Kuzmin, I.V., Ozman-Sullivan, S.K., & Sukhareva, S.I.(2023, June 13). Gall Formation Induced by Mites and Insects. In Encyclopedia.
Desnitskiy, Alexey G., et al. "Gall Formation Induced by Mites and Insects." Encyclopedia. Web. 13 June, 2023.
Gall Formation Induced by Mites and Insects

Publications on gall formation induced on the leaves of dicotyledonous flowering plants by eriophyoid mites (Eriophyoidea) and representatives of four insect orders (Diptera, Hemiptera, Hymenoptera, Lepidoptera) are analyzed. Cellular and molecular level data on the stimuli that induce and sustain the development of both mite and insect galls, the expression of host plant genes during gallogenesis, and the effects of these galling arthropods on photosynthesis are considered. A hypothesis is proposed for the relationship between the size of galls and the volume of secretions injected by a parasite. Multistep, varying patterns of plant gene expression and accompanying histo-morphological changes in the transformed gall tissues are apparent. The main obstacle to better elucidating the nature of the induction of gallogenesis is the impossibility of collecting a sufficient amount of saliva for analysis, which is especially important in the case of microscopic eriophyoids. The use of modern omics technologies at the organismal level has revealed a spectrum of genetic mechanisms of gall formation at the molecular level but has not yet answered the questions regarding the nature of gall-inducing agents and the features of events occurring in plant cells at the very beginning of gall growth.

:eriophyoid mites tenuipalpids galling arthropods gene expression

1. Introduction

Among the herbivorous arthropods, there are a considerable number of species from six orders of insects (Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Thysanoptera), and acariform mites (Eriophyoidea: Eriophyidae, Phytoptidae, and Tetranychoidea: Tenuipalpidae), that induce the growth of galls or cecidia—specialized structures that develop on various organs of flowering plants, especially leaves. Galls develop from the tissues of the host plant and provide the phytophagous parasites inside them with nutrition and protection from predators and adverse external conditions. The estimated total number of galling insect species ranges from 13,000 to 211,000 [1][2][3]. In addition, more than 500 mite species cause gall formation [4]. The ability to induce gall formation in different phylogenetic lineages of flowering plants has arisen independently and numerous times in different phylogenetic lineages of arthropods [5][6][7][8][9]. Historically, the majority of research in this area concerns insect galls, whereas gall induction by mites has drawn much less attention. Despite the very intensive experimental study of arthropod galls [3][10][11][12][13][14], the molecular mechanisms of their formation are not fully understood yet. This can be explained in part by the fact that there is no universal model system for studying gall induction under natural conditions.

2. Functional Diversity of Leaf Galls Induced by Arthropods

Leaf galls on flowering plants are highly diverse in appearance, shape and color (Figure 1). Many attempts have been made to classify galls induced by both eriophyoid mites, e.g., [15][16] and insects, e.g., [17][18][19]. No general theory explains the variability of the leaf galls induced by arthropods. The classification of galls could play an important role in defining the general patterns of the molecular mechanisms of arthropod gallogenesis.
Figure 1. Examples of leaf galls induced by eriophyoid mites (A,B) and gall wasps (C), and a generalized diagram of an arthropod leaf gall with an internal chamber (D). (A)—galls of the mite, Fragariocoptes setiger (Nalepa, 1894), on green strawberry, Fragaria viridis (Weston, 1771); (B)—galls of the mite, Eriophyes padi (Nalepa, 1889), on bird cherry (Prunus padus L., 1753); (C)—galls of the oak gall wasp, Cynips quercusfolii (L., 1758), on petiolate oak (Quercus robur L., 1753). The scale bar represents 5 mm (A,B) and 10 mm (C). Designations: a—abaxial epidermis of the gall, b—transformed mesophyll of the gall, c—typical nutritive tissue, d—conductive bundles of the gall, e—gall chamber, f—normal abaxial leaf epidermis, g—normal leaf mesophyll, h—normal adaxial leaf epidermis.
There is an important similarity in gallogenesis in the eriophyoid mites (superfamily Eriophyoidea, Acariformes), flies of the family Cecidomyiidae (Diptera), wasps of the family Cynipidae (Hymenoptera) and many butterflies (Lepidoptera). During the galling process, stimulation due to parasite feeding causes the formation of typical nutritive tissue rich in carbohydrates, proteins and/or lipids. It lines the gall chambers and serves as a direct food source for the insect and mite parasites inside [8][20]. Hesse [21][22] studied leaf galls in 60 parasite–plant pairs (mainly hymenopterocecidia, acarocecidia, and dipterocecidia) and showed the occurrence of polyploidization of the typical nutritive tissue cells in approximately half of these pairs. The degree of endopolyploidy usually increased from the periphery of the gall towards the parasite. Polyploidization occurred after synchronous mitoses without cell wall formation or after anaphase arrest that led to restitution nuclei. Much more recently, Harper et al. [23] detected the formation of polytene chromosomes in the internal cells of galls induced by the wasp Biorhiza pallida (L., 1758) (Cynipidae) on the leaves of the oak Quercus robur (L., 1753) (Fagaceae). Later, a phenomenon was discovered that is seemingly an alternative to endopolyploidy or polyteny in gall cells. The typical nutritive tissue of some galls induced on the leaves of the tree Copaifera langsdorffii (Desf., 1821) (Fabaceae) by a Neotropical gall midge fly (Cecidomyiidae, species not identified) contained anucleated cells [24].
The functional diversity of galls induced by representatives of various families of the order Hemiptera deserves special attention. Typical nutritive tissue is not formed in galls induced by aphids (Aphididae) and jumping plant lice (Psyllidae) [8][25][26]. In such galls, the typical nutritive tissue is absent, but there is the so-called “nutritive-like tissue”, which surrounds the gall chambers. This tissue is not a source of food for the parasites inside. An attempt has been made to explain this situation as being attributable to the feeding habits of the aphids and psyllids, which do not scrape or chew plant material, as do the larvae of the gall-forming Diptera and Lepidoptera [27], but instead suck nutrients (phloem sap) directly from the conductive bundles [8][28].

3. Stimuli That Induce the Development of Galls

The first interactions of gall-forming parasites with their host plants occur in different ways, depending on the arthropod group [8]. In case of the galling eriophyoid mites (Eriophyoidea), aphids (Aphididae) and phylloxerans (Phylloxeridae), the primary gall-inducing stimulus is produced by females when they commence feeding on young plant leaves. Since the main period of gall formation in the Palearctic region occurs on young leaves in the spring, leaf age apparently plays an important role, but this phenomenon has not been specially studied.
The minute eriophyoid mite (body length: 100–300 μm) attacks a single epidermal cell of the host plant by piercing it with stylets and injecting saliva. The damaged cell dies, but the gall-forming effect then spreads to the adjacent leaf area, probably through plasmodesmata and the conducting system [15][29][30]. At the same time, it remains unclear whether what occurs is the dispersal of the primary, gall-inducing agents of the mite saliva, or the compounds that are synthesized by the attacked cell, or both. The leaf galls induced by eriophyoid mites are usually much smaller than the leaf galls of insects. It is reasonable to hypothesize that this is due to the diminutive size of the eriophyoids and the extremely small amount of their saliva that enters the plant cell at the earliest stages of gall formation.
In the case of gall wasps of the family Cynipidae (Hymenoptera), the primary gall-inducing signal is not the feeding of sexually mature individuals, but the laying of eggs in the leaf tissue [8]. In the process of oviposition, secretions of the venom glands of the female or her ovaries are also released, which could be the stimuli for gall formation [31]. In the case of gall-forming representatives of Diptera and Lepidoptera, the primary signal does not come from adults, but instead from larval feeding, which wounds the epidermal cells of the host [8][20][32]. In addition, not only the saliva of the larvae but also their excrement could play a role in gall initiation [3].
Unusual cases are known when insect larvae acquire the ability to initiate galls only after a few molts. For example, in the micromoth, Caloptilia cecidophora (Kumata, 1966) (Lepidoptera, Gracillariidae), which infests the leaves of the tree, Glochidion obovatum (von Siebold, 1845) (Phyllanthaceae), the first and second instars are leaf-miners. Their feeding produces galleries within the leaf lamina, and they do not have any gall-inducing properties. Gall induction is initiated by the third instar, which releases a cecidogenic substance that has not yet been analyzed [33]. This lepidopteran species is unable to complete its larval development of six instars without feeding on gall nutritive tissue. Interestingly, several related members of the lepidopteran genus, Caloptilia, are exclusively leaf-miners and they do not induce galls.
The salivary glands of a large number of species from all orders of gall-forming insects were demonstrated to contain the phytohormones, auxin and cytokinins, that control normal plant development [34][35][36][37]. Additionally, de Lillo and Monfreda [38] showed that the effects of the saliva of gall-inducing eriophyoid mites on plant tissues are similar to those produced by phytohormones. A biochemical analysis of the saliva of mites has not been done, meaning that the presence of phytohormones in their saliva has not yet been verified. The reason for this is the current impossibility of collecting a sufficient amount of the saliva of galling mites for analysis.
The leading role in the process of gallogenesis caused by arthropods is now attributed to endogenous cytokinins [39]. On the other hand, Hearn et al. [40] reported that they did not detect the expression of genes encoding for phytohormones in the young larvae of the gall wasp, B. pallida. In addition, in the genome of the mite, Fragariocoptes setiger (Nalepa, 1894) (Phytoptidae), which causes galls on strawberry leaves, phytohormone genes and any other genes that could have entered the mite genome from the plant as a result of horizontal transfer were not found [41].
Important work directed towards the understanding of the molecular mechanisms involved in the initial steps in cynipid and aphid gall induction has been published recently. The transcriptome analysis of the venom glands and ovaries of the cynipid wasps Diplolepis rosae (L., 1758) and B. pallida, which induce galls on the rose, Rosa canina (L., 1753), and common oak, Quercus robur, respectively, has been performed [31]. Some maternally expressed wasp proteins (potential effectors) presumably involved in the initial parasite–host interactions were identified. They included apolipoproteins D, peroxidases, alpha-mannosidases, carbonic anhydrases and canopy 1-like proteins.

4. Gall Formation Is a Multistep Process

The most comprehensive experimental data on the multistep character of arthropod gall formation were obtained for the combination of the eriophyoid mite, Eriophyes padi (Nalepa, 1889), and bird cherry, Prunus padus (L., 1753) (Rosaceae) [29]. The scholar reported that on the control leaves, after 10 days of mite feeding, complete galls with differentiated nutritive tissue had developed. In the experiment with 8 h or 24 h contact of mites with the plant and subsequent removal of the parasites, only small primary protrusions of the leaf lamina (“abortive galls”) formed, and no further formation of galls occurred. When the mites were removed from the leaf after 48 h of contact, small pouch galls, which did not yet have typical nutritive tissue, had formed. They were therefore termed “defective galls” [29]. The dependence of the degree of gall development on the duration of the feeding period of the mite indicates a continuous transfer of gall-inducing factors produced by the mite into the plant leaf. It is possible that there is a cumulative effect, i.e., a certain critical mass of mite saliva (with gall formation inducing factors dissolved in it), injected for a certain time, is necessary for the complete development of galls.
A multistep, cumulative effect of gall-inducing agents can also be hypothesized in the case of the development of leaf galls induced by flies of the family Cecidomyiidae [20][32]. By removing the larvae at different stages of gall morphogenesis, it was possible to analyze the succession of the host plant’s responses to parasite feeding. It was demonstrated that larval activity, which differs in nature between the first and subsequent instars, is required throughout the gall formation period. 

5. Expression of Plant Genes during Gall Formation

The eriophyoid mite Fragariocoptes setiger induces galls on the leaves of the green strawberry, Fragaria viridis (Weston, 1771) (Rosaceae). During the initiation and growth of young galls, the increase in the expression of the CYCD3 and CYCB1 cell cycle genes in their tissues is associated with active cell proliferation [42]. By the time of gall maturation, a sharp decrease in the expression of cell cycle genes was found. A similar dynamic of changes in gene expression during mite galling on strawberry leaves was found for the homeobox genes, KNOX and WOX. These two genes are the universal regulators of normal plant development [43]. Finally, during the development of galls on strawberry leaves, there was an abrupt change in the expression pattern of the genes responsible for the adaxial–abaxial polarity of the leaf. 

The development of leaf galls induced by several wasp species of the family Cynipidae (Amphibolips michoacaensis Nieves-Aldrey et Maldonado, 2012, B. pallida, Dryocosmus kuriphilus Yasumatsu, 1951) when they deposit eggs in the meristematic tissues of the leaves of oaks (genus Quercus) and some other trees of the beech family (Fagaceae) has been studied [40][44][45][46]. These studies revealed major differences in gene expression between gall cells and the cells of normal (control) leaves, as well as changes in the expression pattern of hundreds or possibly thousands of plant genes during gall development. 

Particularly noteworthy is a study in which gene expression was analyzed during the development of both participants in a “parasite–host dialogue” involving larval B. pallida and the leaves of the common oak, Q. robur. The study demonstrated that “gall development involves expression of oak and gall wasp genes in repeatable, growth stage-specific patterns” [40]: (p. 19). In particular, in the tissues of young galls, the enhanced expression of ENOD genes occurred. These genes had been discovered in nitrogen-fixing nodules of a legume family (Fabaceae) and were later found in many other plants [47]. Nodulin-like proteins encoded by these genes belong to the large family of arabinogalactan proteins, which are glycoproteins involved in plant growth and development processes, including somatic embryogenesis [48][49][50]

In the young larvae of B. pallida, the expression of PCWDE genes, which code for plant cell wall degrading enzymes, including six pectin/pectate lyases, four cellulases and four rhamnogalacturonan lyases, occurs [40]. Enzymes encoded by these genes disrupt the wall structure of plant cells in this wasp’s feeding area. Then, numerous secreted peptides, including wasp chitinases, move into the gall tissues surrounding the larva, although it is not yet clear which larval tissue produces chitinases. The same scholars inferred that their data supported a hypothesis, although it is not yet generally accepted, that galls induced by wasps of the family Cynipidae can be considered “modified somatic embryos”, with their development being similar to the somatic embryogenesis of plants. They stated that “host arabinogalactan proteins and gall wasp chitinases interact in young galls to generate a somatic embryogenesis-like process in oak tissues surrounding the gall wasp larvae” [40] (p. 1). During somatic embryogenesis, a fully developed fertile plant organism develops from a single somatic cell [51][52]; the molecular aspects of this process have been intensively studied [53][54][55].

A very recent study [56][57] revealed for the first time the tissue-specific gene expression in the active growth phase of young galls induced by the wasp Dryocosmus quercuspalustris (Osten-Sacken, 1861) on the leaves of the red oak, Quercus rubra (L., 1753). The analysis was carried out during a single stage of gall formation, specifically a young actively growing gall with a feeding larva in the internal gall chamber (approximately 5–6 days after oviposition). For the first time, not only were significant differences (28%) revealed between the transcriptomes of the whole gall and the adjacent leaf tissue, but also between the outer gall tissue, which performs a predominantly protective function, and the internal tissue of the gall, on which the parasite feeds. In general, the transcriptome of the outer tissue of the gall was more similar to the transcriptomes of the tissues of leaf buds, twigs and reproductive structures of oak than to the transcriptome of normal leaf tissue. 

Leaf galling is also induced by some hemipterans. In the case of a parasite–plant host pair, the aphid, Schlechtendalia chinensis (Bell, 1851) (Aphididae), and sumac, Rhus javanica (L., 1753) (Anacardiaceae), in the early stages of gall formation, increased expression of the KNOX genes occurs [58]

An attempt to identify the genes involved in leaf gallogenesis involving the simultaneous use of several parasite–host pairs was recently undertaken by Takeda et al. [3][59]. Transcriptomes from galls formed by three pairs were studied: Rhopalomyia yomogicola (Matsumura, 1931) (Diptera, Cecidomyiidae)—Artemisia montana (Pampanini, 1930) (Asteraceae), Caloptilia cecidophora (Lepidoptera, Gracillariidae)—Glochidion obovatum (Phyllanthaceae) and Borboryctis euryae (Kumata et Kuroko, 1988) (Lepidoptera, Gracillariidae)—Eurya japonica (Thunberg, 1783) (Pentaphylacaceae). Their molecular data were discussed in combination with the molecular data obtained by the same scholars for the pair Schlechtendalia chinensisRhus javanica [58].

6. Gallogenesis and Photosynthesis

In the previous section, it was noted that, during gall development induced by representatives of the orders Diptera, Hemiptera, Hymenoptera and Lepidoptera, leaf gall tissues of host plants usually show a significant downregulation of the genes associated with photosynthesis [58][59][60]. The latest study compared internal and external tissues of the young galls induced by the wasp Dryocosmus quercuspalustris on the leaves of the oak, Quercus rubra [56]. The internal tissue, which was termed heterotrophic, was characterized by an increased expression of genes encoding for the synthesis of sucrose, and a complete suppression of the genes associated with photosynthesis.
Leaf galls induced by the eriophyoid mites have not yet been studied with respect to the expression of their photosynthesis-related genes. Nevertheless, in the case of mite gallogenesis, there are morphological and physiological data that indicate significant destruction of the photosynthetic apparatus (reduction in leaf area, a decrease in the chlorophyll and carotenoid content per unit of leaf area and per whole leaf), and inhibition of the process of photosynthesis [61][62]
In general, gall-forming insects and eriophyoid mites have a similar suppressive effect on photosynthesis in the leaf galls induced by them on plants. A notable exception is represented by two unusual galling insect–host plant pairs consisting of the gall-forming beetle weevils, Smicronyx smreczynskii (Solari, 1952) or Smicronyx madaranus (Kôno, 1930) (Coleoptera, Curculionidae), and field dodder, Cuscuta campestris (Yunck., 1932) (Convolvulaceae). Field dodder is an obligate parasitic plant with a very low chlorophyll content and very weak photosynthetic activity. The weevil larvae significantly enhanced the photosynthetic activity in the spherical galls induced by them on the dodder shoots and they therefore acquired nutrient-rich shelters [63][64]
The molecular mechanisms involved in the suppression or enhancement of photosynthesis by gall-forming insects and eriophyoid mites currently remain largely unknown. These phytoparasitic arthropods inhabit the leaves of plants and it is difficult to maintain such parasite–tree systems in the laboratory to study the mechanisms involved in the suppression or enhancement of photosynthesis in gall tissues [64]. Among the reasons for the frequent decrease in the photosynthetic capacity of galled leaves may be a decline in stomatal conductance and in photosystem II efficiency [65][66][67]. The enhancement of photosynthetic activity in the leaves infested by the gall-forming beetle weevils could be a consequence of an increase in chloroplast numbers and chlorophyll content in the inner layer of galls [64].


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