Denis Coelho de Oliveira

Illustrated and Annotated Checklist of Brazilian Gall Morphotypes

The analysis on nine inventories on the richness and diversity of galling herbivores in Brazil accounted for 806 gall systems occurring in 443 host-plant species from 74 plant families. This checklist of the Brazilian gall morphotypes proposes seven standardized morphotypes and five additional shapes that group the majority of the three-dimensional shapes reported in literature. Criteria are proposed to standardize the terminology, and a critical analysis is provided aiming to avoid possible inconsistencies in order to generate easily comparable data in future inventories. The morphotypes are herein catalogued in alphabetical order, accompanied by a conceptual definition, an illustration, and examples that best represent the shape. It is proposed that the inventories should present at least the (1) host-plant species, (2) galling herbivore species or its identification to the lowest possible taxonomic level, (3) host-plant galled organ and gall position, (4) gall morphotype, (5) gall color and registration of indumentum when present, (6) gall phenological and developmental data, (7) association with other trophic levels, and (8) additional information, such as dimension, and number of chamber(s).

Do Cecidomyiidae galls of Aspidosperma spruceanum (Apocynaceae) fit the pre-established cytological and histochemical patterns?

Cecidomyiidae galls commonly present a zonation of tissues with lignified cell layers externally limiting a reserve tissue and internally limiting a specialized nutritive tissue next to the larval chamber. The cytological aspects of this specialized tissue indicate high metabolic activity as well as carbohydrate accumulation. In Aspidosperma spruceanum–Cecidomyiidae gall system, ultrastructural and histochemical investigations corroborated this pattern and also revealed the storage of proteins in the nutritive cells. Reactive oxygen species (ROS), callose, and pectin accumulation were related to the feeding activity of the galling herbivore. Phosphorylase, glucose-6-phosphatase, acid phosphatases, invertases, and sucrose synthase activities were detected for the first time, in the Neotropical region, and discussed in relation to gall maintenance and the feeding activity of the Cecidomyiidae.

Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds

Biologists who study insect-induced plant galls are faced with the overwhelming diversity of plant forms and insect species. A challenge is to find common themes amidst this diversity. We discuss common themes that have emerged from our cytological and histochemical studies of diverse neotropical insect-induced galls. Gall initiation begins with recognition of reactive plant tissues by gall inducers, with subsequent feeding and/or oviposition triggering a cascade of events. Besides, to induce the gall structure insects have to synchronize their life cycle with plant host phenology. We predict that reactive oxygen species (ROS) play a role in gall induction, development and histochemical gradient formation. Controlled levels of ROS mediate the accumulation of (poly)phenols, and phytohormones (such as auxin) at gall sites, which contributes to the new cell developmental pathways and biochemical alterations that lead to gall formation. The classical idea of an insect-induced gall is a chamber lined with a nutritive tissue that is occupied by an insect that directly harvests nutrients from nutritive cells via its mouthparts, which function mechanically and/or as a delivery system for salivary secretions. By studying diverse gall-inducing insects we have discovered that insects with needle-like sucking mouthparts may also induce a nutritive tissue, whose nutrients are indirectly harvested as the gall-inducing insects feeds on adjacent vascular tissues. Activity of carbohydrate-related enzymes across diverse galls corroborates this hypothesis. Our research points to the importance of cytological and histochemical studies for elucidating mechanisms of induced susceptibility and induced resistance.

Is the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf photosynthesis

The generation of ROS (reactive oxygen species) in plant galls may induce the degradation of the membrane systems of a plant cell and increase the number of plastoglobules. This numerical increase has been related to the prevention of damage to the thylakoid systems, and to the maintenance of photosynthesis rates. To investigate this hypothesis in gall systems, a comparative study of the ultrastructure of chloroplasts in non-galled leaves and in leaf galls of A. australe and A. spruceanum was conducted. Also, the pigment composition and the photosynthetic performance as estimated by chlorophyll fluorescence measurements were evaluated. The ultrastructural analyses revealed an increase in the number and size of plastoglobules in galls of both species studied. The levels of total chlorophylls and carotenoids were lower in galls than in non-galled tissues. The chlorophyll a/b ratio did not differ between the non-galled tissues and both kinds of galls. The values of maximum electron transport rate (ETR(MAX)) were similar for all the samples. The occurrence of numerous large plastoglobules in the galled tissues seemed to be related to oxidative stress and to the recovery of the thylakoid membrane systems. The maintenance of the ETR(MAX) values indicated the existence of an efficient strategy to maintain similar photosynthetic rates in galled and non-galled tissues.

Reações de defesas químicas e estruturais de Lonchocarpus muehlbergianus Hassl. (Fabaceae) à ação do galhador Euphalerus ostreoides Crawf. (Hemiptera: Psyllidae)

Galhas sao estruturas vegetais induzidas em resposta ao ataque de organismos indutores. Euphalerus ostreoides (Psyllidae) induz galhas sobre a face adaxial de foliolos nas nervuras de segunda ordem de Lonchocarpus muehlbergianus (Fabaceae). Secoes anatomicas foram realizadas e comparados os tecidos de foliolos sadios com os de galhas imaturas e maduras. Testes histoquimicos para deteccao de derivados fenolicos, flavonoides, ligninas, lipidios e amido foram realizados para avaliar o impacto quimico causado pelo galhador. Em termos estruturais, a perda de sinuosidade das celulas epidermicas, a neoformacao de tricomas, de celulas condutoras e de fibras foram os caracteres mais conspicuos observados em decorrencia da inducao das galhas. Destaca-se a hiperplasia e hipetrofia do mesofilo com manutencao da estratificacao, a producao de goticulas lipidicas e amido, flavonas, flavonois e flavanonas nos tecidos das galhas. Contudo, a formacao de cristais de oxonio pela adicao de acido sulfurico somente nos tecidos das galhas foi uma caracteristica marcante. Os resultados sugerem que L. muehlbergianus esta submetida a alto estresse oxidativo induzido pela acao do E. ostreoides. Conclui-se que as alteracoes sao consideradas reacoes de defesa da planta contra herbivoria e mecanismos de adaptacao que em conjunto favorecem o estabelecimento do galhador nos tecidos vegetais.

Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae)—Cecidomyiidae gall systems

Previous ultrastructural and histochemical analysis proposed patterns in the accumulation of substances in galls of Diptera: Cecidomyiidae in some plant species of the temperate region. Similar analyses were done to verify the conservativeness of these patterns in the Neotropical region, where a great number of species of Cecidomyiidae is responsible for a wide diversity of morphotypes. Two gall morphotypes induced by Cecidomyiidae in a unique host plant, Copaifera langsdorffii, were studied. The gradients of carbohydrates and the activity of invertases and acid phosphatases were similar, but the cytological gradients and distribution of proteins evidenced that the sites of the induction as well as the amount of neoformed tissues may be peculiar to each gall system. The production of lipids just in the secretory cavities either in the non-galled or galled tissues indicated a potentiality of the host plant which could not be manipulated by the galling insects. Further, the absence of nucleus in the nutritive tissue, an exclusive feature of the horn-shaped galls, indicates cell death attributed to the feeding habit of the galling herbivore.

The imbalance of redox homeostasis in arthropod-induced plant galls: Mechanisms of stress generation and dissipation☆

BACKGROUND Galls have specialized tissues for the protection and nutrition of the inducers, and these tissues have been studied from the developmental and histochemical perspectives. Recently, the role of oxidative stress in galls has been tested histochemically through detection of H2O2 in gall tissues. SCOPE OF REVIEW Developmental processes and cytological events are revisited from the perspective of the redox-potential balance in both the apoplast and symplast, especially concerning the accumulation of reactive oxygen species (ROS). MAJOR CONCLUSIONS The redox potential is imbalanced differently in the apoplast and symplast at gall sites, with the apoplast having lower antioxidant-buffering capacity than the symplast. The strategies to recover redox-potential homeostasis involve the dissipation of ROS by scavenging molecules, such as phenolics, flavonoid derivatives, tocopherol, and enzyme systems. GENERAL SIGNIFICANCE Insect galls are good models to test developmental hypotheses. Although the exact mechanisms of gall induction and development have not been elucidated at the biochemical and biophysical levels, modulation of the redox potential is involved in the crucial steps of gall initiation and establishment. This article is part of a Special Issue entitled Redox regulation of differentiation and de-differentiation.

The redifferentiation of nutritive cells in galls induced by Lepidoptera on Tibouchina pulchra (Cham.) Cogn. reveals predefined patterns of plant development

Insect galls may present nutritive tissues with distinct cytological features related to the order of the gall inducer. Galling Lepidoptera larvae chew plant cells and induce the redifferentiation of parenchymatic cells into nutritive ones. The nutritive cells in the galls induced by a microlepidoptera on the leaves of Tibouchina pulchra (Cham.) Cogn. (Melastomataceae) are organelle-rich, with developed Golgi apparatus, endoplasmic reticulum, ribosomes, polyribosomes, mitochondria, plastids, and one great central or several fragmented vacuoles. The nonobservance of the nuclei in the nutritive cells deserves special attention, and confers a similarity between the nutritive cells and the vascular conductive ones. The great amount of rough endoplasmic reticulum, ribosomes, polyribosomes, and mitochondria is indicative of the high metabolic status of these cells. They are vascular cambium-like, with high protein synthesis and lipid storage. The proteins are essential to enzymatic metabolism, and secondarily, to larvae nutrition, similarly to the lipid droplets which confer energetic profile to these nutritive cells. The living enucleated cells receive mRNA from their neighbor ones, which may support the high metabolic profile of endoplasmic reticulum and ribosomes observed in galls. Thus, the nutritive cells are stimulated by the galling larvae activity, generating a new cell type, whose redifferentiation includes a mix of intrinsic and common plant pathways.

Developmental anatomy and immunocytochemistry reveal the neo-ontogenesis of the leaf tissues of Psidium myrtoides (Myrtaceae) towards the globoid galls of Nothotrioza myrtoidis (Triozidae).

Key messageThe temporal balance between hyperplasia and hypertrophy, and the new functions of different cell lineages led to cell transformations in a centrifugal gradient that determines the gall globoid shape.AbstractPlant galls develop by the redifferentiation of new cell types originated from those of the host plants, with new functional and structural designs related to the composition of cell walls and cell contents. Variations in cell wall composition have just started to be explored with the perspective of gall development, and are herein related to the histochemical gradients previously detected on Psidium myrtoides galls. Young and mature leaves of P. myrtoides and galls of Nothotrioza myrtoidis at different developmental stages were analysed using anatomical, cytometrical and immunocytochemical approaches. The gall parenchyma presents transformations in the size and shape of the cells in distinct tissue layers, and variations of pectin and protein domains in cell walls. The temporal balance between tissue hyperplasia and cell hypertrophy, and the new functions of different cell lineages led to cell transformations in a centrifugal gradient, which determines the globoid shape of the gall. The distribution of cell wall epitopes affected cell wall flexibility and rigidity, towards gall maturation. By senescence, it provided functional stability for the outer cortical parenchyma. The detection of the demethylesterified homogalacturonans (HGAs) denoted the activity of the pectin methylesterases (PMEs) during the senescent phase, and was a novel time-based detection linked to the increased rigidity of the cell walls, and to the gall opening. Current investigation firstly reports the influence of immunocytochemistry of plant cell walls over the development of leaf tissues, determining their neo-ontogenesis towards a new phenotype, i.e., the globoid gall morphotype.

The role of pectic composition of cell walls in the determination of the new shape-functional design in galls of Baccharis reticularia (Asteraceae)

The pectic composition of cell wall is altered during the processes of cell differentiation, plant growth, and development. These alterations may be time-dependent, and fluctuate in distinct regions of the same cell or tissue layer, due to the biotic stress caused by the activity of the gall inducer. Among the roles of the pectins in cell wall, elasticity, rigidity, porosity, and control of cell death may be crucial during gall development. Galls on Baccharis reticularia present species-specific patterns of development leading to related morphotypes where pectins were widely detected by Ruthenium red, and the pectic epitopes were labeled with specific monoclonal antibodies (LM1, LM2, LM5, LM6, JIM5, and JIM7) in distinct sites of the non-galled and the galled tissues. In the studied system B. reticularia, the epitopes for extensins were not labeled in the non-galled tissues, as well as in those of the rolling and kidney-shaped galls. The high methyl-esterified homogalacturonans (HGA) were labeled all over the tissues either of non-galled leaves or of the three gall morphotypes, while the intense labeling for arabinogalactans was obtained just in the rolling galls. The pectic composition of non-galled leaves denotes their maturity. The kidney-shaped gall was the most similar to the non-galled leaves. The pectic dynamics in the gall tissues was particularly altered in relation to low methyl-esterified HGA, which confers elasticity and expansion, as well as porosity and adhesion to cell walls, and are related to the homogenization and hypertrophy of gall cortex, and to translocation of solutes to the larval chamber. Herein, the importance of the pectic dynamics of cell walls to the new functional design established during gall development is discussed for the first time. The repetitive developmental patterns in galls are elegant models for studies on cell differentiation.