Galls are neoformed structures induced by specific animals, fungi, bacteria, virus or some parasitic plants on their host plant organs. Developmental processes are well known in Agrobacterium tumefasciens galls, but the animal-induced galls have a striking anatomical diversity, concerning several patterns, which were reunited herein. Anatomical traits observed in animal-induced galls involve manipulation of plant morphogenesis in convergent ways. Nematode, mite and insect galls usually contain homogeneous storage parenchyma and develop due to hyperplasia and cell hypertrophy. The development of typical nutritive tissues, giant cells, or hypertrophied vascular bundles may occur. Some other anatomical features may be usually restricted to galls induced by specific taxa, but they may eventually be related to the developmental potentialities of the host plants. The combination of distinct morphogenetic peculiarities in each gall system culminates in extant gall structural diversity. Convergent anatomical traits are observed according to the feeding mode of the gall inducers, representing potentiation or inhibition of similar events of host plant morphogenesis and cell redifferentiation, independent of gall-inducing taxa.

Feeding and Other Gall Facets: Patterns and Determinants in Gall Structure

Animal-induced galls are considered extended phenotypes of their inducers, and therefore plant morphogenesis and metabolism may vary according to the species of gall inducers. The alterations in vacuolar and apoplastic polyphenols, carotenoids, chlorophyll fluorescence rates, PSII quantum yield, and phospholipid peroxidation were studied in galls induced by Ditylenchus gallaeformans (Nematoda) on Miconia albicans and M. ibaguensis (Melastomataceae), and by an unidentified Eriophyidae (Acarina) on M. ibaguensis. The focus currently addressed is gall metabolism as the extended phenotype of the gall inducers, and the neglected determination of gall functionalities over host plant peculiarities. Galls induced by D. gallaeformans on M. albicans and by the Eriophyidae on M. ibaguensis have increased accumulation of apoplastic and vacuolar phenolics, which is related to the control of phospholipid peroxidation and photoprotection. The galls induced by D. gallaeformans on M. ibaguensis have higher carotenoid and vacuolar polyphenol contents, which are related to excessive sunlight energy dissipation as heat, and photoprotection. Accordingly, antioxidant strategies varied according to the gall-inducing species and to the host plant species. The distinctive investments in carotenoid and/or in polyphenol concentrations in the studied galls seemed to be peculiar mechanisms to maintain oxidative homeostasis. These mechanisms were determined both by the stimuli of the gall-inducing organism and by the intrinsic physiological features of the host plant species. Therefore, the roles of both associated organisms in host plant-galling organisms systems over gall metabolism is attested.

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Antioxidant metabolism in galls due to the extended phenotypes of the associated organisms.

How Galling Organisms Manipulate the Secondary Metabolites in the Host Plant Tissues?: A Histochemical Overview in Neotropical Gall Systems

The histopathogenesis of the foliar galls induced by Nothanguina phyllobia Thorne in Solanum elaeagnilolium Cav. was examined via serial sections prepared from plant shoots at 11 time intervals (0.5-30 days) following inoculation. Nematodes infected the blades and petioles of young leaves surrounding the shoot apex. Hypertrophy and hyperplasia of the palisade, pith, cortical, and vascular parenchyma resulted in the formation of confluent leaf, petiole, and stem galls up to 25 cm(3) in volume. Externally, leaf galls were irregular, light-green, convoluted spheroid bulges distending the abaxial surface. Mature galls contained a cavity lined with parenchymogenous nutritive tissue comprising intercellular spaces and actively dividing hypertrophied cells. These cells contained granular cytoplasm, hypertrophied nuclei, and brightly stained large nucleoli. Vascular tissues were not discernibly affected during the early stages of gall development. As gall development progressed, however, vascular elements were often displaced and disoriented. The histopathology of this nematode indicates that N. phyllobia is a highly specialized parasite and, for that reason, is suitable as a biological control agent.

Histopathogenesis of the galls induced by Nothanguina phyllobia in Solanum elaeagnifolium [Silver-leaf nightshade, perennial weeds, biological control agents]

Cell walls and protoplast may work together or distinctly in the establishment of the functional profiles of gall tissue compartments. This presumption is herein evaluated in three gall systems by immunocytochemical and ultrastructural analyses. The common storage tissues (CSTs) of leaf galls induced by Eriophyidae on Miconia ibaguensis leaves and by Ditylenchus gallaeformans on M. ibaguensis and M. albicans have rigid and porous cell walls due to their composition of pectins. Hemicelluloses in CST cell walls are scarcer when compared to the cell walls of the control leaves, being functionally compensated by rigid pectate gels. The typical nutritive tissues (TNTs) in galls induced by Ditylenchus gallaeformans are similar to promeristematic and secretory cells regarding their enriched cytoplasm, several mitochondria, and proplastids, as well as multivesicular and prolamellar bodies in cell membranes. The cytological features of the feeding cells of Eriophyidae galls indicate that they are not as metabolically active as the cells of the TNT in nematode galls. However, their cell wall composition suggests more plasticity and porosity than the cells of the TNT, which can compensate the less production of nutrients with more transport. The ultrastructural and immunocytochemical profiles of CST cells reveal functional similarities, which are independent of the taxa of the gall inducer or of the host plant. Despite their analogous functionalities, the protoplast and cell wall features of TNT cells of nematode galls and of the feeding cells of the Eriophyidae galls are distinct, and work out through different strategies toward keeping gall developmental site active.

Cytological attributes of storage tissues in nematode and eriophyid galls: pectin and hemicellulose functional insights

Galling herbivores induce structural and chemical alterations in their host plant's tissues. These insects have been the focus of little study in the case of Australian taxa. Leptocybe invasa, a native Australian galling hymenopteran associated with Eucalyptus species, causes economic damage to plantation eucalypts in many countries around the world. Leptocybe invasa oviposits in the midribs and petioles of expanding leaves thereby intercepting photosynthates and impairing normal expansion. We analysed the ultrastructural and chemical cellular changes in L. invasa galls on Eucalyptus camaldulensis (probably subspecies camaldulensis) to diagnose how the insect manipulates plant cells and tissues and the significance of these alterations for insect nutrition and protection. Galling stimuli induce the formation of two functionally compartmentalised types of tissue. Phenolic plant secondary metabolites and anthocyanins (plant pigments) accumulate in the outer compartment, while primary metabolites accumulate in the inner compartment. The nutritive cells (inner compartment) accumulate protein and lipids that provide food for the larvae. Total polyphenol concentrations did not differ significantly between outer and inner compartments. Nevertheless, the concentrations of quercetin and kaempferol derivatives were higher in the outer compartment than in the inner compartment. These differences could be related to the protection of plant tissues against ultraviolet rays and the maintenance of redox homeostasis. There were higher ratios of hexahydroxydiphenoyl‐containing hydrolysable tannins rather than galloyl‐containing hydrolysable tannins in the inner compartment. This shift in the oxidative capacity of the polyphenols in the inner compartment could represent a defensive plant response to the larvae.

Functional compartmentalisation of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae)

Thysanoptera-induced galls commonly culminate in simple folding or rolling leaf gall morphotypes. Most of these galls are induced by members of the suborder Tubulifera, with only a few species of the suborder Terebrantia being reported as gall inducers. The Terebrantia, as most of the gall inducers, manipulates the host plant cellular communication system, and induces anatomical and biochemical changes in its host plant. In an effort to keep its homeostasis, the host plant reacts to the stimuli of the galling insect and triggers chemical signaling processes. In contrast to free-living herbivores, the signaling processes involving galling herbivores and their host plants are practically unknown. Current investigation was performed into two steps: first, we set the structural profile of non-galled and galled leaves, and looked forward to find potential alterations due to gall induction by an undescribed species of Nexothrips (suborder Terebrantia) on Myrcia splendens. Once oil glands had been altered in size and number, the second step was the investigation of the chemical profile of three tissue samples: (1) non-galled leaves of a control individual, (2) non-galled leaves of galled plants, and (3) galls. This third sample was divided into two groups: (3.1) galls from which the inducing thrips were manually removed and (3.2) galls macerated with the inducing thrips inside. The chemical profile was performed by gas chromatography/ mass spectrometric detector after headspace solid-phase extraction.The galling activity of the Nexothrips sp. on Myrcia splendens culminates in mesophyll compactness interspersed to diminutive hypersensitive spots, development of air cavities, and the increase in size and number of the secretory glands. Seventy-two compounds were completely identified in the volatile profile of the three samples, from which, sesquiterpenes and aldehydes, pertaining to the “green leaf volatile” (GLVs) class, are the most abundant. The rare event of gall induction by a Terebrantia revealed discrete alterations toward leaf rolling, and indicated quantitative differences related to the plant bioactivity manipulated by the galling thrips. Also, the content of methyl salicilate has varied and has been considered a potential biomarker of plant resistance stimulated as a long-distance effect on M. splendens individuals.

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Danielle Ramos de Alvarenga

Papers

Feeding and Other Gall Facets: Patterns and Determinants in Gall Structure

Functional compartmentalisation of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae)

Structural and Chemical Profiles of Myrcia splendens (Myrtaceae) Leaves Under the Influence of the Galling Nexothrips sp. (Thysanoptera).

Anatomical and histometric explanations for leaf folding on Holopothrips striatus galls in Myrcia retorta