Complex meristematic activity induced by Eucecidoses minutanus on Schinus engleri turns shoots into galls.

PREMISE: Gall-inducing organisms change the development of their host plant organs, resulting in ontogenetic patterns not observed in the non-galled plants. Distinct taxa induce galls on Schinus spp., manipulating meristematic patterns in the host plant in distinct ways. Here we report ontogenetic novelties induced in the lateral buds of S. engleri by Eucecidoses minutanus, a Cecidosidae, whose galls have been poorly understood. METHODS: The anatomy, histochemistry, and histometry of galls in distinct phases of development, non-galled buds, and stems of Schinus engleri were analyzed in parallel with the instars of E. minutanus to detail the morphogenetic changes in the host with each larval stage. RESULTS: Ontogenetic phases of the galls were intricately associated with larval development. First and second-instar larvae induced pericycle and pith cells to dedifferentiate into the gall inner meristem, where hyperplasia and cell hypertrophy characterized the growth and development phase of the gall. The innermost layers were lipid-rich nutritive cells that lined the larval chamber. Additional vascular bundle rows were produced in young galls. Third and fourth instar-larvae were associated with the gall maturation phase: centripetal lignification of the outer parenchyma cell layers, epidermal stratification, and activation of a cambium-like meristem (CLM). The CLM activity resulted in new layers of nutritive cells that differentiated inward as the first layers of nutritive cells were consumed by E. minutanus larvae, and, also, in more parenchyma cell layers that formed outward. All tissues between the innermost layer of nutritive tissue that surround the gall chamber and the outermost layer of the dermal system that externally covers the gall form the gall wall, and increased in thickness until the end of gall maturation. CONCLUSIONS: E. minutanus induces a structurally complex globoid stem gall, modifying all host plant tissues and stimulating a novel meristematic pattern in S. engleri. The gall developmental stages are each related to specific gall-inducing instars, as gall development progresses according to the development of E. minutanus.

Reacquisition of New Meristematic Sites Determines the Development of a New Organ, the Cecidomyiidae Gall on Copaifera langsdorffii Desf. (Fabaceae).

The development of gall shapes has been attributed to the feeding behavior of the galling insects and how the host tissues react to galling stimuli, which ultimately culminate in a variable set of structural responses. A superhost of galling herbivores, Copaifera langsdorffii, hosts a bizarre "horn-shaped" leaflet gall morphotype induced by an unidentified species of Diptera: Cecidomyiidae. By studying the development of this gall morphotype under the anatomical and physiological perspectives, we demonstrate the symptoms of the Cecidomyiidae manipulation over plant tissues, toward the cell redifferentiation and tissue neoformation. The most prominent feature of this gall is the shifting in shape from growth and development phase toward maturation, which imply in metabolites accumulation detected by histochemical tests in meristem-like group of cells within gall structure. We hypothesize that the development of complex galls, such as the horn-shaped demands the reacquisition of cell meristematic competence. Also, as mature galls are green, their photosynthetic activity should be sufficient for their oxygenation, thus compensating the low gas diffusion through the compacted gall parenchyma. We currently conclude that the galling Cecidomyiidae triggers the establishment of new sites of meristematic tissues, which are ultimately responsible for shifting from the young conical to the mature horn-shaped gall morphotype. Accordingly, the conservative photosynthesis activity in gall site maintains tissue homeostasis by avoiding hypoxia and hipercarbia in the highly compacted gall tissues.

Multivesicular bodies differentiate exclusively in nutritive fast-dividing cells in Marcetia taxifolia galls.

Marcetia taxifolia (A. St.-Hil.) DC. hosts two gall morphotypes, a pistil-shaped gall induced by a Cecidomyiidae (Diptera) and a fusiform stem gall induced by a Lepidoptera. The cytological study of these galls aimed to answer how the difference in nutritive tissues of Diptera and Lepidoptera galls could be explained on cytological basis. The nutritive tissues of lepidopteran galls have a fast-dividing cell zone, the storage nutritive tissue, which replaces the cells of the typical nutritive tissue, where the larvae feed. The differentiation of multivesicular bodies in the plasma membrane occurred exclusively in these fast-dividing cells of the lepidopteran galls, evidencing the meristematic condition of such tissue. The accumulation of reactive oxygen species (ROS) analyzed in situ in the nutritive cells is not sufficient to induce programmed cell death (PCD), as the cells of M. taxifolia have plastoglobules and accumulate polyphenols and terpenoids, which are diagnostic defenses against oxidative stress. The two taxa of galling insects have different nutritional requirements, thus inducing specific cytoplasm-enriched cells on their nutritive tissues.

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 MESSAGE: The 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. Plant 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.

Biology and systematics of gall-inducing triozids (Hemiptera: Psylloidea) associated with Psidium spp. (Myrtaceae).

Psidium myrtoides (Myrtaceae) shelters the gall inducer Nothotrioza myrtoidis gen. et sp. n. (Hemiptera: Psylloidea) which is described and illustrated here. Nothotrioza belongs to the family Triozidae and is probably most closely related to Neolithus, a monotypic Neotropical genus associated with Sapiun (Euphorbiaceae). Three species are recognized within Nothotrioza: the type species N. myrtoidis sp. n. associated with Psidium myrtoides, N. cattleiani sp. n. (misidentified by Butignol & Pedrosa-Macedo as Neotrioza tavaresi) with Psidium cattleianum, and N. tavaresi (Crawford) comb. n. (from Neotrioza) with an unidentified species of Malpighiaceae, respectively. A lectotype is designated here for Neotrioza tavaresi. Also, the diversity of insect galls associated with P. myrtoides and the biology of N. myrtoidis were examined. N. myrtoidis presents five instars and an annual life cycle synchronised with the phenology of P. myrtoides. Gall size was proportional to the insect developmental stages, and rates of parasitism and mortality were 15.7 % and 29.8 %, respectively. The red colour is an important macroscopic diagnostic feature of the gall that could be associated with parasite-free condition of the galling insect. The biological features presented by the system Psidium myrtoides--Nothotrioza myrtoidis are in accordance with other systems involving sucking galling insects, however, it is exceptional by its univoltine life cycle associated with a perennial plant in the Neotropics. The galls induced by the three known Nothotrioza spp. are morphologically similar, i.e. closed, globoid and unilocular, as well as the opening mechanism for releasing the adults.