RESUMO

Galls are plant neoformations induced by specialized parasites. Since gall inducers rely on reactive plant sites for gall development, variations in abiotic factors that affect plant phenology are expected to impact the life cycle of gall inducers. To test the hypothesis that different light conditions affect both host plant and gall inducer life cycles, we studied the system Eugenia uniflora (Myrtaceae) - Clinodiplosis profusa (Cecidomyiidae), comparing plants occurring in sunny and shaded environments. We mapped phenological differences among individuals of E. uniflora occurring in the two environments and related them to the influence of luminosity on the life cycle of the gall inducer. Shade plants showed lower intensity of leaf sprouting throughout the year compared to sun-exposed plants, especially during the rainy season. Young and mature galls are synchronized with the peak of leaf sprouting at the beginning of the rainy season, lasting longer in sun-exposed plants - approximately two months longer compared to shade plants. The greater light intensity positively impacts the formation and growth of leaves and galls, with an extended period available for their induction and growth. Thus, light is an important factor for the development of gallers, considering that variations in luminosity influenced not only the phenology of the host plant, but also determined the life cycle of gall inducers. Furthermore, changes in plant-environment interactions are expected to affect the life cycle and richness of other host plant-gall inducer systems.

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RESUMO

The gall-host Eugenia uniflora (Myrtaceae) is adaptable to different light conditions, enabling leaf production and survival in both sun and shade. Leaves of E. uniflora in shaded environments have more mesophyll layers, and galls of Clinodiplosis profusa (Cecidomyiidae) are larger and wider. Based on these previous observations, this study investigated the morphogenesis of galls induced by C. profusa on leaves of E. uniflora in different light conditions, revealing if the galls have a potential for acclimation, as observed with leaves. For this purpose, we compared the anatomical, histometric, and histochemical development of leaves and galls at different stages of development in sun and shade environments. Additionally, we analyzed the cytological features of the tissues composing the mature gall walls. Cells of shade galls expanded more toward the end of the developmental phase, which may explain the larger volume found for shade galls in a previous study. However, during the mature phase, these galls showed no significant differences in tissue thickness and final cell elongation in the contrasting light conditions. In the ultrastructural analyses, mature galls showed a gradient distinguishing the outer and inner parenchyma cells. The inner parenchyma had nutritive cells, with dense cytoplasm and abundant organelles. A higher accumulation of starch grains in nutritive cells, with evidence of hydrolysis of starch grains detected in the innermost layers leads to the accumulation of reducing sugars, which, with the presence of plastoglobules and protein bodies, are important mechanisms of oxidative stress dissipation in the cells in contact with the gall inducer.

RESUMO

Leaf-galling Eriophyidae (Acarina) may promote simple or complex alterations in the organs of their host plants, such as an increase in indumentum density or the reorganization of epidermis and ground system tissue patterns. To test if hairy galls of Eriophyidae on Avicennia schaueriana (Acanthaceae) are related to complex changes, leaf galls in distinct developmental phases were compared to non-galled leaves using anatomical, histochemical, and histometric analyses. Quantitative comparisons of preferential gall induction sites and gall area according to distinct leaf portions were made to evaluate if the impacts of gall formation can be related to the distinct potentialities of leaf microsites. The apical portion of the leaves and leaf margins were the sites with the highest occurrence of galls, but no relationship was detected between gall area and induction site. The gall anatomy revealed that epidermal features are influenced the most with the development of abnormal stomata and projected or sunken salt glands. The most striking change is the neoformation of elongated filiform trichomes on the abaxial surface (where the mites occur) that accumulate reducing sugars and proteins. The filiform trichomes may protect the inducers against abiotic stressors and enemies, and the primary metabolites that accumulate are important foods for mites. The mesophyll has simple alterations, only in the spongy parenchyma. Complex alterations occur only in abaxial epidermal cells close to feeding sites of the inducer. The number of inducers per gall seems to be the most important influence on gall size, since gall area is not related to the position in the leaves.

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Gall cytological, metabolic, and structural traits are established due to the feeding habits of the associated galling herbivores, and sometimes are influenced by other organisms involved in the interaction. We tested this assumption on three gall morphotypes, the globoid, the lenticular, and the fusiform, induced by Cecidomyiidae on leaflets of Inga ingoides (Rich.) Willd. (Fabaceae: Caesalpinioideae). Taking for granted that the three Cecidomyiidae galls are induced on the same host plant and organ, we assume that the cytological and histochemical traits of their nutritive cells may be similar, but under the fungi influence, the ambrosia gall cytological profile may be peculiar and reflect on the accumulation of primary metabolites. The ambrosia globoid galls involve three organisms (host plant, gall inducer, and fungi), while the fusiform and the lenticular galls involve two organisms (host plant and gall inducer). The accumulation of primary metabolites is similar among the three gall morphotypes, except for the non-detection of reducing sugars in the fusiform galls. The fungi presence can impact the system but does not define exclusive features for the ambrosia globoid galls when compared to the lenticular and fusiform morphotypes. In fact, the cytological traits have revealed three different cytological mechanisms for food resources availability to the three galling Cecidomyiidae: (a) cell wall destructuring and cell death by fungi intermediation in the ambrosia globoid galls, (b) necrosis-type cell death in the fusiform galls, and (c) maintenance of continuous metabolic activity in the lenticular galls.

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Plant cell and tissue responses to the attack of mining herbivores may be diagnosed by anatomical and histochemical analyses, herein investigated regarding the mining activity of Phyllocnistis hemera larvae in the leaf lamina of Daphnopsis fasciculata. The larva enters the leaf lamina through the adaxial epidermis, and feeds on palisade parenchyma cells. A healing tissue is produced after the larva passes, and its cells are reactive to histochemical tests for lignins and pectins. At first, the leaf mine is composed of a channel that is limited by palisade parenchyma cell wall fragments. Later, it is filled with a regenerative tissue constituted by isodiametric cells recruited from the spongy parenchyma, which fills up the mine channel. The cells differentiated inside the mine, regenerated the damage caused to leaf tissues, and may isolate the mine from the entrance of pathogens. Daphnopsis fasciculata is capable of reconstructing mesophyll tissues, which involves the totipotency of parenchyma cells and enables an important strategy for plant recovering after the attack of mining parasites.

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Root growth is reduced in soils with low pH [H+] and abundant soluble aluminum [Al3+], which can be a consequence of the interaction between Al3+ and cell wall composition. The competition between Al3+ and Ca2+ toward binding to pectin molecules was evaluated in roots of Urochloa decumbens, an African grass highly adapted to acidic Al-rich soils. Variations in the composition and distribution of pectins can change the extensibility, rigidity, porosity, and adhesive properties of plant cell walls, which were tested in seedlings of U. decumbens exposed to pH 3.5, 4.5 and 5.8 and to 0, 80, 160 and 320 µM of Al3+ for 80h. Root growth corroborated that U. decumbens is very tolerant to soil acidity, with effective reduction of root growth only at pH 3.5. Immunocytochemical approaches demonstrated variations in pectin composition induced both by Al3+ and by H+ in root tissues and zones. Based on the usual linkage between Ca2+ and pectins, Density Functional Theory (DFT) analyses indicated that Al3+ bound easier to pectins than Ca2+ did, leading to the formation of more Al3+-pectate complexes than Ca2+-pectate complexes, which resulted in higher rigidity of cell walls, and hampered cell extension.

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Insect galls may be study models to test the distribution of pectins and arabinogalactan-proteins (AGPs) and their related functions during plant cell cycles. These molecules are herein histochemically and immunocitochemically investigated in the kidney-shaped gall induced by Baccharopelma dracunculifoliae (Psyllidae) on leaves of Baccharis dracunculifolia DC. (Asteraceae) on developmental basis. The homogalacturonans (HGAs) (labeled by JIM5) and the arabinans (labeled by LM6) were detected either in non-galled leaves or in young galls, and indicated stiffening of epidermal cell walls, which is an important step for cell redifferentiation. The labeling of HGAs by JIM7 changed from young to senescent stage, with an increase in the rigidity of cell walls, which is important for the acquaintance of the final gall shape and for the mechanical opening of the gall. The variation on the degree of HGAs during gall development indicated differential PMEs activity during gall development. The epitopes recognized by LM2 (AGP glycan) and LM5 (1-4-ß-D-galactans) had poor alterations from non-galled leaves towards gall maturation and senescence. Moreover, the dynamics of pectin and AGPs on two comparable mature kidney-shaped galls on B. dracunculifolia and on B. reticularia revealed specific peculiarities. Our results indicate that similar gall morphotypes in cogeneric host species may present distinct cell responses in the subcelular level, and also corroborate the functions proposed in literature for HGAs.

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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.

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RESUMO

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.

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