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

Isaías, Rosy Mary dos Santos; Oliveira, Dênis Coelho de; Moreira, Ana Sílvia Franco Pinheiro; Soares, Geraldo Luiz Gonçalves; Carneiro, Renê Gonçalves da Silva

doi:10.1016/j.bbagen.2015.03.007

Cited by 78 publications

(72 citation statements)

References 80 publications

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“…The relationship between the absence of reducing sugars and high accumulation of ROS in the inner tissues is theoretically proposed for Cecidomyiidae-induced galls. High levels of sugars are expected for Cecidomyiidae galls (Bronner, 1992), and should be crucial for disrupting the high oxidative stress detected by the presence of H 2 O 2 in the inner compartment, as hypothesized by Isaias et al (2015).…”

Section: Ros Accumulation and Reducing Sugars Suppression In Nutritivmentioning

confidence: 97%

“…The gall metabolic requirements generate a sink of primary and secondary metabolites, which may compartmentalize in protective and/or nutritive tissues (Carneiro, Castro, & Isaias, 2014). The carbohydrates drained to the gall developmental site are responsible for plant cell machinery support (Oliveira, Christiano, Soares, & Isaias, 2006;Castro et al 2012), and can also act as potential signaling molecules for cell division and growth (Koch, 2004;Wind, Smeenkens, & Hanson, 2010;Isaias, Oliveira, Moreira, Soares, & Carneiro, 2015). The signaling function in gall sites has also been attributed to reactive oxygen species (ROS) (Oliveira & Isaias 2010a;Oliveira, Moreira, & Isaias, 2014;Isaias et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Compartmentalization of Metabolites and Enzymatic Mediation in Nutritive Cells of Cecidomyiidae Galls on Piper Arboreum Aubl. (Piperaceae)

Bragança¹,

Oliveira²,

Isaías³

2016

JPS

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Galling insects commonly change the chemical profile of their host plant tissues during gall induction and establishment. As a consequence, galls accumulate a wide range of metabolites in specialized cells, which may be organized in a nutritive tissue and in outer storage cells. The nutrients compartmentalized in nutritive cells may be directly assessed or metabolized via enzymatic mediation, while the gall outer cortex may accumulate secondary metabolites. These secondary metabolites may configure a specialized chemical barrier against the attack of natural enemies. Either the nutritive inner cells or the outer cortical cells, with their specific metabolic apparatus, should differentiate under the chemical constraints of each host plant-galling herbivore interaction. This premise is herein addressed by the investigation of the histochemical profile of the non-galled leaves and galls induced by Diptera: Cecidomyiidae on Piper arboreum. The spatial compartmentalization of the nutritive and defensive metabolites indicates the new functions assumed during the redifferentiation of the host plant cells. The enzymatic mediation of the primary metabolites by sucrose synthase and invertases favors the nutritive requirements of the galling Cecidomyiidae or the structural maintenance of the gall. The accumulation of secondary metabolites is restrict to the tissue layers not involved in nutrition, and may act in the chemical protection against predators or parasitoids. Current results systematically document metabolites compartmentalization, evidence the impairment of toxic compounds storage in cells surrounding the larval chamber, as well as, detect the redirection of nutritive substances to the site of the Cecidomyiidae feeding. The activity of sucrose synthase is restrict to the nutritive tissue in the galls on Piper arboreum, and reinforces previous detection of this enzyme mediation in carbohydrate metabolism in Cecidomyiidae galls.

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Section: Ros Accumulation and Reducing Sugars Suppression In Nutritivmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Compartmentalization of Metabolites and Enzymatic Mediation in Nutritive Cells of Cecidomyiidae Galls on Piper Arboreum Aubl. (Piperaceae)

Bragança¹,

Oliveira²,

Isaías³

2016

JPS

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“…Therefore, the accumulation of lignins in parenchymatic cells are direct responses to distinct types of stress. 20,22,27 Also, the development of sclerenchyma layers in insect galls, and of sclereids and lignified fiber sheaths in xeromorphous leaves, involves stressful conditions. 18,22 Moreover, agronomists are studying, selecting, and/or genetically enhancing cultivars with the lower possible amount of lignins.…”

Section: Research-article2016mentioning

confidence: 99%

“…23,24 Such functions may be triggered in biotic stresses, water deficiency, and excessive light exposition. 13,14,19,20,22,25 Some flavonoids, such as anthocyanins in the vacuoles, are important to give purple, pink, or blue color to some plant organs, acting as attractive traits for specialist pollinators and dispersers. 13,23,24 The lignins are deposited in the cell walls, rigidifying and waterproofing these outer structures of plant cells.…”

Section: Research-article2016mentioning

confidence: 99%

“…17,18 The phenolics act in the avoidance of excessive damage of reactive oxygen species (ROS) in cellular membranes and organelles. 13,[18][19][20][21][22] They are also important antioxidant compounds, capturing the ROS, protecting plant structures from ultraviolet (UV) radiation, and avoiding the programmed cell death. 23,24 Such functions may be triggered in biotic stresses, water deficiency, and excessive light exposition.…”

Section: Research-article2016mentioning

confidence: 99%

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Preventing False Negatives for Histochemical Detection of Phenolics and Lignins in PEG-Embedded Plant Tissues

Ferreira

Falcioni

Guedes

et al. 2016

J Histochem Cytochem.

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SummaryPolyethylene glycol (PEG) is a low-cost and advantageous embedding medium, which maintains the majority of cell contents unaltered during the embedding process. Some hard or complex plant materials are better embedded in PEG than in other usual embedding media. However, the histochemical tests for phenolics and lignins in PEG-embedded plant tissues commonly result in false negatives. We hypothesize that these false negatives should be prevented by the use of distinct fixatives, which should avoid the bonds between PEG and phenols. Novel protocols for phenolics and flavanols detection are efficiently tested, with fixation of the samples in ferrous sulfate and formalin or in caffeine and sodium benzoate, respectively. The differentiation of lignin types is possible in safranin-stained sections observed under fluorescence. The Maule's test faultlessly distinguishes syringyl-rich from guaiacyl-and hydroxyphenyl-rich lignins in PEG-embedded material under light microscopy. Current hypothesis is corroborated, that is, the adequate fixation solves the false-negative results, and the new proposed protocols fill up some gaps on the detection of phenolics and lignins. (J Histochem Cytochem 65:105-116, 2017)

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

Ferreira

Moreira

Carneiro

et al. 2022

American J of Botany

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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.

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

Cited by 78 publications

References 80 publications

Compartmentalization of Metabolites and Enzymatic Mediation in Nutritive Cells of Cecidomyiidae Galls on Piper Arboreum Aubl. (Piperaceae)

Compartmentalization of Metabolites and Enzymatic Mediation in Nutritive Cells of Cecidomyiidae Galls on Piper Arboreum Aubl. (Piperaceae)

Preventing False Negatives for Histochemical Detection of Phenolics and Lignins in PEG-Embedded Plant Tissues

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

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