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

Oliveira, Dênis Coelho de; Isaías, Rosy Mary dos Santos; Fernandes, Geraldo Wilson; Ferreira, Bruno García; Carneiro, Renê Gonçalves da Silva; Fuzaro, Leandro

doi:10.1016/j.jinsphys.2015.11.012

Cited by 147 publications

(106 citation statements)

References 78 publications

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“…Changes in the pectin composition of cell walls, especially in the degree of methyl esterification, may be related to the age of plant organs or to the functional profiles of cells and tissues (Dolan et al 1997). Gall development requires manipulation of host-plant tissues and triggering of new morphogenetic patterns stimulated by the galling insect, culminating in the formation of tissue compartments at gall-development sites (Shorthouse et al 2005;Oliveira et al 2016;Bragança et al 2017). The orchestration of cell growth, division and redifferentiation, as well as changes in plant cell wall composition are fundamental for the generation of new shapes (Majewaska-Sawka and Nothnagel 2000;Lev-Yadun 2003), which determines the gall morphotypes .…”

Section: Introductionmentioning

confidence: 99%

Immunocytochemical demonstration of cell wall components related to tissue compartments in the globoid galls induced by Clinodiplosis sp. (Cecidomyiidae) on Croton floribundus Spreng. (Euphorbiaceae)

Teixeira

Oliveira

Kuster

et al. 2018

Botany

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The dynamics of cell wall components during gall development are related to structural specialization to meet the defensive or nutritional requirements of gall tissues. Cell wall features have been studied mostly in galls induced by hemipterans (Psylloidea), while galls induced by Cecidomyiidae have been little explored. We applied monoclonal antibodies to epitopes of proteins and pectins in the cell walls of non-galled leaves and galls induced by Clinodiplosis sp. (Diptera; Cecidomyiidae) on Croton floribundus Spreng. (Euphorbiaceae). The complexity of tissue zonation in Clinodiplosis galls reflected the impairment of the activity of the pectin-methylesterases during development. The labeling of the epitopes of extensins in young galls denoted cell enlargement with resistant cell walls, while the labeling of epitopes of the arabinogalactan proteins in senescent galls indicated the involvement of these proteins with programmed cell death, at the end of cell cycles at the gall development site. We conclude that the cell wall profile in Clinodiplosis galls implies an imbalance between tissue porosity, cell-to-cell signaling, and resistance linked to tissue structural and functional compartments. Current data confirm the presence of the epitopes of extensins in young galls, and the compartmentalization of homogalacturonans and rhamnogalacturonan I in galls as an independent taxon feature.

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Section: Introductionmentioning

confidence: 99%

Immunocytochemical demonstration of cell wall components related to tissue compartments in the globoid galls induced by Clinodiplosis sp. (Cecidomyiidae) on Croton floribundus Spreng. (Euphorbiaceae)

Teixeira

Oliveira

Kuster

et al. 2018

Botany

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“…In addition, the photochemical activity minimizes the triplet chlorophyll ( ∗ Chl 3 ) production, which ends up in the formation of ROS molecules (Pavlovic, 2012). Some of these molecules, such as the H 2 O 2 , have been histochemically detected in galls, and are indicative of a high oxidative stress imposed by the galling insects (Oliveira et al, 2011, 2014a, 2016; Isaias et al, 2015). …”

Section: Introductionmentioning

confidence: 99%

Sink Status and Photosynthetic Rate of the Leaflet Galls Induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae)

et al. 2017

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The galling insect Bystracoccus mataybae (Eriococcidae) induces green and intralaminar galls on leaflets of Matayba guianensis (Sapindaceae), and promotes a high oxidative stress in host plant tissues. This biotic stress is assumed by the histochemical detection of hydrogen peroxide, a reactive oxygen species (ROS), whose production alters gall physiology. Thus, we hypothesize that high levels of nutrients are accumulated during gall development in response to a local maintenance of photosynthesis and to the galling insect activity. Moreover, the maintenance of low levels of photosynthesis may guarantee O2 production and CO2 consumption, as well as may avoid hypoxia and hypercarbia in gall tissues. To access the photosynthesis performance, the distribution of chlorophyllous tissues and the photochemical and carboxylation rates in gall tissues were analyzed. In addition, histochemical tests for hydrogen peroxide and phenolic derivatives were performed to confirm the biotic stress, and set the possible sites where stress dissipation occurs. The contents of sugars and nitrogen were evaluated to quantify the gall sink. Currently, we assume that the homeostasis in gall tissues is ruptured by the oxidative stress promoted by the galling insect activity. Thus, to supply the demands of gall metabolism, the levels of water-soluble polysaccharides and starch increase in gall tissues. The low values of maximum quantum efficiency of PSII (Fv/Fm) indicate a low photosynthetic performance in gall tissues. In addition, the decrease of PSII operating efficiency, (F’m–F’)/F’m, and Rfd (instantaneous fluorescence decline ratio in light, to measure tissue vitality) demonstrate that the tissues of B. mataybae galls are more susceptible to damage caused by stressors than the non-galled tissues. Thus, the high oxidative stress in gall developmental sites is dissipated not only by the accumulation of phenolic derivatives in the protoplast, but also of lignins in the walls of neoformed sclereids.

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“…First, galls may offer effective protection against the harsher climatic variation in dry habitats (Price et al 1987;Fernandes and Price 1988;. Second, the gall inducing larva is able to manipulate the host plant, even in habitats where plants usually exhibit a poor nutritional status, to obtain a food resource free of the high defensive compounds found in stressed or sclerophyllous host plants (Fernandes 1987;Nyman and Julkunen-Tiitto 2000; see also Oliveira et al 2016). Third, the rate of attack by natural enemies and mortality caused by host plant resistance in harsher habitats is lower than mesic ones (Fernandes and Price 1992;Schultz 1992;Fernandes et al 2005).…”

Section: Introductionmentioning

confidence: 99%

Understory host plant and insect gall diversity changes across topographic habitats differing in nutrient and water stress in the Brazilian Amazon rainforest

et al. 2017

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Topographic gradients in terra firme forests are associated with pronounced changes in soil texture, soil nutrients and distance to the water-table, thereby creating different hydric and nutritional conditions for plants and their associated herbivore community. The aim of this study was to investigate galling species and host plant richness and gall species composition across topographic habitats differing in nutrient and water stress in the Brazilian Amazon rainforest. Nineteen 250 x 3 m plots were randomly sampled in the valley, slope, plateau-slope transition, and plateau habitats in terra firme forests. All individual dicotyledonous plants 1 to 3 meters high were examined for the presence of insect galls. Galling species and host plant richness differed significantly among the studied habitats and were higher in slope habitats (drier habitats), as expected. More humid areas (valleys) showed the lowest richness of galling species, and a lower number of understory host plants. PERMANOVA and PERMDISP results demonstrated that the gall species composition differed significantly in the valley, slope, plateau-slope transition, and plateau areas. However, these structural differences in species composition could be due to unequal dispersion of variability among forest habitats. Our data suggested that spatial heterogeneity, such as a mosaic of local water status and nutrient availability resulting from the topographic conditions, can affect host plants and their associated galling insects. KEYWORDS: habitat stress, soil nutrients, species diversity, terra firme forest, topographic gradient Riqueza de insetos galhadores associados a habitats de sub-bosque com diferentes topografias e níveis de estresse hídrico e nutricional em uma floresta da Amazônia Central, Brasil RESUMOAs variações topográficas encontradas nas florestas de terra firme são acompanhadas por fortes mudanças no conteúdo de argila e concentração de nutrientes do solo, criando, portanto, diferentes condições hídricas e nutricionais para plantas e as comunidades de herbívoros associadas. O objetivo do presente estudo foi avaliar a riqueza e composição de espécies de insetos galhadores e suas plantas hospedeiras ao longo de um gradiente topográfico com habitats que diferem quanto ao estresse hídrico e nutricional. Dezenove parcelas de 250 x 3 m foram estabelecidos aleatoriamente em habitats de vertente, platô, transição platô-vertente e baixio, claramente distintos em áreas de terra firme. Todas as dicotiledôneas com 1 a 3 metros de altura foram examinadas quanto à presença de galhas de insetos. As galhas encontradas foram coletadas e insetos galhadores foram classificados em morfoespécies. A riqueza de galhadores e de plantas hospedeiras diferiram significativamente entre os habitats estudados, e como esperado, foi maior no habitat de vertente. As áreas mais úmidas (baixios) apresentaram menor riqueza de plantas hospedeiras no sub-bosque e, conseqüentemente, um número menor de espécies de galhadores. Os resultados das análises de PERMANOVA e P...

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

Cited by 147 publications

References 78 publications

Immunocytochemical demonstration of cell wall components related to tissue compartments in the globoid galls induced by Clinodiplosis sp. (Cecidomyiidae) on Croton floribundus Spreng. (Euphorbiaceae)

Immunocytochemical demonstration of cell wall components related to tissue compartments in the globoid galls induced by Clinodiplosis sp. (Cecidomyiidae) on Croton floribundus Spreng. (Euphorbiaceae)

Sink Status and Photosynthetic Rate of the Leaflet Galls Induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae)

Understory host plant and insect gall diversity changes across topographic habitats differing in nutrient and water stress in the Brazilian Amazon rainforest

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