Ana Sílvia Franco Pinheiro Moreira

Is the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf photosynthesis

The generation of ROS (reactive oxygen species) in plant galls may induce the degradation of the membrane systems of a plant cell and increase the number of plastoglobules. This numerical increase has been related to the prevention of damage to the thylakoid systems, and to the maintenance of photosynthesis rates. To investigate this hypothesis in gall systems, a comparative study of the ultrastructure of chloroplasts in non-galled leaves and in leaf galls of A. australe and A. spruceanum was conducted. Also, the pigment composition and the photosynthetic performance as estimated by chlorophyll fluorescence measurements were evaluated. The ultrastructural analyses revealed an increase in the number and size of plastoglobules in galls of both species studied. The levels of total chlorophylls and carotenoids were lower in galls than in non-galled tissues. The chlorophyll a/b ratio did not differ between the non-galled tissues and both kinds of galls. The values of maximum electron transport rate (ETR(MAX)) were similar for all the samples. The occurrence of numerous large plastoglobules in the galled tissues seemed to be related to oxidative stress and to the recovery of the thylakoid membrane systems. The maintenance of the ETR(MAX) values indicated the existence of an efficient strategy to maintain similar photosynthetic rates in galled and non-galled tissues.

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

BACKGROUND Galls have specialized tissues for the protection and nutrition of the inducers, and these tissues have been studied from the developmental and histochemical perspectives. Recently, the role of oxidative stress in galls has been tested histochemically through detection of H2O2 in gall tissues. SCOPE OF REVIEW Developmental processes and cytological events are revisited from the perspective of the redox-potential balance in both the apoplast and symplast, especially concerning the accumulation of reactive oxygen species (ROS). MAJOR CONCLUSIONS The redox potential is imbalanced differently in the apoplast and symplast at gall sites, with the apoplast having lower antioxidant-buffering capacity than the symplast. The strategies to recover redox-potential homeostasis involve the dissipation of ROS by scavenging molecules, such as phenolics, flavonoid derivatives, tocopherol, and enzyme systems. GENERAL SIGNIFICANCE Insect galls are good models to test developmental hypotheses. Although the exact mechanisms of gall induction and development have not been elucidated at the biochemical and biophysical levels, modulation of the redox potential is involved in the crucial steps of gall initiation and establishment. This article is part of a Special Issue entitled Redox regulation of differentiation and de-differentiation.

Phenological relationships between two insect galls and their host plants: Aspidosperma australe and A. spruceanum (Apocynaceae)

Phenological relationships between two insect galls and their host plants: Aspidosperma australe and A. spruceanum (Apocynaceae)). Although gall diversity in the Neotropical region is immense, comparative studies on the phenology of host plants and their galls are scarce. Gall systems generally require high levels of phenological synchrony between the associated organisms. The relationships between the phenology of two leaf galls induced by an unidentifi ed Cecidomyiidae in Aspidosperma spruceanum Benth. ex Muell. Arg. and by Pseudophacopteron sp. in A. australe Muell. Arg. were investigated. The investigation was performed on ten individuals per species in 15-day intervals taking into consideration the percentage of galled leaves. In a one-year study, three distinct phenophases for the leaf galls and four phenophases for host plants were observed. The maximum percentage of leaf galls (80%) on A. australe occurred just after the peak of leaf sprouting. In A. spruceanum, the percentage of leaf galls was always over 50%, which can be related to continuous leaf production and gall induction in this species. In both species, developing galls were observed over the entire year, indicating multivoltinism. The ability to induce galls at young and mature sites seems to be a good strategy for galling species survivorship.

Water stress and phenological synchronism between Copaifera langsdorffii (Fabaceae) and multiple galling insects: formation of seasonal patterns

Abstract The gall-induction rates in a population of the superhost Copaifera langsdorffii, located in a rocky field vegetation in Brazil, should follow sprouting events and water availability. The presence or absence of leaf flushing, the activity index for the vegetative phenophases, and the water potential were used to test this hypothesis, and ordination via canonical correspondence analysis was employed to test possible synchronisms. Based on 6881 sampled galls, three seasonal syndromes were observed for nine distinct morphotypes along a one-year cycle. The first syndrome related the decrease in the abundance of horn-shaped and cup-shaped galls with dry season. The second one revealed that other four morphotypes adjusted their cycles to leaf flushing, and the third syndrome involved three galls which occurred homogeneously along the year, with a tenuous peak of abundance in July. These syndromes reflect a strategy towards the occupation of distinct temporal niches on the same host plant.

Nitric oxide increases tolerance responses to moderate water deficit in leaves of Phaseolus vulgaris and Vigna unguiculata bean species.

Drought stress is one of the most intensively studied and widespread constraints, and nitric oxide (NO) is a key signaling molecule involved in the mediation of abiotic stresses in plants. We demonstrated that a sprayed solution of NO from donor sodium nitroprusside increased drought stress tolerance responses in both sensitive (Phaseolus vulgaris) and tolerant (Vigna unguiculata) beans. In intact plants subjected to halting irrigation, NO increased the leaf relative water content and stomatal conductance in both species. After cutting leaf discs and washing them, NO induced increased electrolyte leakage, which was more evident in the tolerant species. These leaf discs were then subjected to different water deficits, simulating moderate and severe drought stress conditions through polyethylene glycol solutions. NO supplied at moderate drought stress revealed a reduced membrane injury index in sensitive species. In hydrated discs and at this level of water deficit, NO increased the electron transport rate in both species, and a reduction of these rates was observed at severe stress levels. Taken together, it can be shown that NO has an effective role in ameliorating drought stress effects, activating tolerance responses at moderate water deficit levels and in both bean species which present differential drought tolerance.

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

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.

Functional Gradients in Insect Gall Tissues: Studies on Neotropical Host Plants

The first mechanism by which the insect recognizes its host plant was not elucidated yet. Once the induction occurs, the plant, in general, responds by the redifferentiation of tissues with typical features and functions of a new organ. These tissues may guarantee adaptive advantages to the galling insect against natural enemies, microenvironmental stresses, and also provide adequate nutrition. Moreover, the formation of the final gall body, i.e., its morphological design, is directly related to the formation of the tissues of the gall. This is especially true for the reserve tissue or the outer cortex, and the nutritive tissue or inner cortex. Interesting questions to be addressed are how these tissues differentiate, and whether cytological and histochemical gradients are developed in galls. In fact, these gradients seem to occur in the majority of the galls, and their formation may be related to the formation of reactive oxygen species (ROS) since the onset of the interaction.

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.

Do leaf traits in two Dalbergia species present differential plasticity in relation to light according to their habitat of origin

The phenotypic plasticity to light of two congeneric species of leguminous trees from distinct habitats was evaluated in a common-garden experiment. For that, we assessed the following two groups of leaf morphological and anatomical traits of 1-year-old seedlings: (1) traits related to light interception (tissues thickness and leaflet mass per area), and (2) traits related to gas exchange (number of leaflets per leaf and measurements of stomatal size and density). Dalbergia nigra (Vell.) Allemao ex Benth. is an endemic Atlantic forest species, and D. miscolobium Benth. is a typical cerrado species. Both were grown under shade and full-sunlight conditions. The phenotypic plasticity of leaves was determined by a relative distance plasticity index (RDPI). For both species, sun leaflets were thicker than shade ones, and only D. nigra presented lower values for stomatal density (nst), percentage of the leaflet area occupied by stomatal pores (nast) and estimated stomatal conductance (gst) under shade conditions. The forest species (D. nigra) had higher plasticity for variables related to gas exchange (number of leaflets per leaf, nst, ast, nast and gst), whereas the cerrado species (D. miscolobium) had higher plasticity for variables related to light interception, such as leaflet mass per area, leaflet thickness and palisade and spongy parenchyma thickness. The degree of plasticity was different for each analysed parameter, and not used to define which species is more plastic. The leaf traits of D. nigra and D. miscolobium that showed high plasticity were related to resources that are not limiting to improve its photosynthesis in a changing light environment.

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

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.