ANOTHER BRICK IN GALL WALLS

Rosy Isaias; Denis Coelho de Oliveira; Renê Gonçalves da Silva Carneiro; Bruno Garcia Ferreira

All Papers

Submission

Paper Title

ANOTHER BRICK IN GALL WALLS

Authors

Rosy Isaias
Denis Coelho de Oliveira
Renê Gonçalves da Silva Carneiro
Bruno Garcia Ferreira

Modality

Lecture

Subject area

Biology of Galls

Publishing Date

05/05/2021

Country of Publishing

Brasil

Language of Publishing

Inglês

Paper Page

https://www.even3.com.br/anais/2ndbiologyofgalls/330959-another-brick-in-gall-walls

ISBN

978-65-5941-213-6

Keywords

auxins, cell walls, cytokinins, development, gall anatomy, ROS

Summary

All living organisms are composed of cells, as states the cell theory. The cells are elementary units both of plant and gall bodies, like the bricks are the elementary units of the walls of human constructions. The investigation of the dynamics of cell wall components help us understand the cascade of events involved in gall development from the host plant metabolism perspective. The mystery involving this cascade of events has intrigued many cecidologists, and such investigation guides one of the lines of research pursued by the Neotropical gall group. The host plant-galling herbivore interactions have been interpreted as true efforts to confer protection and nutrition and keep the galling organism alive. Moreover, from the plant metabolism perspective, all the efforts to keep the galling organism alive demands keeping plant cells alive, as well. The attempt of using galls as micro-laboratories to investigate plant reactions at the cellular level has revealed important pieces to solve the great puzzle of the triggering and orchestration of gall development. We address plant responses involved in such processes by five lines of research on galls in the Brazilian flora: morphology, histology, cytology, histochemistry, and immunocytochemistry. Our first premise is that the accumulation of each molecule in gall developmental sites indicates a response of plant cells toward the alien stimuli, but in an attempt to avoid imbalanced homeostasis and to keep their metabolic viability. The quite common histochemical detection of phenolics in gall induction sites, usually interpreted as a chemical defense against natural enemies, from the plant perspective may be interpreted as the reaction toward scavenging the excess of oxidants. The overgeneration of reactive oxygen species (ROS) due to the direct contact of galling organisms with plant tissues can be detected in two cell compartments: the symplast and the apoplast. The biochemical and biophysical reactions in the inner side of the plasma membrane and in cell walls lead to cell redifferentiation, and new tissue layer organization. The peculiar orchestration of the cell and tissue responses in each host plant-galling herbivore system culminates in the development of the variety of gall morphotypes. The ROS have been histochemically detected in nutritive cells, vascular bundles, and photosynthetic parenchyma, and the scavenging of ROS molecules performed by the phenolics modulates cell reprogramming. The co-occurrence of ROS, phenolics, and indol-3-acetic acid (IAA) in cells of some super-hosts of galling herbivores has been interpreted as evidence of the involvement of these compounds in the coordinated control of gall growth. Hence, the accumulation of phenolics as a metabolic strategy to scavenge de excess of ROS results in the blockage of IAA-oxidases, which results in the increase in IAA concentration in gall developmental sites. This molecular interaction favors the occurrence of the acid growth and consequently, of cell hypertrophy. The overlapping of ROS, IAA and phenolics in specific tissue compartments contributes to the generation of the specific gall morphotypes as their detection relates to specific spatial and temporal dynamics. As this premise solves the mystery of signaling toward cell hypertrophy, the missing brick regards the increment in cell division, the hyperplasia. Suck mystery has been investigated by histochemical and immunocytochemical detection both of IAA and cytokinins (CKs) and has been elegantly demonstrated in gall morphotypes associated to super-host plants. Curiously, gall tissues where IAAs and phenolics co-occur have higher degrees of cell hypertrophy, while sites CKs accumulation have smaller cells, as indicative of increased cell divisions, i.e., hyperplasia. The CKs were detected in tissue compartments distinct from those where IAA and phenolics occurred in galls in growth and development stage. The mapping of the phytohormones in spatial and temporal scales on distinct gall morphotypes associated to super-host plants corroborates our hypotheses on the roles of IAAs, phenolics and CKs, and help setting lights on the mechanisms of gall shape determination. In addition, the histochemical localization both of IAA and CKs were confirmed with the use of polyclonal antibodies. The variety of gall morphotypes observed in nature involve not only events of cell hypertrophy and tissue hyperplasia, but also alterations in subcellular level. The dynamics of cell wall components along gall developmental stages have been studied to understand how ordinary conditions of plant cells are changed toward new structural and functional profiles. Immunocytochemical studies have assessed cell wall components of galls induced by insects, mites, and nematodes. The main component of plant cell walls, the cellulose, and the remodeling of its microfibrils have been demonstrated by the calcofluor white fluorescence, and as expected confirmed that alterations in shapes demands adjustments in the isotropic and anisotropic patterns of cell growth. We have been testing if the predominance of isotropic elongation of cell axis may relate to the development of isodiametric shapes, such as the globoid morphotypes. In fact, the patterns of cell elongation vary across the different tissue compartments, i.e., the cell layers with specific structural and functional traits, and regarding gall developmental stages, even when similar gall morphotypes are compared. For the uncommon and bizarre shapes, the predominance of anisotropic elongation in cell axis in specific tissue layers is expected, and the spatial dynamics of isotropic and anisotropic elongations may explain each specific gall shape. Together with the cellulose, hemicelluloses also have functional traits other than the ordinary role of anchorage of cellulose microfibrils in gall developmental sites. These cell wall components have contributed to the increase in resistance of secondary cell walls from young gall stages toward gall maturation, as is the case of the xylans labeled by the monoclonal antibody LM10 in cell walls of the mechanical gall tissues. Other two types of hemicelluloses, the xyloglucans and the heteromannans, have been labeled in nutritive cell walls, where their functional role has been accredited to the nutritional support to the galling herbivores. These hemicelluloses are additional carbohydrate reserves, that together with reducing sugars, lipids and proteins, may be assessed by the inducers according to their specific modes of feeding. Finally, the dynamics of pectins in galls induced by Diptera: Cecidomyiidae and Hemiptera: Psylloidea has indicated higher rigidity along gall maturation and higher porosity from the outer toward the inner tissue compartment. The cell wall porosity ensures a transferring pathway for the nutritional molecules through the apoplast of the outer tissue compartment cells toward the nutritive cells. Regarding the proteins, the functions performed by the arabinogalactan-proteins (AGPs) are still controversial as their labeling is not constant either in temporal or spatial scale in gall developmental sites. The AGPs are associated not only with the cell walls but also with the plasma membrane and the intercellular spaces, and their ordinary functional roles rely on the contribution to cell divisions and expansion. The AGPs may also be important in blocking processes of cell death that would interrupt gall development. The extensins, another class of proteins we have been investigating, should be labeled at the end of cell expansion as their classical role is determining cell final shape, but in our gall models of study, extensins have been labeled by LM1 in young galls, indicating that the cytological compartments respond peculiarly in specific host plant-galling herbivores systems. In the ultrastructural perspective, plant cells of galls induced by insects, mites, and nematodes respond to the over accumulation of ROS by producing plastoglobules. The plastoglobules contain, among other proteins, tocopherol cyclase, a key enzyme on the biosynthesis of tocopherols, which protect the thylakoid membranes and the proteins related to photosynthesis from oxidative damage caused by the ROS. The plastoglobules are linked to each other and to the membranes of the thylakoids, which allow the exchange of lipophilic molecules between the plastoglobules. The lipophilic molecules serve as electron corridors, and protect the photosynthetic apparatus from damage caused by free radicals. Other cytological evidence of plant cell efforts to survive the impact of gall induction and development is the differentiation of multivesicular bodies, lamellar bodies, and lomassomes. The multivesicular bodies were observed in fast-dividing cells of lepidopteran galls, and are responsible for the rebuilding of the plasma membranes in meristem-like cells. Additionally, lamellar bodies and lomassomes, together with multivesicular bodies, were reported for nutritive cells of galls induced by different insect orders. The oxidative stress confirmed by the detection of ROS in nutritive cells may be compensated by the activity of the lomassomes, lamellar bodies, and multivesicular bodies, which help the endoplasmic reticulum in recycling the endomembrane systems. In summary, our knowledge on plant structure, physiology and chemistry has been used to assemble the pieces of the great puzzle regarding the variety of gall developmental pathways toward the variety of morphotypes. Moreover, we try to understand plant potentialities to deal with the strong stress of the interaction with galling herbivores and keep their cells and tissues alive and metabolic viable. In fact, “all in all these are just bricks in the gall walls”.

Title of the Event: 2nd Symposium on The Biology of Galls
Title of the Proceedings of the event: Annals of the 2nd Symposium on the Biology of Galls
Name of the Publisher: Even3
Means of Dissemination: Meio Digital

How to cite

ISAIAS, Rosy et al.. ANOTHER BRICK IN GALL WALLS.. In: Annals of the 2nd Symposium on the Biology of Galls. Anais...Rio de Janeiro(RJ) UFRJ, 2021. Available in: https//www.even3.com.br/anais/2ndbiologyofgalls/330959-ANOTHER-BRICK-IN-GALL-WALLS. Access in: 21/06/2025