Influence of auxin and phenolic accumulation on the patterns of cell differentiation in distinct gall morphotypes on Piptadenia gonoacantha (Fabaceae)

Abstract

The cascade of biochemical changes occurring at sites of gall development seems to involve a group of common metabolites in plants, namely, the phenolics. Phenolic accumulation has been commonly related to chemical defence, but their primary role seems to be the regulation of cell hypertrophy in galls. Such regulation implies phenolics–auxin (IAA) association at some cell re-differentiation sites, and determines final gall shapes. Herein, we investigated phenolic and auxin accumulation in four gall systems, grouped in two morphotypes, namely lenticular and globoid, induced on pinnulas of Piptadenia gonoacantha (Mart.) J.F.Macbr. Changes in the direction and type of cell expansion between non-galled pinnula and galls were also evaluated. Galling insects associated to lenticular and globoid gall morphotypes promoted changes in host plant cells, leading to the development of different cell sizes, different degrees of anisotropy, and different directions of cell expansion. The accumulation of IAA–phenolics compartmentalised on the basis of gall morphotype, i.e. in the cells of superior and lateral inferior cortices in the lenticular gall morphotypes, and throughout the outer cortex in the globoid gall morphotypes. The sites of accumulation of IAA and phenolics coincided with the most hypertrophied regions, influencing on the determination of the final gall shape.

Enzyme‐mediated metabolism in nutritive tissues of galls induced by Ditylenchus gallaeformans (Nematoda: Anguinidae)

“…The accumulation sites of IAA detected in the current analyses are correspondent to the sites of accumulation of vacuolar (poly)phenols in the same galls (Ferreira et al ). These findings corroborate the proposals of Hori () and Bedetti et al (, ), who described phenolics as important inhibitors of IAA oxidases in some cells of galls, where auxins accumulate, and therefore lead to cell hypertrophy.…”

“…Auxins, detected with Erlich’s reagent in the vacuoles of hypertrophied cells in M. albicans , are usually associated with the promotion of cell cycles (Himanen et al ), cell expansion and vascular tissue differentiation (Yamaguchi et al ). A higher accumulation of IAA was observed in the most hypertrophied cells of non‐galled leaves (in palisade parenchyma, adaxial epidermis and cortical parenchyma) as well as in galls (in CST; Bedetti et al , , ; Suzuki et al ).…”

“…Abnormal growth induced by galling organisms on plants is often mediated by increased levels of auxins (IAA, indole acetic acid) and cytokinins, which ultimately lead to formation of galls via cell hypertrophy and hyperplasia (Byers et al ; Mapes & Davies ,; Yamaguchi et al ; Tooker & Helms ; Favery et al ). In fact, histochemical and immunocytochemical analyses of plant hormones have demonstrated the presence of IAA and cytokinins in insect‐induced galls, mainly in sites where cell division, growth and differentiation are evident (Bedetti et al , , ; Suzuki et al ).…”

“…Root and shoot nematode galls, as insect and mite galls, usually have outer tissue compartments ( sensu Bragança et al ) with hypertrophied cells that accumulate starch and polyphenols (Ferreira et al , , ; Isaias et al ). The accumulation of polyphenols in the outer gall compartments inhibits the activity of IAA oxidase, leading to the accumulation of IAA and, consequently, to cell hypertrophy (Bedetti et al , , ; Suzuki et al ). Outer tissue compartments constitute a common storage tissue (CST) with starch accumulation in galls induced by Ditylenchus gallaeformans (Nematoda: Anguinidae) on leaves and reproductive meristems of Miconia spp.…”

Hemicelluloses and associated compounds determine gall functional traits

“…The alterations in the dynamics of cellulose fibrils–hemicelluloses in the inner tissue compartment may have been mediated by ROS signal transmission (Isaias et al 2015), as H 2 O 2 was the only molecule detected in this gall tissue site. Although phenolic compounds, ROS and IAA were crucial for cell wall flexibility during the development of the gall morphotypes (Suzuki et al 2015; Bedetti et al 2017), each galling herbivore orchestrated cell wall flexibility to generate its own specific gall morphotype through changes in the direction of cell enlargement. In addition to the association with auxin, allowing flexibility to cell walls, phenolic compounds also contribute to cell wall rigidity.…”