Nutritive tissue rich in reserves in the cell wall and protoplast: the case of Manihot esculenta (Euphorbiaceae) galls induced by Iatrophobia brasiliensis (Diptera, Cecidomyiidae)

Protoplasma. 2024 May;261(3):513-525. doi: 10.1007/s00709-023-01912-z. Epub 2023 Dec 19.

Abstract

The galls can offer shelter, protection, and an adequate diet for the gall-inducing organisms. Herein, we evaluated the structure of Manihot esculenta leaves and galls induced by Iatrophobia brasiliensis in order to identify metabolic and cell wall composition changes. We expected to find a complex gall with high primary metabolism in a typical nutritive tissue. Non-galled leaves and galls were subjected to anatomical, histochemical, and immunocytochemical analyses to evaluate the structural features, primary and secondary metabolites, and glycoproteins, pectins, and hemicelluloses in the cell wall. The gall is cylindric, with a uniseriate epidermis, a larval chamber, and a parenchymatic cortex divided into outer and inner compartments. The outer compartment has large cells with intercellular spaces and stocks starch and is designated as storage tissue. Reducing sugars, proteins, phenolic compounds, and alkaloids were detected in the protoplast of inner tissue cells of galls, named nutritive tissue, which presents five layers of compact small cells. Cell walls with esterified homogalacturonans (HGs) occurred in some cells of the galls indicating the continuous biosynthesis of HGs. For both non-galled leaves and galls, galactans and xyloglucans were broadly labeled on the cell walls, indicating a cell growth capacity and cell wall stiffness, respectively. The cell wall of the nutritive tissue had wide labeling for glycoproteins, HGs, heteroxylans, and xyloglucans, which can be used as source for the diet of the galling insect. Manihot esculenta galls have compartments specialized in the protection and feeding of the galling insect, structured by nutritive tissue rich in resource compounds, in the cell walls and protoplast.

Keywords: Cassava; Hemicellulose; Pectin; Protein; Sugar.

MeSH terms

  • Animals
  • Cell Wall
  • Diptera*
  • Euphorbiaceae*
  • Glycoproteins / metabolism
  • Manihot*
  • Phobic Disorders*
  • Plant Leaves / metabolism
  • Plant Tumors
  • Protoplasts

Substances

  • Glycoproteins

Supplementary concepts

  • Iatrophobia