Virulent Hessian Fly (Diptera: Cecidomyiidae) Larvae Induce a Nutritive Tissue During Compatible Interactions with Wheat

Abstract

The compatible interaction between virulent Hessian fly, Mayetiola destructor (Say), larvae and susceptible wheat, Triticum aestivum L., plants was investigated at the light microscope and ultrastructural levels. During the first day of larval attack at the base of the sheath of the third leaf of a wheat seedling, small punctures of the appropriate size (0.1 μm in diameter) and spacing of the paired larval mandibles were found in the outer wall of epidermal cells. Inside epidermal cells, nuclei and cytoplasmic organelles seemed to be breaking down, and the number and size of cytoplasmic vacuoles had increased. Two to 3 d later, epidermal and mesophyll cells at the base of the third leaf showed signs of becoming nutritive. Nutritive cells were identified by an increase in cytoplasmic staining, increased numbers of cellular organelles (mitochondria, proplastids, Golgi, and rough endoplasmic reticulum), numerous small vacuoles, and an irregularly shaped nucleus. The Hessian fly nutritive tissue probably acts as a sink tissue within the wheat seedling, benefiting the growth of larvae by importing photoassimilates. Breakdown of nutritive cells began soon after they were first observed, indicated by a change in the shape and density of the cell nucleus. Contents of nutritive cells moved through compromised cell walls into adjacent cells that had a more complete breakdown and loss of cytoplasm. Structural changes were not restricted to the third leaf. The sixth leaf, a leaf more recently initiated by the shoot apical meristem that was not directly fed upon by larvae, was found to consist primarily of well-developed epidermal layers, with poorly developed mesophyll cells. The implications of these findings for understanding incompatible interactions between avirulent Hessian fly larvae and R gene-defended plants are briefly discussed.