Some plant parasites manipulate their hosts by inducing changes at the attack site. Changes include galls and nutritive tissue, syncytia, giant cells, cankers, and crown galls. Diversion of plant resources to the parasite-induced sink tissue can cause host death or reduced fitness. The parasite derives enhanced nutrition, and may suppress plant defenses. To defend against this highly specific attack, the plant must excel at early parasite detection and rapid defense before parasite manipulation is complete; these occur in gene-for-gene resistance.

We tested the hypothesis that gene-for-gene resistance prevents parasite manipulation. For the interaction between wheat, Triticum aestivum, and the Hessian fly, Mayetiola destructor, plant measurements and light and electron microscopy revealed that larval attack of susceptible and R-gene resistant plants begins with the larva’s tiny mandibles puncturing the outer wall of leaf-sheath epidermal cells. In plants lacking effective R-gene resistance, nutritive cells develop then break down, with cellular contents moving through compromised cell walls. The virulent larva grows rapidly. Leaves younger than the attacked leaf neither elongate nor develop beyond initial epidermal layers. Unless tillers escape larval manipulation, the susceptible plant dies without producing seed. In plants with non-host resistance or host resistance, the avirulent larva initially suppresses leaf growth but dies within 3-5 days. R-gene plants exhibit no nutritive tissue. We confirmed the absence of nutritive tissue in larval-attacked resistant plants for five Hessian-fly-specific R-genes. Cell wall changes are consistent with a localized defense response, and resistant plants ultimately suffer no fitness deficit.