Ultrastructure of root cortical cells parasitized by the ring nematodeCriconemella xenoplax

Summary

Individuals of the plant-parasitic nematodeCriconemella xenoplax, monoxenically cultured on root expiants of clover, carnation, and tomato, fed continuously for up to 8 days from single cells in the outer root cortex. Individual cortical cells parasitized by nematodes were modified into discrete “food cells” in all hosts examined. The nematode's stylet penetrated between epidermal cells and frequently through a subepidermal cortical cell. Electron-transparent callose-like material continuous with the cell wall enveloped the portion of the stylet that traversed subepidermal cortical cells. Food cells were typically located in the first or second cell layers of the cortex. The stylet penetrated 5–6 μm through the wall of the food cell without penetrating the plasma membrane. Electron-transparent callose-like deposits formed between the invaginated plasma membrane and stylet, except at its aperture. The plasma membrane of the food cell was appressed tightly to the wall of the stylet aperture creating a 130–160 nm hole in the membrane. This opening provided continuity between the lumen of the stylet and the food cell cytosol for ingestion of nutrients by the nematode. Ribosomes were dissociated from the cisternae of the endoplasmic reticulum in food cells and accumulated with other cell organelles in a zone of modified cytoplasm around the stylet. A fibrillar material appeared to form a barrier in the cytosol around the stylet aperture that limited movement of cell organelles toward the aperture. Electron-dense secretory components were secreted into the food cell by the nematode. Clusters of putative nematode secretory components consisting of 20–40 nm diameter, electron-dense particles were dispersed in the densely particulate zone of cytoplasm around the stylet tip. The cytosol immediately around the stylet aperture in the center of the modified cytoplasm was finely granular.

Plasmodesmata connecting the cytoplasm of the food cell with the cytoplasm of neighboring cells were greatly modified in a way that could facilitate solute transport into the food cell. The plasma membrane-lined canals of the modified plasmodesmata appeared to be increased in diameter and lacked desmotubules. Additionally, they frequently were lengthened by electron-transparent callose-like deposits projecting from the wall into the cytoplasm of the food cell. An electron-dense “cap” that formed an apparent tight seal with the plasma membrane developed over the entrance of each modified plasmodesma in the neighboring cells. These caps excluded all cell organelles from the cytosol contained within them. The nucleus of the food cell was usually enlarged and atypically shaped with dense peripheral clumps of condensed chromatin. Our results show thatC. xenoplax induces elaborate cellular modifications in host tissue to support sustained ingestion of nutrients from a single food cell.