Structure and host–actinomycete interactions in developing root nodules of Comptonia peregrina

Abstract

Correlated fluorescence, bright-field, transmission electron, and scanning electron microscopic studies were made on developing root nodules of Comptonia peregrina (L.) Coult. (Myricaceae) produced by a soil actinomycete which invades the root and establishes a symbiosis leading to fixation of atmospheric dinitrogen. After entering the host via a root hair infection, the hyphae of the endophyte perforate root cortical cells by local degradation of host cell walls and penetration of the host cytoplasm. The intracellular hyphae are always surrounded by host plasma membrane and a thick polysaccharide material termed the capsule. (For convenience, term intracellular refers to the endophyte being inside a Comptonia cell as distinguished from being intercellular, i.e.. between host cells, even though the former is actually extracellular as the endophyte is separated from the host cytoplasm by the host plasmalemma.) Numerous profiles of vesiculate rough endoplasmic reticulum (RER) occur near the growing hyphae. Although the capsule shows a positive Thiery reaction indicating its polysaccharide nature, the fibrillar contents of the RER do not, leaving uncertain whether the capsule results from polymers derived from the RER. Amyloplasts of the cortical cells lose their starch deposits during hyphal proliferation. The hyphae branch extensively in specific layers of the cortex, penetrating much of the host cytoplasm. At this stage, hyphal ends become swollen and form septate club-shaped vesicles within the periphery of the host cells. Lipid-like inclusions and Thiery-positive particles, possibly glycogen, are observed in the hyphae at this time. Associated with hyphal development is an increase in average host cell volume, although nuclear volume appears to remain constant. Concomitant with vesicle maturation, the mitochondrial population increases sharply, suggesting a possible relationship to vesicle function. The intimate interactions between host and endophyte during development of the symbiotic relationship are emphasized throughout.