Survey of the Taxonomic and Tissue Distribution of Microsomal Binding Sites for the Non-Host Selective Fungal Phytotoxin, Fusicoccin

Abstract

The recent identification of the fusicoccin-binding protein (FCBP) in plasma membranes from monocotyledonous and dicotyledonous angiosperms has opened the basis for an elucidation of the toxin’s mechanism(s) of action and indicated a widespread occurrence of the FCBP in plants. Results of a detailed taxonomic survey of fusicoccin-binding sites are reported. Binding sites were not found in prokaryotes, animal tissues, fungi and algae including the most direct extant ancestors of the land plants (Coleochaete). From the Psilotales (Psilophytatae) to the monocotyledonous angiosperms, all taxa analyzed possessed high-affinity microsomal fusicoccin-binding sites. A heterogeneous picture emerged for the Bryophvta. Anthoceros crispulus (Anthocerotae), the only hornwort available to study, lacked fusicoccin binding. Within the Hepaticae as well as the Musci, species lacking and species exhibiting toxin binding were found. The binding site thus seems to have emerged very early in the evolution of the land plants. The tissue distribution of fusicoccin-binding sites was studied in Vicia faba L. shoots. All tissues analyzed showed fusicoccin binding, although not to the same extent. On a per-cell basis, guard cells were found to contain, compared to mesophyll cells, a nine-fold higher number of binding sites. Based on cell surface area, the site density is by a factor of 32 higher in guard cells than in mesophyll cells. Tissue specific expression of the binding sites is suggested by these findings.

Summary

“…However, fusicoccin binding sites could not be detected in Saccharomyces cerevisiae (Meyer et al, 1993). We therefore tested the possibility that expression of plant H ϩ -ATPase in yeast generates fusicoccin receptors.…”

“…The role of 14-3-3 proteins in the binding of fusicoccin, however, has remained unresolved. Despite the fact that 14-3-3 proteins are well conserved in eukaryotes, fusicoccin binding activity has only been detected in plants (Meyer et al, 1993) and expression of plant 14-3-3 proteins in yeast failed to create fusicoccin binding sites (Andersen, 1997).…”

Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis

“…Binding of 14-3-3 to the Cterminal (regulatory) domain of the H + pump releases its autoinhibitory action (Baunsgaard et al, 1998;Palmgren, 2001), which results in increased H + -extrusion along with changes in cytoplasmic pH (Felle et al, 1986). Despite the considerable structural conservation of 14-3-3 proteins from plants and animals (Fu et al, 2000;Sehnke et al, 2002), and the large number of 14-3-3 partners identified thus far in both kingdoms (Van Hemert et al, 2001), the presence of FC binding sites in organisms other than higher plants has never been demonstrated (Meyer et al, 1993).…”

The fusicoccin receptor of plants is a member of the 14‐3‐3 superfamily of eukaryotic regulatory proteins

“…The toxin activates the ATPase by a mechanism involving the C-terminal autoinhibitory domain of the enzyme [2] and exerts its effects by means of a high-affinity binding protein (FCBP) located at the plasma membrane of plants . The FCBP exhibits conserved biochemical properties in all species studied so far and occurs ubiquitous from the mosses to the angiosperms [9]. Mutants of Arabidopsis thaliana with reduced binding affinity of the FCBP towards FC are toxin insensitive and show greatly reduced or lacking physiological responses to FC, proving that the FCBP represents the plant's FC receptor [lo].…”