The role of ethylene perception in plant disease resistance

Abstract

Ethylene is a plant hormone that is involved in responses of the plant to various stress situations, such as pathogen attack. The role of ethylene in plant-pathogen interactions seems to be diverse. Exposure of plants to ethylene can induce disease resistance, but treatment with ethylene during disease development can also increase symptom development. Transgenic, ethylene-insensitive tobacco plants (Tetr) that are grown in normal potting soil spontaneously develop wilting and stem rot, whereas tobacco plants that are not transformed do not. Various fungi and were isolated from such diseased Tetr tobacco plants. These isolates caused disease in Tetr tobacco when inoculated onto plants growing in soil that was sterilized by autoclaving. Non-transformed tobacco developed less severe or no disease at all when inoculated in a similar manner. Similarly, in Arabidopsis ethylene-insensitive mutants appeared to be more susceptible to these microorganisms than wild-type plants. These results indicate that in tobacco and Arabidopsis similar resistance mechanisms are impaired by insensitivity to ethylene. In addition, it was demonstrated that Tetr tobacco allows more growth of Pythium than non-transformed plants. A culturing-independent, molecular approach was used to examine microorganisms that colonize Tetr plants growing in potting soil. Using specific primers for PCR, bacterial, fungal, and oomycete populations were examined in roots of non-transformed and Tetr plants, growing either in non-autoclaved or autoclaved soil. Before the onset of disease development, plants growing in non-autoclaved soil contained microbial populations that were completely different from those of plants growing in autoclaved soil. Moreover, bacterial and oomycete populations on the roots of non-diseased plants differed between non-transformed and Tetr tobacco, indicating that ethylene sensitivity affects microbial development in the root system. Analysis of spontaneously diseased Tetr plants growing in non-autoclaved soil demonstrated that the stems of young plants were primarily colonized by oomycetes, whereas stems of older plants were colonized mainly by fungi. Various necrotrophic and biotrophic pathogens were tested on non-transformed and Tetr plants. In general, Tetr plants were more susceptible to necrotrophic bacteria, fungi, and oomycetes, that cause symptoms of necrosis and / or rotting, but not to biotrophic fungi, oomycetes and tobacco mosaic virus, which require living host tissues. Ethylene-insensitive Arabidopsis plants are likewise more susceptible to necrotrophic, but not to biotrophic pathogens. Both ethylene-insensitive tobacco and Arabidopsis displayed reduced activity of peroxidase, an enzyme often associated with disease resistance. Apparently, in tobacco and Arabidopsis ethylene insensitivity impairs the same kind of disease resistance mechanisms, resulting in enhanced susceptibility to a similar range of pathogens. We investigated whether resistance in Tetr plants can be restored by treatments that are known to protect plants against diseases.Treatments of Tetr tobacco with chemicals that induced expression of genes encoding pathogenesis-related (PR) proteins, did not reduce disease development. Overexpression of PR genes in the transgenic Tetr plants did not enhance resistance either. Also rhizobacteria that induce systemic resistance in tobacco and other plant species, or that directly antagonize pathogen growth, did not effectively protect Tetr plants. These results indicate that it is difficult to counteract the enhanced disease susceptibility of ethylene-insensitive Tetr tobacco plants. Apparently, ethylene signaling plays a central role in basal disease resistance against necrotrophic microorganisms.