Ethylene sensing and gene activation in Botrytis cinerea: a missing link in ethylene regulation of fungus-plant interactions?

Ethylene production by infected plants is an early resistance response leading to activation of plant defense pathways. However, plant pathogens also are capable of producing ethylene, and ethylene might have an effect not only on the plant but on the pathogen as well. Therefore, ethylene may play a dual role in fungus-plant interactions by affecting the plant as well as the pathogen. To address this question, we studied the effects of ethylene on the gray mold fungus Botrytis cinerea and the disease it causes on Nicotiana benthamiana plants. Exposure of B. cinerea to ethylene inhibited mycelium growth in vitro and caused transcriptional changes in a large number of fungal genes. A screen of fungal signaling mutants revealed a Galpha null mutant (deltabcg1) which was ethylene insensitive, overproduced ethylene in vitro, and showed considerable transcriptional changes in response to ethylene compared with the wild type. Aminoethoxyvinylglycine (AVG)-treated, ethylene-nonproducing N. benthamiana plants developed much larger necroses than ethylene-producing plants, whereas addition of ethylene to AVG-treated leaves restricted disease spreading. Ethylene also affected fungal gene expression in planta. Expression of a putative pathogenicity fungal gene, bcspl1, was enhanced 24 h after inoculation in ethylene-producing plants but only 48 h after inoculation in ethylene-nonproducing plants. Our results show that the responses of B. cinerea to ethylene are partly mediated by a G protein signaling pathway, and that ethylene-induced plant resistance might involve effects of plant ethylene on both the plant and the fungus.