Jasmonic acid signalling mediates resistance of the wild tobacco Nicotiana attenuata to its native Fusarium, but not Alternaria, fungal pathogens

Abstract

We recently characterized a highly dynamic fungal disease outbreak in native populations of Nicotiana attenuata in the southwestern United States. Here, we explore how phytohormone signalling contributes to the observed disease dynamics. Single inoculation with three native Fusarium and Alternaria fungal pathogens, isolated from diseased plants growing in native populations, resulted in disease symptoms characteristic for each pathogen species. While Alternaria sp.-infected plants displayed fewer symptoms and recovered, Fusarium spp.-infected plants became chlorotic and frequently spontaneously wilted. Jasmonic acid (JA) and salicylic acid (SA) levels were differentially induced after Fusarium or Alternaria infection. Transgenic N.attenuata lines silenced in JA production or JA conjugation to isoleucine (JA-Ile), but not in JA perception, were highly susceptible to infection by F.brachygibbosumUtah 4, indicating that products derived from the JA-Ile biosynthetic pathway, but not their perception, is associated with increased Fusarium resistance. Infection assays using ov-nahG plants which were silenced in pathogen-induced SA accumulations revealed that SA may increase N.attenuata's resistance to Fusarium infection but not to Alternaria. Taken together, we propose that the dynamics of fungal disease symptoms among plants in native populations may be explained by a complex interplay of phytohormone responses to attack by multiple pathogens. Our study examines the phytohormone-mediated signaling responses of the wild tobacco plant to its native fungal pathogens and provides insights into the dynamics of pathogen attack in a natural environment. Three native fungal pathogen species of Fusarium and Alternaria induce different salicylic and jasmonic acid responses in their wild tobacco host plant, which results in disease symptoms characteristic for each pathogen. By using transgenic lines, the trade-offs between JA- and SA- mediated defense responses was analyzed in a situation in which plants were under attack from hemi-biotrophic Fusarium species (SA-mediated response) and necrotrophic Alternaria species (JA-mediated response).