Endophytes versus biotrophic and necrotrophic pathogens—are fungal lifestyles evolutionarily stable traits?

Abstract

Endophytes infect living plant tissues without causing symptoms of disease. Indeed, many of them contribute to the resistance phenotype of their host. However, fungal endophytes are generally closely related to plant pathogens, fungi that either develop within living host tissue (biotrophic fungi) or that kill the host cells and then live in the dead tissue (necrotrophic fungi). We adopted a phylogenetic approach to investigate whether these strategies represent evolutionarily stable lifestyles and to elucidate their general phylogenetic relationships. We analysed 163 fungal strains for which we found information on the sequence of the 5.8S rRNA gene and the flanking internal transcribed spacer regions, the identity of the host plant and the concrete phenotypic outcome of the infection. A Maximum-Likelihood analysis combined with ancestral character mapping by maximum parsimony revealed that some fungal lineages had switched multiple times between a necrotrophic and an endophytic lifestyle. Ancestral character mapping indicated a minimum of four changes from an endophytic to a necrotrophic lifestyle, four changes in the opposite direction and eight changes among these lifestyles for which the direction could not be determined unambiguously. By contrast, biotrophs formed five clusters that did not contain necrotrophs or endophytes. Once biotrophy evolves there is apparently no regression to one of the other two lifestyles. We conclude that biotrophy usually represents a derived and evolutionarily stable trait, whereas fungi easily can switch between an endophytic and necrotrophic lifestyle at the evolutionary and even the ecological timescale. Future experimental studies should focus on the environmental or genetic changes that cause the rapid switches between these two phenotypically different lifestyles.