Pervasive effects of an endophytic fungus on host genetic and phenotypic expression in a tropical tree

Background/Question/Methods

It is increasingly recognized that macro-organisms are most properly viewed as consisting of both host tissues and multiple microbial symbionts that play an essential role in their host’s ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them, are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) living within their leaf tissues without visible effects on their hosts. Experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here we demonstrate that the phenotypic and genetic effects of FEF are, in fact, pervasive.

Results/Conclusions

The inoculation of endophyte-free (E-) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induced significant, consistent changes in the expression of hundreds of host genes. Further, a cacao gene that confers resistance to pathogen damage in the absence of endophytes was highly up-regulated in E+ leaves. In addition to enhanced pathogen resistance, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (A_max), and enrichment of nitrogen-15 and carbon-13 isotopes that all correspond to changes in expression of specific functional genes in related pathways. Thus, the genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts are, in fact, pervasive. The benefits of increased pathogen resistance in E+ plants due to endophyte-enhanced induction of intrinsic host defense pathways are offset by potential costs including reduced photosynthesis and endophyte metabolism of host tissues. Similar effects are likely properties of most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.