Biotic and Abiotic Stress Tolerance of Phenylalanine Ammonia Lyase-Suppressed Brachypodium

The phenylpropanoid pathway in plants synthesizes a variety of structural and defence compounds, and is an important target in efforts to reduce cell wall lignin for improved biomass conversion to biofuels. Pathway manipulations can have undesired effects on plant fitness and biomass yield. To gain new insights into the phenylpropanoid pathway and related processes, we targeted by RNA interference (RNAi) PHENYLALANINE AMMONIA LYASE (PAL) isoforms in the model grass Brachypodium distachyon; PAL enzymes catalyse the first pathway step. BdPAL RNAi plants were found to have large reductions (up to 85%) in transcript abundance for two of the eight putative BdPAL genes. Along with a 43% reduction in lignin and a nearly two-fold increase in the amounts of polysaccharide-derived carbohydrates released by thermochemical and hydrolytic enzymic partial digestion, BdPAL-suppressed plants’ cell walls had a 57% reduction in ferulate, suggesting a shared biosynthetic route for lignin-bound monolignols and hemicellulose-bound ferulate. PAL-suppressed plants exhibited increased susceptibilities to the fungal pathogens Fusarium culmorum and Magnaporthe oryzae, but surprisingly had wild-type (WT) resistances to caterpillar herbivory, drought, and ultraviolet light. Drug studies and RNA-seq data analyses revealed that the PAL-suppressed plants’ reduced root growth and fungal susceptibility phenotypes were partially a consequence of increased ethylene production and subsequent signalling. These data reveal that trade-offs exist in how Brachypodium, and likely other grasses, respond to challenges involving the phenylpropanoid pathway, and provide targets for enhancing the fitness of economically important grasses including bioenergy-crop grasses having reduced cell wall lignin.