A Systems Approach to Elucidate the Impact of Gene-Environment Interactions on an Engineered Crop

Switchgrass (Panicum virgatum) is a promising perennial bioenergy crop due to its high yield and soil conservation attributes. However, efficient conversion of the complex cell wall into simple monomers for use in microbial conversion remains challenging. One strategy to overcome this is to engineer the cell wall biosynthetic pathways to reduce recalcitrance. Previously, greenhouse experiments demonstrated that switchgrass expressing the bacterial gene QsuB gained the ability to produce protocatechuic acid, a valuable industrial compound, while exhibiting reduced lignin and improved saccharification. When grown in randomized field trials, transgenic switchgrass lines lost the altered lignin phenotype, but displayed significantly higher yields over multiple cuts and growing seasons. To explore these observations, we took a systems biology approach. Transcriptomics, metabolomics, and cell wall chemistry were performed on clonally propagated material grown either in the greenhouse or field to identify potential metabolic changes that result in the field-specific phenotypes. Here we show that in addition to upregulation of the well-established phenylalanine derived pathway, we also see evidence for an increase in the recently discovered tyrosine pathway in grasses. These potential compensation mechanisms may be responsible for phenotype reversal upon exposure to the added stresses of the natural environment. We anticipate that these findings may provide targets for future engineering of the phenylpropanoid pathway. Consideration of alternate compensation pathways will be important for ensuring the maintenance of desired traits when moving transgenic crops out of the laboratory.