Populus phenylpropanoid metabolism across biological scales

Abstract

Phenylpropanoid metabolism is a major contributor to plant biotic and abiotic stress responses while also influencing ecosystem-level processes such as nitrogen cycling. Populus in particular is characterized by its rich diversity of phenylpropanoids, varying both qualitatively and quantitatively within and across species. This dissertation develops a cross-scale view of Populus secondary metabolism to consider (1) the genetic basis of metabolic diversity within the genus, (2) influences of phenylpropanoid homeostasis on cellular metabolism, and (3) theoretical ecosystem-level effects of altered Populus phenylpropanoid levels. I first characterized the Populus BAHD acyltransferase family, due to its likely contributions to phenylpropanoid diversity in the taxon, using a phylogenomic approach. The one hundred putative full-length BAHD genes in Populus arose through genome-wide and local duplication events, and possibly through retrotransposition. Correlation of phylogenetic and gene expression data suggests that some recent duplicates have undergone functional divergence. To study the cellular-level effects of phenylpropanoid metabolism in Populus, I analyzed metabolite and gene expression profiles of cell cultures fed phenylpropanoid enzyme inhibitors and/or the elicitor methyl jasmonate. Results suggest that the effects of enzyme inhibitors manifest primarily at the metabolic level, in contrast to the transcriptionally-driven changes under methyl jasmonate elicitation. Links between core phenylpropanoid metabolism and phenylpropanoid derivatives, glycosylation, amino acid metabolism, and the Krebs cycle became evident under metabolic perturbation. To consider possible ecological effects of manipulating phenylpropanoid metabolism in Populus, I developed ecosystem models for probing indirect effects of Populus phenotypes exhibiting increased growth and reduced secondary metabolism. Such phenotypes would be consistent with metabolic engineering goals for trees to be used as biofuels. Initial simulations indicated shifts in biomass of ecosystem components not directly interacting with Populus and generated hypotheses for future field research. The results support the potential of ecological modeling as a research and decision-making tool prior to design and field release of novel tree genotypes. This research advances knowledge of Populus phenylpropanoid metabolism in a coordinated manner across biological scales and subdisciplines, that should be complementary to more traditional, single-discipline oriented research.