The partitioning of carbon for growth, storage and constitutive chemical defenses is widely framed in terms of a hypothetical sink-source differential that varies with nutrient supply. According to this framework, phenolics accrual is passive and occurs in source leaves when normal sink growth is not sustainable due to a nutrient limitation. In assessing this framework, we present gene and metabolite evidence that condensed tannin (CT) accrual is strongest in sink leaves and sequesters carbon in a way that impinges upon foliar sink strength and upon phenolic glycoside (PG) accrual in Populus. The work was based on two Populus fremontii × angustifolia backcross lines with contrasting rates of CT accrual and growth, and equally large foliar PG reserves. However, foliar PG accrual was developmentally delayed in the high-CT, slow-growth line (SG), and nitrogen-limitation led to increased foliar PG accrual only in the low-CT, fast-growth line (FG). Metabolite profiling of developing leaves indicated comparatively carbon-limited amino acid metabolism, depletion of several Krebs cycle intermediates and reduced organ sink strength in SG. Gene profiling indicated that CT synthesis decreased as leaves expanded and PGs increased. A most striking finding was that the nitrogenous monoamine phenylethylamine accumulated only in leaves of SG plants. The potential negative impact of CT hyper-accumulation on foliar sink strength, as well as a mechanism for phenylethylamine involvement in CT polymerization in Populus are discussed. Starch accrual in source leaves and CT accrual in sink leaves of SG may both contribute to the maintenance of a slow-growth phenotype suited to survival in nutrient-poor habitats.
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