Perturbation of tonoplast sucrose transport alters carbohydrate utilization for seasonalgrowth and defense metabolism in coppiced poplar

Non-structural carbohydrate reserves of stems and roots underpin overall tree fitness. These reserves also contribute to productivity under short-rotation management practices such as coppicing for bioenergy. While sucrose and starch comprise the predominant carbohydrate reserves of Populus, utilization is understood primarily in terms of starch turnover. The tonoplast sucrose transport protein SUT4 modulates sucrose export from source leaves to distant sinks during photoautotrophic growth, but the possibility of its involvement in remobilizing carbohydrates from sinks during heterotrophic growth has not been explored. Here, we used PtaSUT4-knockout mutants of Populus tremula x P. alba (INRA 717-1B4) in winter (cool) and summer (warm) glasshouse coppicing experiments to strain carbon demand and test for SUT4 involvement in reserve utilization. We show that epicormic bud emergence, subsequent growth, and xylem hexose increases were delayed or reduced in sut4 mutants following lower temperature winter coppicing. Depletion of stem reserves during post-coppice regrowth was not impaired in sut4, but sut4 winter maintenance costs may have been higher in metabolic terms. Bark accrual of abundant defense metabolites, including salicinoids, chlorogenic acids, and flavonoid products, was prioritized in the summer, but attenuated in sut4 mutants. Summer sprout growth was not reduced in sut4 compared to controls. Together, our results point to shifting priorities for SUT4 modulation of seasonal trade-offs between growth and other priorities in the stem and emerging buds during reserve utilization in Populus.