Nitrogen inputs influence vegetative metabolism in maize engineered with a seed-specific carotenoid pathway.

KEY MESSAGE: Metabolomic profiling of a maize line engineered with an endosperm-specific carotenogenic pathway revealed unexpected metabolic readjustments of primary metabolism in leaves and roots. High-carotenoid (HC) maize was engineered to accumulate high levels of carotenoids in the endosperm. The metabolic interventions influenced the flux through non-target pathways in tissues that were not affected by the targeted intervention. HC maize at the vegetative stage also showed a reduced susceptibility to insect feeding. It is unknown, however, whether the metabolic history of the embryo has any impact on the metabolite composition in vegetative tissues. We, therefore, compared HC maize and its isogenic counterpart (M37W) to test the hypothesis that boosting the carotenoid content in the endosperm triggers compensatory effects in core metabolism in vegetative tissues. Specifically, we investigated whether the metabolite composition of leaves and roots at the V6 stage differs between HC and M37W, and whether N inputs further alter the core metabolism of HC compared to M37W. We found an increase in the abundance of organic acids from the tricarboxylic acid (TCA) cycle in HC even under restricted N conditions. In contrast, low levels of carotenoids and chlorophyll were measured regardless of N levels. Sugars were also significantly depleted in HC under low N. We propose a model explaining the observed genotype-dependent and input-dependent effects, in which organic acids derived from the TCA cycle accumulate during vegetative growth and contribute to the increased demand for pyruvate and/or acetyl-CoA in the endosperm and embryo. This response may in part reflect the transgenerational priming of vegetative tissues in the embryo induced by the increased demand for metabolic precursors during seed development in the previous generation.