Elevated atmospheric CO2-induced reprogramming leads to decreased seed protein and nutritional quality in forest trees.

While the global increases in atmospheric CO2 levels have had a beneficial effect on plant growth, the negative impacts of this CO2 fertilization effect on seed quality are often overlooked. Using data from acorns produced by mature oak (Quercus robur) trees in the eighth year of eCO2, we present evidence of negative consequences for seed quality. The acorns produced by the near-200-yr-old oak trees under eCO2 at the free air carbon dioxide enrichment facility at the Birmingham Institute for Forest Research (BIFoR) had higher phytate levels but decreased protein content. Quantitative label-free proteomics identified 335 proteins in all acorns, but 9 proteins were undetectable in acorns produced under eCO2 compared to ambient air (aCO2), and 1 protein was uniquely detected in the eCO2 acorns. Further subsets of proteins were identified with either higher or lower abundance in eCO2 than aCO2 acorns. Proteins that were more abundant in the acorns produced under eCO2 include allene oxide cyclase and phosphomannomutase. RNA-seq analysis revealed that 154 transcripts were more abundant in the eCO2 acorns compared to those grown under aCO2, while 54 were much less abundant. Transcripts encoding several transcription factors and phytohormone signaling proteins, as well as trehalose 6-phosphate phosphatase, were increased in eCO2 acorns. Taken together, these findings demonstrate that the transcriptome and proteome profiles of acorns produced under eCO2 are significantly changed compared to those produced in aCO2, with important implications for seed metabolism, particularly those underpinning the observed changes in seed protein and phytate levels.