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.