Endoplasmic reticulum adenylate transporter activity affects amino acid metabolism under photorespiratory conditions

The involvement of the endoplasmic reticulum (ER)-localized adenylate transporter1 (ER-ANT1) in photorespiratory metabolism has been established, yet its precise physiological function remains uncertain. Rice er-ant1 mutant plants grown in ambient air exhibited stunted growth and substantial alterations in amino acid metabolites, but recovery in a high CO 2 condition (1.5%). We show that the absence of ER-ANT1 hindered the breakdown of glycine without affecting its synthesis, leading to a substantial accumulation of glycine, diminished levels of serine, and depleted reserves of glutamate and alanine. Intriguingly, the er-ant1 plants grown in high CO 2 and later exposed to ambient air displayed reduced serine levels within 12 h, yet they accumulated serine a week after transferring to ambient air due to induced phosphorylated serine synthesis pathways. Furthermore, knockout of ER-ANT1 marginally impacted the transcription of genes governing core enzymes in photorespiration, but notably upregulated BOU expression that encodes a putative mitochondrial glutamate transporter and AGAT1 that encodes an alanine:glyoxylate aminotransferase gene. Surprisingly, AGAT1, an ER-localized protein, exhibited higher activity that correlates with the decreased alanine levels observed in the er-ant1 mutant. Lack of ER-ANT1 activity also led to a significantly elevated NADH/NAD + ratio that potentially hinders the glycine-to-serine conversion process. This supports the hypothesis that the lack of ER-ANT1 -induced limitation of ATP usage might inhibit GDC activity by modulating the NADH/NAD + ratio. Moreover, non-proteinogenic amino acids, including β-alanine and γ-aminobutyrate (GABA), underwent significant alterations, even under high CO 2 conditions in the er-ant mutant, implying additional non-photorespiration roles of ER-ANT1. Taken together, our results indicate that ER-localized ER-ANT1 plays a crucial role in amino acid metabolism during photorespiration.