Functions of serine from the phosphorylated pathway on growth, male gametogenesis, and metabolism in Marchantia polymorpha

Abstract

Serine is an important precursor of various biomolecules. Here, we investigated the role of the phosphorylated pathway of serine biosynthesis in a non-vascular plant Marchantia polymorpha by analyzing knockout mutants of MpPGDH, a single gene encoding the first committed enzyme 3-phosphoglycerate dehydrogenase (PGDH), to assess functions of this pathway in relation to those of the other two pathways. Growth phenotypes of the mutants indicated that serine supply from the phosphorylated pathway in the dark was crucial for vegetative growth. Sperm formation required serine from this pathway, while egg formation did not depend on it. Knockout of MpPGDH in the maternal genome disrupted sporophyte development. When the mutants were grown in high CO2 where the photorespiratory glycolate pathway for serine biosynthesis is inhibited, thallus growth was suppressed and not fully recovered to wild-type level by exogenous serine supplement, suggesting that serine homeostasis involving both the phosphorylated and glycolate pathways was essential. Metabolome and lipidome analyses indicated that the phosphorylated pathway mainly influenced the tricarboxylic acid cycle, the amino acid and nucleotide metabolism, and lack of serine significantly perturbed lipid metabolism. Our results indicate the importance of serine from the phosphorylated pathway for sperm formation, sporophyte development, and metabolism in M. polymorpha.