Stromal NADH supplied by PHOSPHOGLYCERATE DEHYDROGENASE3 is crucial for photosynthetic performance

Abstract

During photosynthesis, electrons travel from light-excited chlorophyll molecules along the electron transport chain to the final electron acceptor nicotinamide adenine dinucleotide phosphate (NADP) to form NADPH, which fuels the Calvin–Benson–Bassham cycle (CBBC). To allow photosynthetic reactions to occur flawlessly, a constant resupply of the acceptor NADP is mandatory. Several known stromal mechanisms aid in balancing the redox poise, but none of them utilizes the structurally highly similar coenzyme NAD(H). Using Arabidopsis (Arabidopsis thaliana) as a C3-model, we describe a pathway that employs the stromal enzyme PHOSPHOGLYCERATE DEHYDROGENASE 3 (PGDH3). We showed that PGDH3 exerts high NAD(H)-specificity and is active in photosynthesizing chloroplasts. PGDH3 withdrew its substrate 3-PGA directly from the CBBC. As a result, electrons diverted from NADPH via the CBBC into the separate NADH redox pool. pgdh3 loss-of-function mutants revealed an overreduced NADP(H) redox pool but a more oxidized plastid NAD(H) pool compared to wild-type plants. As a result, photosystem I acceptor side limitation increased in pgdh3. Furthermore, pgdh3 plants displayed delayed CBBC activation, changes in nonphotochemical quenching, and altered proton motive force partitioning. Our fluctuating light-stress phenotyping data showed progressing photosystem II damage in pgdh3 mutants, emphasizing the significance of PGDH3 for plant performance under natural light environments. In summary, this study reveals an NAD(H)-specific mechanism in the stroma that aid in balancing the chloroplast redox poise. Consequently, the stromal NAD(H) pool may provide a promising target to manipulate plant photosynthesis.

Metabolism and Regulatory Functions of O-Acetylserine, S-Adenosylmethionine, Homocysteine, and Serine in Plant Development and Environmental Responses

“…AtPGDH1 is the target of redox regulation of chloroplast proteins, and this regulation is associated with the redox-active Cys pair uniquely found in land plant PGDH (Yoshida et al, 2020). Recently, Höhner et al (2021) reported that AtPGDH3 plays a crucial role in NADH supply in plastid stroma and eventually in photosynthetic performance under natural fluctuating light environment.…”

The Complementary Roles of Chloroplast Cyclic Electron Transport and Mitochondrial Alternative Oxidase to Ensure Photosynthetic Performance

“…Finally, plastid terminal oxidase couples PQ oxidation with the reduction of oxygen to water ( Nawrocki et al, 2015 ). Another recently described pathway uses the stromal enzyme phosphoglycerate dehydrogenase to indirectly transfer electrons from the NADPH to NADH pool ( Höhner et al, 2021 ).…”

Indirect Export of Reducing Equivalents From the Chloroplast to Resupply NADP for C3 Photosynthesis—Growing Importance for Stromal NAD(H)?

“…However, if this were correct it seems hard to comprehend why C 3 plant species possess NAD-dependent MDHs with confirmed enzyme activity in light and dark-incubated chloroplasts (Backhausen et al, 1998 ). Indeed, evidence suggesting a significant function for NAD(H) in illuminated chloroplasts has been growing over the last years (Zhao et al, 2018 ; Höhner et al, 2021 ).…”

“…Homozygous pgdh1 loss of function mutants are not viable (Benstein et al, 2013 ). Interestingly, PGDH1 and PGDH3 loci differ greatly in their co-expression patterns: PGDH1 clusters with PGDH2 and other components of amino acid metabolism; PGDH3 is co-expressed with subunits of the thylakoid NDH complex suggesting a potential link to PSI and photosynthesis (Casatejada-Anchel et al, 2021 ; Höhner et al, 2021 ).…”