Commonalities and specialties in photosynthetic functions of PROTON GRADIENT REGULATION5 variants in Arabidopsis

Penzler, Jan-Ferdinand; Marino, Giada; Reiter, Bennet; Kleine, Tatjana; Naranjo, Belén; Leister, Dario

doi:10.1093/plphys/kiac362

Cited by 14 publications

(15 citation statements)

References 53 publications

(104 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The Arabidopsis pgr5 mutant has recently been shown to have point mutations in two separate genes encoding the PGR5 and PPT1 proteins, the latter of which seems to perpetuate long-term damage to PSI (Wada et al, 2021). Importantly for the conclusions of this work, however, the low pmf and Y(ND) phenotypes were shown to be associated with the PGR5 mutation alone, consistent with tDNA knock-out results in rice and a recent CRISPR-Cas9 pgr5 mutant generated in Arabidopsis (Nishikawa et al, 2012;Penzler et al, 2022). Pmf and vH + in the hope2 pgr5 double mutant dropped significantly below hope2, except under very low light (Figure 4a,c), whereas gH + was similar in hope2 and hope2 pgr5 (Figure 4b).…”

Section: Pgr5 Is the Major Cet Pathway In Hope2supporting

confidence: 81%

High cyclic electron transfer via the PGR5 pathway in the absence of photosynthetic control

et al. 2023

View full text Add to dashboard Cite

The light reactions of photosynthesis couple electron and proton transfers across the thylakoid membrane, generating NADPH, and proton motive force (pmf) that powers the endergonic synthesis of ATP by ATP synthase. ATP and NADPH are required for CO2 fixation into carbohydrates by the Calvin-Benson-Bassham cycle (CBBC). The dominant ΔpH component of the pmf also plays a photoprotective role in regulating photosystem II (PSII) light harvesting efficiency through non-photochemical quenching (NPQ) and photosynthetic control via electron transfer from cytochrome b6f (cytb6f) to photosystem I (PSI). ΔpH can be adjusted by increasing the proton influx into the thylakoid lumen via upregulation of cyclic electron transfer (CET) or decreasing proton efflux via downregulation of ATP synthase conductivity (gH+). The interplay and relative contributions of these two elements of ΔpH control to photoprotection are not well understood. Here, we showed that an Arabidopsis (Arabidopsis thaliana) ATP synthase mutant hunger for oxygen in photosynthetic transfer reaction 2 (hope2) with 40% higher proton efflux has supercharged CET. Double crosses of hope2 with the CET-deficient proton gradient regulation 5 and ndh-like photosynthetic complex I (ndho) lines revealed that PGR5-dependent CET is the major pathway contributing to higher proton influx. PGR5-dependent CET allowed hope2 to maintain wild-type levels of ΔpH, CO2 fixation and NPQ, however photosynthetic control remained absent and PSI was prone to photoinhibition. Therefore, high CET in the absence of ATP synthase regulation is insufficient for PSI photoprotection.

show abstract

Section: Pgr5 Is the Major Cet Pathway In Hope2supporting

confidence: 81%

High cyclic electron transfer via the PGR5 pathway in the absence of photosynthetic control

et al. 2023

View full text Add to dashboard Cite

show abstract

Section: Pgr5 Is the Major Cet Pathway In Hope2supporting

confidence: 84%

Supercharged PGR5-dependent cyclic electron transfer compensates for mis-regulated chloroplast ATP synthase

Degen

Jackson

Proctor

et al. 2022

Preprint

View full text Add to dashboard Cite

The light reactions of photosynthesis couple electron and proton transfers across the thylakoid membrane, generating NADPH, and proton motive force (pmf) that powers the endergonic synthesis of ATP by ATP synthase. ATP and NADPH are required for CO2 fixation into carbohydrates by the Calvin-Benson-Bassham cycle (CBBC). The dominant ΔpH component of the pmf also plays a photoprotective role in regulating photosystem II (PSII) light harvesting efficiency, through non-photochemical quenching (NPQ), and cytochrome b6f (cytb6f) to photosystem I (PSI) electron transfer, via photosynthetic control. ΔpH can be adjusted by increasing the proton influx into the thylakoid lumen via upregulation of cyclic electron transfer (CET) or decreasing proton efflux via downregulation of ATP synthase conductivity (gH+). The interplay and relative contributions of these two elements of ΔpH control to photoprotection are not well understood. Here, we show that an Arabidopsis ATP synthase mutant (hope2) with 40% higher proton efflux, has supercharged CET. Double crosses of hope2 with the CET-deficient pgr5 and ndho lines reveal that PGR5-dependent CET is the major pathway contributing to higher proton influx. PGR5-dependent CET allows hope2 to maintain wild-type levels of ΔpH, CO2 fixation and NPQ, however photosynthetic control remains absent, and PSI is acceptor-side limited. Therefore, high CET in the absence of ATP synthase regulation is insufficient for PSI photoprotection.

show abstract

“…Since the original pgr5 mutant was generated by EMS mutagenesis, we also checked for the presence of oscillations in the pgr5 -CAS mutant (Penzler et al, 2022), which does not contain any other background mutations (Fig. 8).…”

Section: Resultsmentioning

confidence: 99%

PGR5 is required to avoid photosynthetic oscillations during light transitions

Degen,

Pastorelli,

Johnson

2023

Preprint

View full text Add to dashboard Cite

The production of ATP and NADPH by the light reactions of photosynthesis and their consumption by the Calvin-Benson-Bassham (CBB) cycle and other downstream metabolic reactions requires careful regulation. Environmental shifts perturb this careful balance, leading to photo-oxidative stress and losses in CO2 assimilation. Imbalances in the production and consumption of ATP and NADPH manifest themselves as transient instability in the chlorophyll fluorescence, P700, electrochromic shift and CO2 uptake signals recorded on leaves. These oscillations can be induced in wild-type plants by sudden shifts in CO2 concentration or light intensity, however mutants exhibiting increased oscillatory behaviour have yet to be reported. This has precluded an understanding of the regulatory mechanisms employed by plants to suppress oscillations. Here we show that the Arabidopsis pgr5 mutant, which is deficient in PGR5-dependent cyclic electron transfer (CET), exhibits increased oscillatory behaviour. In contrast, mutants lacking the NDH-dependent CET are largely unaffected. The absence of oscillations in the hope2 mutant, which like pgr5, lacks photosynthetic control and exhibits high ATP synthase conductivity, ruled out loss of these photoprotective mechanisms as causes. Instead, we observed slower formation of proton motive force and by inference ATP synthesis in pgr5 following environmental perturbation, leading to the transient reduction of the electron transfer chain and photosynthetic oscillations. PGR5-dependent CET therefore plays a major role in damping the effect of environmental perturbations on photosynthesis to avoid losses in CO2 fixation.

show abstract

Commonalities and specialties in photosynthetic functions of PROTON GRADIENT REGULATION5 variants in Arabidopsis

Cited by 14 publications

References 53 publications

High cyclic electron transfer via the PGR5 pathway in the absence of photosynthetic control

High cyclic electron transfer via the PGR5 pathway in the absence of photosynthetic control

Supercharged PGR5-dependent cyclic electron transfer compensates for mis-regulated chloroplast ATP synthase

PGR5 is required to avoid photosynthetic oscillations during light transitions

Contact Info

Product

Resources

About