Plastid terminal oxidase (PTOX) protects photosystem I and not photosystem II against photoinhibition in Arabidopsis thaliana and Marchantia polymorpha.

The plastid terminal oxidase PTOX controls the oxidation level of the plastoquinone pool in the thylakoid membrane and acts as a safety valve upon abiotic stress, but detailed characterization of its role in protecting the photosynthetic apparatus is limited. Here we used PTOX mutants in two model plants Arabidopsis thaliana and Marchantia polymorpha. In Arabidopsis, lack of PTOX leads to a severe defect in pigmentation, a so-called variegated phenotype, when plants are grown at standard light intensities. We created a green Arabidopsis PTOX mutant expressing the bacterial carotenoid desaturase CRTI and a double mutant in Marchantia lacking both PTOX isoforms, the plant-type and the alga-type PTOX. In both species, lack of PTOX affected the redox state of the plastoquinone pool. Exposure of plants to high light intensity showed in the absence of PTOX higher susceptibility of photosystem I to light-induced damage while photosystem II was more stable compared with the wild type demonstrating that PTOX plays both, a pro-oxidant and an anti-oxidant role in vivo. Our results shed new light on the function of PTOX in the protection of photosystem I and II.

Manganese concentration affects chloroplast structure and the photosynthetic apparatus in Marchantia polymorpha.

Manganese (Mn) is an essential metal for plant growth. The most important Mn-containing enzyme is the Mn4CaO5 cluster that catalyzes water oxidation in photosystem II (PSII). Mn deficiency primarily affects photosynthesis, whereas Mn excess is generally toxic. Here, we studied Mn excess and deficiency in the liverwort Marchantia polymorpha, an emerging model ideally suited for analysis of metal stress since it accumulates rapidly toxic substances due to the absence of well-developed vascular and radicular systems and a reduced cuticle. We established growth conditions for Mn excess and deficiency and analyzed the metal content in thalli and isolated chloroplasts. In vivo super-resolution fluorescence microscopy and transmission electron microscopy revealed changes in the organization of the thylakoid membrane under Mn excess and deficiency. Both Mn excess and Mn deficiency increased the stacking of the thylakoid membrane. We investigated photosynthetic performance by measuring chlorophyll fluorescence at room temperature and 77 K, measuring P700 absorbance, and studying the susceptibility of thalli to photoinhibition. Nonoptimal Mn concentrations changed the ratio of PSI to PSII. Upon Mn deficiency, higher non-photochemical quenching was observed, electron donation to PSI was favored, and PSII was less susceptible to photoinhibition. Mn deficiency seemed to favor cyclic electron flow around PSI, thereby protecting PSII in high light. The results presented here suggest an important role of Mn in the organization of the thylakoid membrane and photosynthetic electron transport.