The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth

Abstract

SUMMARYThe Arabidopsis phosphate transporter PHT4;1 was previously localized to the chloroplast thylakoid membrane. Here we investigated the physiological consequences of the absence of PHT4;1 for photosynthesis and plant growth. In standard growth conditions, two independent Arabidopsis knockout mutant lines displayed significantly reduced leaf size and biomass but normal phosphorus content. When mutants were grown in high-phosphate conditions, the leaf phosphorus levels increased and the growth phenotype was suppressed. Photosynthetic measurements indicated that in the absence of PHT4;1 stromal phosphate was reduced to levels that limited ATP synthase activity. This resulted in reduced CO 2 fixation and accumulation of soluble sugars, limiting plant growth. The mutants also displayed faster induction of non-photochemical quenching than the wild type, in line with the increased contribution of DpH to the proton-motive force across thylakoids. Small-angle neutron scattering showed a smaller lamellar repeat distance, whereas circular dichroism spectroscopy indicated a perturbed long-range order of photosystem II (PSII) complexes in the mutant thylakoids. The absence of PHT4;1 did not alter the PSII repair cycle, as indicated by wild-type levels of phosphorylation of PSII proteins, inactivation and D1 protein degradation. Interestingly, the expression of genes for several thylakoid proteins was downregulated in the mutants, but the relative levels of the corresponding proteins were either not affected or could not be discerned. Based on these data, we propose that PHT4;1 plays an important role in chloroplast phosphate compartmentation and ATP synthesis, which affect plant growth. It also maintains the ionic environment of thylakoids, which affects the macro-organization of complexes and induction of photoprotective mechanisms.

An update on the regulation of photosynthesis by thylakoid ion channels and transporters in Arabidopsis

“…The envelope‐located PHT4;1 could also regulate the ATP synthase before the activation of other envelope Pi transporters. The pht4;1 mutants displayed wild‐type levels of ETR and faster induction of NPQ, but did not differ in the steady state from the wild‐type (Karlsson et al ).…”

“…The taac thylakoid structure was not distinguishable from the wild‐type in plants exposed to standard growth light, but higher grana stacks were observed in high light conditions due to impaired PSII cycle (Yin et al ). The pht4;1 thylakoid organization did not appear affected in the transmission electron microscopy analyses, however, small‐angle neutron scattering revealed smaller lamellar repeat distance of thylakoids, attributed to a tighter stacking and/or narrower lumen in the likely altered ionic environment (Karlsson et al ). The pam71 mutants did not differ from the wild‐type in organization of chloroplast and thylakoid membranes (Schneider et al ).…”

Retracted: Each of the chloroplast potassium efflux antiporters affects photosynthesis and growth of fully developed Arabidopsis rosettes under short‐day photoperiod

“…Our previous studies of Arabidopsis chloroplast kea mutants were carried out on young developing rosettes of plants grown under long‐day conditions, and did not reveal detrimental phenotypes in kea1 , kea2 and kea3 single mutants (Kunz et al ). Arabidopsis mutants for several other chloroplast transporters grown under short‐day photoperiod (8 h light per day) were shown to display a phenotype only after plants were fully developed (Yin et al , Irigoyen et al , Karlsson et al ). Therefore, in this study, we aimed to investigate whether chloroplast KEAs play redundant roles in chloroplast function also in older plants with fully developed rosettes grown under short‐day photoperiod.…”

The Impacts of Phosphorus Deficiency on the Photosynthetic Electron Transport Chain

“…The high-affinity P i transporter PHT4;1 75 (K M < 400 µM) has been localized in the stroma-exposed regions of the thylakoid membrane, and 76 mediates P i transport from the thylakoid lumen to the stroma 77 Yin et al, 2015). A study of Arabidopsis knockout mutants showed that the absence of PHT4;1 78 resulted in a marked decrease in ATP synthase activity; it was assumed that PHT4;1 operates in 79 close proximity to ATP synthase in the thylakoid membrane to maintain sufficient P i levels for ATP 80 synthesis (Karlsson et al, 2015). It was proposed that an altered supply of P i in the stroma reduced 81 the ATP levels and thereby reduced CO 2 assimilation, but no changes in the photosynthetic 82 machinery composition or electron transport activity were observed (Karlsson et al, 2015).…”

“…Three P i transporter families are localized in the 331 chloroplast to supply P i in the stroma, where PHT4;1 is the only transporter localized in the 332 thylakoid membrane. Furthermore, a limitation in ATP synthase and reduced growth has only been 333 demonstrated for PHT4;1 mutants (Karlsson et al, 2015). PHT4;1 mediates the availability of P i for 334 ATP synthesis in the chloroplast stroma (Karlsson et al, 2015), and it is likely that the P i 335 concentration in chloroplasts is regulated by effective phosphate homeostasis to maintain ATP 336 synthesis and drive the Calvin cycle .…”