Transcriptional Regulation of the Glucose-6-Phosphate/Phosphate Translocator 2 Is Related to Carbon Exchange Across the Chloroplast Envelope

Abstract

The exchange of reduced carbon across the inner chloroplast envelope has a large impact on photosynthesis and growth. Under steady-state conditions it is thought that glucose 6-phosphate (G6P) does not cross the chloroplast membrane. However, growth at high CO 2 , or disruption of starch metabolism can result in the GPT2 gene for a G6P/P i translocator to be expressed presumably allowing G6P exchange across the chloroplast envelope. We found that after an increase in light, the transcript for GPT2 transiently increases several 100-fold within 2 h in both the Col-0 and WS ecotypes of Arabidopsis thaliana . The increase in transcript for GPT2 is preceded by an increase in transcript for many transcription factors including Redox Responsive Transcription Factor 1 (RRTF1). The increase in GPT2 transcript after exposure to high light is suppressed in a mutant lacking the RRTF1 transcription factor. The GPT2 response was also suppressed in a mutant with a T-DNA insert in the gene for the triose-phosphate/P i translocator (TPT). However, plants lacking TPT still had a robust rise in RRTF1 transcript in response to high light. From this, we conclude that both RRTF1 (and possibly other transcription factors) and high amounts of cytosolic triose phosphate are required for induction of the expression of GPT2 . We hypothesize that transient GPT2 expression and subsequent translation is adaptive, allowing G6P to move into the chloroplast from the cytosol. The imported G6P can be used for starch synthesis or may flow directly into the Calvin-Benson cycle via an alternative pathway (the G6P shunt), which could be important for regulating and stabilizing photosynthetic electron transport and carbon metabolism.

Photosynthetic Acclimation to Fluctuating Irradiance in Plants

“…The ability to undergo dynamic acclimation in Arabidopsis has been linked to the glucose-6-phosphate/phosphate translocator across the chloroplast envelope (Athanasiou et al, 2010;Dyson et al, 2015;Miller et al, 2017) and loss-of-function mutants in this gene had significantly lower fitness when grown under fluctuating irradiance (Athanasiou et al, 2010). The increase in activity of this transporter in response to an increase in irradiance could result in the import of glucose-6-phosphate into the chloroplast, which would stabilize photosynthetic metabolism during acclimation (Weise et al, 2019) but it is still unclear why its expression is required for dynamic acclimation to occur.…”

Source of 12C in Calvin–Benson cycle intermediates and isoprene emitted from plant leaves fed with 13CO2

“…The free hexoses can then reenter the active carbon pool by hexokinase and fructokinase ( Figure 1). Since the leaf glucose-6-phosphate transporter (GPT2) is normally not expressed in photosynthetic tissue [53,54] it is necessary that the hexose phosphates be converted to pentose phosphates for entry into chloroplasts on the xylulose phosphate transporter (XPT) [55,56]. It is assumed that the flux through sucrose, glucose, and fructose is small relative to their pool sizes.…”

“…The cytosolic shunt can return unlabeled carbon to the CBC as a result of hexokinase action on glucose and fructokinase action on fructose [73]. Hexose phosphates generally are not transported across chloroplast membranes of photosynthesizing leaves [53,54], but after conversion to ribulose 5-phosphate and isomerization to xylulose 5-phosphate this carbon can reenter the chloroplast and CBC on the XPT, which can transport both xylulose and ribulose 5-phosphate [55,56]. The activity of cytosolic hexokinase may cause sugar signaling that could adjust photosynthetic activity and co-ordinate photosynthesis with other physiological processes in plants [74].…”

A Failure Mode and Effect Analysis of plant metabolism reveals why cytosolic fumarase is required for temperature acclimation in Arabidopsis

“…While we have focused here on malate as a high-risk metabolite, our analysis has identified other high-risk candidates. Interestingly, some of them have previously been noted as critical components of acclimation (Timm et al, 2012;Dyson et al, 2015;Weise et al, 2019). For example, it was shown that expression of GTP2, a chloroplast glucose 6phosphate/phosphate translocator, is required for acclimation to high light in the Arabidopsis accession Wassilewskija-4 (Dyson et al, 2015).…”