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Lack of TROL protein and FNR release from thylakoid membranes influences cellular redox poise and renders plants energy depleted

We have recently identified a long sought thylakoid membrane protein responsible for tethering of ferredoxin:NADP+ oxidoreductase (FNR), the enzyme responsible for the final reaction of NADPH synthesis in oxygenic photosynthesis (S. Jurić, et al., Plant J. 60 (2009) 783-794). Thylakoid rhodanase-like protein (TROL) interacts with FNR via the C-terminal ITEP domain similar to repeats found in Tic62 protein family. Yeast-two-hybrid analysis indicates very strong ITEP-FNR interaction which exceeds Tic62-FNR interaction by more than 8 fold. TROL is an integral membrane protein which has a dual localization ; it can be found in a precursor form at the inner envelope and as processed protein at the non-appressed regions of thylakoids. TROL, via rhodanase-like domain, might interact with energy carriers within the thylakoid membrane (plastoquinone). Using gene inactivation approach in the model plant Arabidopsis, we have shown that the binding of FNR to TROL is necessary for sustaining high rates of photosynthetic electron flow and the induction of non-photochemical quenching (NPQ). Chlorophyll a quenching measured after high-light exposure drops significantly below F0. Depletion of TROL does not influence cyclic electron flow mediated by the NDH complex. TROL exists in several multiprotein complexes containing proteins of photosystem II (PSII) and cytochrome b6/f. Depletion of TROL causes alterations in nuclear gene expression (retrograde-signaling) which leads to changes in chloroplast biogenesis ; chloroplast stay smaller in size and contain less stacked thylakoids. TROL deficient plants suffer a severe deficiency in leaf pyridine nucleotide pool which indicates that interaction of FNR with thylakoid membranes exerts a more general impact on cellular energetics. Furthermore, lack of this interaction leads to changes in the redox poise of the entire cell, the NADP(H) pool is shifted towards more reduced state. We propose that TROL is not only an important checkpoint for redox regulation of photosynthetic energy distribution, but also represents a link between photosynthesis and other cellular processes mediated by pyridine nucleotides.

linear electron flow; non-photochemical quenching; metabolic retrograde signaling; NADP(H) pool; redox regulation

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