Phospholipase Dδ and phosphatidic acid mediate heat-induced nuclear localization of glyceraldehyde-3-phosphate dehydrogenase in Arabidopsis

Cytosolic glyceraldehyde-3-phosphate dehydrogenase (GAPC) is a glycolytic enzyme, but undergoes stress-induced nuclear translocation for moonlighting. We previously reported that in response to heat stress, GAPC accumulated in the nucleus to modulate transcription and thermotolerance. Here we show a cellular and molecular mechanism that mediates heat-induced nuclear translocation of cytosolic GAPC in Arabidopsis thaliana. Heat-induced GAPC nuclear accumulation and plant heat tolerance were reduced in Arabidopsis phospholipase D (PLD) knockout mutants of pld delta and pld alpha 1pld delta, but not of pld alpha 1. These changes were restored to wild type by genetic complementation with active PLD delta, but not with catalytically inactive PLD delta. GAPC overexpression enhanced the seedling thermotolerance and the expression of heat-inducible genes, but this effect was abolished in the pld delta background. Heat stress elevated the levels of the PLD product phosphatidic acid (PA) in the nucleus in wild type, but not in pld delta plants. Lipid labeling demonstrated the heat-induced nuclear co-localization of PA and GAPC, which was impaired by zinc, which inhibited the PA-GAPC interaction, and by the membrane trafficking inhibitor brefeldin A (BFA). The GAPC nuclear accumulation and seedling thermotolerance were also decreased by treatment with zinc or BFA. Our data suggest that PLD delta and PA are critical for the heat-induced nuclear translocation of GAPC. We propose that PLD delta-produced PA mediates the process via lipid-protein interaction and that the lipid mediation acts as a cellular conduit linking stress perturbations at cell membranes to nuclear functions in plants coping with heat stress.

Automated summary

This study reveals the cellular and molecular mechanism of heat-induced nuclear translocation of cytosolic GAPC in Arabidopsis thaliana. PLD delta and PA play critical roles in this process, mediated by lipid-protein interaction. These findings suggest a cellular conduit linking stress perturbations at cell membranes to nuclear functions in plants coping with heat stress.