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Various stress conditions induce the nuclear translocation of cytosolic glyceraldehyde-3-phosphate dehydrogenase (GAPC), but its nuclear function in plant stress responses remains elusive. Here we show that GAPC interacts with a transcription factor to promote the expression of heat-inducible genes and heat tolerance in Arabidopsis. GAPC accumulates in the nucleus under heat stress. Overexpression ofGAPCenhances heat tolerance of seedlings and the expression of heat-inducible genes whereas knockout ofGAPCshas opposite effects. Screening of Arabidopsis transcription factors identifies nuclear factor Y subunit C10 (NF-YC10) as a GAPC-binding protein. The effects ofGAPCoverexpression are abolished whenNF-YC10is deficient, the heat-induced nuclear accumulation of GAPC is suppressed, or the GAPC-NF-YC10 interaction is disrupted.GAPCoverexpression also enhances the binding ability of NF-YC10 to its target promoter. The results reveal a cellular and molecular mechanism for the nuclear moonlighting of a glycolytic enzyme in plant response to environmental changes.