Nuclear moonlighting of cytosolic glyceraldehyde-3-phosphate dehydrogenase regulates Arabidopsis response to heat stress

Sang-Chul Kim,Xuemin Wang,Liang Guo

doi:10.1038/s41467-020-17311-4

Abstract

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 of GAPC enhances heat tolerance of seedlings and the expression of heat-inducible genes whereas knockout of GAPCs has opposite effects. Screening of Arabidopsis transcription factors identifies nuclear factor Y subunit C10 (NF-YC10) as a GAPC-binding protein. The effects of GAPC overexpression are abolished when NF-YC10 is deficient, the heat-induced nuclear accumulation of GAPC is suppressed, or the GAPC-NF-YC10 interaction is disrupted. GAPC overexpression 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.

Highlights

Various stress conditions induce the nuclear translocation of cytosolic glyceraldehyde-3phosphate dehydrogenase (GAPC), but its nuclear function in plant stress responses remains elusive
The protein mixture was co-immunoprecipitated with GAPC2Flag that was purified from Arabidopsis overexpressing the recombinant protein or from control plants with empty vector (EV) using an anti-Flag antibody
Based on our data presented in this study, we propose that heat stress promotes translocation of a portion of the cytoplasmic GAPC pool into Arabidopsis nuclei, where GAPC is associated with the transcription factor nuclear factor Y subunit C10 (NF-YC10) to increase the expression of target heat-inducible genes and plant heat tolerance (Fig. 10)

Summary

Introduction

Various stress conditions induce the nuclear translocation of cytosolic glyceraldehyde-3phosphate dehydrogenase (GAPC), but its nuclear function in plant stress responses remains elusive. We show that GAPC interacts with a transcription factor to promote the expression of heat-inducible genes and heat tolerance in Arabidopsis. GAPC has been implicated in plant response to stresses, including cadmium, long-chain bases (dihydrosphingosine), reactive oxygen species, the lipid mediator phosphatidic acid (PA), and cold-induced sweetening and apical dominance of potato[6,7,8,9,10]. Even though some of the mechanisms required for stressinduced nuclear localization is determined, a clear role of nuclear GAPC remains elusive in plant stress responses. We show that GAPC interacts with the transcription factor nuclear factor Y subunit C10 (NF-YC10) and regulates transcriptional and physiological responses to heat stress

Methods

Results

Conclusion