Epigenetic regulation of cell wall-associated WAK1 by HDC1 promotes iron remobilization under Fe-limited conditions.

Abstract

Iron (Fe) deficiency is a major abiotic stress limiting crop production. HDC1, a component of the histone deacetylase complex, plays important roles in plant development and stress responses, yet its function in Fe deficiency responses remains unclear. This study reveals that HDC1 promotes the reallocation and utilization of cell wall pectin-bound Fe under Fe-limited conditions through an ATAF1-dependent epigenetic pathway regulating the expression of the cell wall-associated receptor kinase WAK1. We found that Fe deficiency triggers HDC1 protein degradation via the ubiquitin-proteasome pathway, leading to increased acetylation of histone H3 at lysine 9 and 14 (H3K9ac/H3K14ac). RNA-seq and ChIP-qPCR analyses identified WAK1 as a key downstream gene negatively regulated by HDC1. Mechanistically, the transcription factor ATAF1 directly binds to and activates the WAK1 promoter, while HDC1 represses WAK1 transcription by indirectly promoting ATAF1 ubiquitination and degradation. Loss of WAK1 function results in increased pectin content, enhanced Fe sequestration in the cell wall, and heightened sensitivity to Fe deficiency. Conversely, the hdc1 mutant exhibits upregulated WAK1 expression, reduced pectin content, enhanced release of apoplastic Fe, and increased Fe translocation to shoots, collectively improving Fe deficiency tolerance. Together, our findings uncover an HDC1-ATAF1-WAK1 signaling module and elucidate an epigenetic mechanism wherein histone deacetylation regulates cell wall metabolism to promote Fe reutilization, providing new theoretical insights for improving plant Fe nutrition efficiency.