HDA6-mediated histone deacetylation restricts premature tapetal PCD to maintain male fertility during early flowering in Arabidopsis

Abstract

Histone deacetylation regulates plant development, yet its role in male gametophyte development and fertility remains unclear. Here, we show that histone deacetylase 6 (HDA6), an RPD3-like histone deacetylase, epigenetically regulates timely tapetal programmed cell death (PCD) and male fertility, predominantly during early flowering in Arabidopsis. Loss of HDA6 in axe1-4 causes early-stage male sterility followed by fertility recovery, accompanied by premature tapetal PCD, impaired pollen development and defective pollen wall formation. HDA6 interacts with squamosa promoter binding protein-like 8 (SPL8) to repress Arabidopsis NAC domain containing protein 087 (ANAC087) through H3K9/K14 deacetylation. In axe1-4, ANAC087 derepression activates cysteine endopeptidase 1 (CEP1), triggering precocious tapetal PCD. Genetic suppression of ANAC087 or CEP1 restores male fertility. Thus, HDA6-SPL8 establishes a stage-dependent epigenetic checkpoint that restrains the ANAC087-CEP1 cell death pathway and ensures timely tapetal PCD. Our study reveals how chromatin regulation integrates with developmental timing to safeguard plant male fertility.