BASIC PENTACYSTEINE1 regulates ABI4 by modification of two histone marks H3K27me3 and H3ac during early seed development of Medicago truncatula

Front Plant Sci. 2024 Jun 10:15:1395379. doi: 10.3389/fpls.2024.1395379. eCollection 2024.

Abstract

Introduction: The production of highly vigorous seeds with high longevity is an important lever to increase crop production efficiency, but its acquisition during seed maturation is strongly influenced by the growth environment.

Methods: An association rule learning approach discovered MtABI4, a known longevity regulator, as a gene with transcript levels associated with the environmentally-induced change in longevity. To understand the environmental sensitivity of MtABI4 transcription, Yeast One-Hybrid identified a class I BASIC PENTACYSTEINE (MtBPC1) transcription factor as a putative upstream regulator. Its role in the regulation of MtABI4 was further characterized.

Results and discussion: Overexpression of MtBPC1 led to a modulation of MtABI4 transcripts and its downstream targets. We show that MtBPC1 represses MtABI4 transcription at the early stage of seed development through binding in the CT-rich motif in its promoter region. To achieve this, MtBPC1 interacts with SWINGER, a sub-unit of the PRC2 complex, and Sin3-associated peptide 18, a sub-unit of the Sin3-like deacetylation complex. Consistent with this, developmental and heat stress-induced changes in MtABI4 transcript levels correlated with H3K27me3 and H3ac enrichment in the MtABI4 promoter. Our finding reveals the importance of the combination of histone methylation and histone de-acetylation to silence MtABI4 at the early stage of seed development and during heat stress.

Keywords: ABI4; BPC1; H3Ac; H3K27me3; longevity; seed development.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was conducted in the framework of the regional program ‘Objectif Végétal, Research, Education and Innovation in Pays de la Loire’, supported by the French Region Pays de la Loire, Angers Loire Métropole and the European Regional Development Fund. The bpc1 Tnt1 mutants of Medicago truncatula used in this research project, which is jointly owned by the Centre National de la Recherche Scientifique, were obtained from the Samuel Roberts Noble Foundation, Inc. and were created through research funded, in part, by a grant from the National Science Foundation (NSF# 703285).