Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis

Abstract

Somatic embryogenesis (SE), which is a process that involves the in vitro-induced embryogenic reprogramming of plant somatic cells, requires dynamic changes in the cell transcriptome. These changes are fine-tuned by many genetic and epigenetic factors, including posttranslational histone modifications such as histone acetylation. Antagonistically acting enzymes, histone acetyltransferases (HATs) and deacetylases (HDACs), which control histone acetylation in many developmental processes, are believed to control SE. However, the function of specific HAT/HDACs and the genes that are subjected to histone acetylation-mediated regulation during SE have yet to be revealed. Here, we present the global and gene-specific changes in histone acetylation in Arabidopsis explants that are undergoing SE. In the TSA (trichostatin A)-induced SE, we demonstrate that H3 and H4 acetylation might control the expression of the critical transcription factor (TF) genes of a vital role in SE, including LEC1, LEC2 (LEAFY COTYLEDON 1; 2), FUS3 (FUSCA 3) and MYB118 (MYB DOMAIN PROTEIN 118). Within the HATs and HDACs, which mainly positively regulate SE, we identified HDA19 as negatively affecting SE by regulating LEC1, LEC2 and BBM. Finally, we provide some evidence on the role of HDA19 in the histone acetylation-mediated regulation of LEC2 during SE. Our results reveal an essential function of histone acetylation in the epigenetic mechanisms that control the TF genes that play critical roles in the embryogenic reprogramming of plant somatic cells. The results implicate the complexity of Hac-related gene regulation in embryogenic induction and point to differences in the regulatory mechanisms that are involved in auxin- and TSA-induced SE.

The improvement of the in vitro plant regeneration in barley with the epigenetic modifier of histone acetylation, trichostatin A

“…That implies the substantial role of histone acetylation and the TSA-sensitive HDACs in the genetic mechanism regulating plant regeneration. In support, the involvement of HDA6 and HDA19 in the repression of LEC1 , FUS3 , and BBM was reported (Tanaka et al 2008 ; Jia et al 2014 ; Morończyk et al 2022 ). Thus, we assumed that the upregulation of TFs in barley cultures resulted from TSA-induced inhibition of the enzymatic activity of HDACs (Wójcikowska et al 2018 ).…”

Histone acetylation functions in the wound-induced spore formation in nori

“…Several transcription factor genes have been identified to be targets of histone acetylation in response to abiotic and biotic stresses in plants. In somatic embryogenesis of Arabidopsis explants, histone H3 and H4 acetylation control the expression of some critical transcription factor genes, including LEC1 , LEC2 ( LEAFY COTYLEDON 1, 2 ), FUS3 ( FUSCA 3 ) and MYB118 ( MYB DOMAIN PROTEIN 118 ) ( Morończyk et al., 2022 ). All of these TF genes are confirmed to be of vital roles in somatic embryogenesis.…”

Recent advances in understanding of the epigenetic regulation of plant regeneration

“…Specifically, HDA19 inhibits somatic embryogenesis by negatively regulating LEC1 , LEC2 , and BBM expression by reducing their acetylation levels (Fig. 1 B) (Morończyk et al 2022 ). However, when leaves were used as the explant, TSA inhibited callus formation (Lee et al 2016 ).…”