Trithorax Group Proteins Act Together with a Polycomb Group Protein to Maintain Chromatin Integrity for Epigenetic Silencing during Seed Germination in Arabidopsis

Abstract

Polycomb group (PcG) and trithorax group (trxG) proteins have been shown to act antagonistically to epigenetically regulate gene expression in eukaryotes. The trxG proteins counteract PcG-mediated floral repression in Arabidopsis, but their roles in other developmental processes are poorly understood. We investigated the interactions between the trxG genes, ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) and ULTRAPETALA1 (ULT1), and the PcG gene EMBRYONIC FLOWER 1 (EMF1) during early development. Unexpectedly, we found that mutations in the trxG genes failed to rescue the early-flowering phenotype of emf1 mutants. Instead, emf1 atx1 ult1 seedlings showed a novel swollen root phenotype and massive deregulation of gene expression. Greater ectopic expression of seed master regulatory genes in emf1 atx1 ult1 triple than in emf1 single mutants indicates that PcG and trxG factors together repress seed gene expression after germination. Furthermore, we found that the widespread gene derepression is associated with reduced levels of H3K27me3, an epigenetic repressive mark of gene expression, and with globally altered chromatin organization. EMF1, ATX1, and ULT1 are able to bind the chromatin of seed genes and ULT1 can physically interact with ATX1 and EMF1, suggesting that the trxG and EMF1 proteins directly associate at target gene loci for EMF1-mediated gene silencing. Thus, while ATX1, ULT1, and EMF1 interact antagonistically to regulate flowering, they work together to maintain chromatin integrity and prevent precocious seed gene expression after germination.

Epigenetic Regulation of Auxin-Induced Somatic Embryogenesis in Plants

“…Interestingly, depending on the plant's developmental stage that is controlled, the proteins of the PRC and TrxG complexes can interact in an antagonistic vs. cooperative manner. For example, to prevent any precocious seed gene expression after germination, the ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1), ULTRAPETALA1 (ULT1) of the TrxG, and EMF1 of the PRC1/2 work together to maintain chromatin integrity [21]. The TrxG proteins control gene expression in plant development via multiple mechanisms that include modifying the chromatin structure via the deposition of the H3K4me2/3 marker [161].…”

“…The TrxG factors, the ATX1 of H3K4me3 methyltransferase activity, and ULT1 interact physically to reduce the H3K27me3 marker in the targeted genes, including the SE-regulators, LEC1, LEC2, FUS3, and ABI3 [20]. The direct binding of both ATX1 and ULT1 to the seed gene loci, ABI3 and LEC2, was observed [21].…”

“…The essential regulatory function of TrxG/PRC complexes in the auxin-mediated processes implied a vast number of the auxin-related genes that showed a misregulation of expression in the mutants impaired in the genes encoding the TrxG and PRC proteins [21]. BRAHMA (BRM) of the TrxG complex has been found to directly activate the auxin efflux carriers (PINs) in part by antagonizing the H3K27me3-associated chromatin repression that is mediated by the PcG proteins [162].…”

“…The specific epigenetic marks that activate and repress gene transcription are indicated in green and red, respectively. Arrows and circle-shaped ends show the activation or repression of gene expression, respectively [14][15][16][17][18][19][20][21][22][23][24][25][26][27]. ( miRNAs, which are products of the MIRNA genes, are small (19 to 24 nucleotides long), single-stranded non-coding RNA molecules that regulate both the state of the chromatin-associated with their targets and the availability of the encoded transcripts for protein translation [26].…”

Source and Sink Relations Mediate Depletion of Intrinsic Cycad Seed Carbohydrates by Aulacaspis yasumatsui Infestation

“…Our revelations that reduced seed resources may partly explain poor germination and seedling performance of infested seeds do not exclude other causal factors. For example, epigenetic regulation of gene expression is heavily involved in seedto-seedling transition (Xu et al, 2018), and direct herbivory of seed integument tissues by the nonnative A. yasumatsui may directly alter these epigenetic phenomena. The study of the epigenetic basis of cycad seed development may allow for a better understanding of how A. yasumatsui herbivory negatively influences Cycas plants.…”