Epigenetic mechanisms are integral to plant growth, development, and adaptation to environmental stimuli. Over the past two decades, our comprehension of these complex regulatory processes has expanded remarkably, producing a substantial body of knowledge on both locus-specific mechanisms and genome-wide regulatory patterns. Studies initially grounded in the model plant Arabidopsis have been broadened to encompass a diverse array of crop species, revealing the multifaceted roles of epigenetics in physiological and agronomic traits. With recent technological advancements, epigenetic regulations at the single-cell level and at the large-scale population level are emerging as new focuses. This review offers an in-depth synthesis of the diverse epigenetic regulations, detailing the catalytic machinery and regulatory functions. It delves into the intricate interplay among various epigenetic elements and their collective influence on the modulation of crop traits. Furthermore, it examines recent breakthroughs in technologies for epigenetic modifications and their integration into strategies for crop improvement. The review underscores the transformative potential of epigenetic strategies in bolstering crop performance, advocating for the development of efficient tools to fully exploit the agricultural benefits of epigenetic insights.

Plants must reprogram gene expression to adapt constantly changing environmental temperatures. With the increased occurrence of extremely low temperatures, the negative effects on plants, especially on growth and development, from cold stress are becoming more and more serious. In this research, strand-specific RNA sequencing (ssRNA-seq) was used to explore the dynamic changes in the transcriptome landscape of Arabidopsis thaliana exposed to cold temperatures (4°C) at different times. In total, 7,623 differentially expressed genes (DEGs) exhibited dynamic temporal changes during the cold treatments. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis showed that the DEGs were enriched in cold response, secondary metabolic processes, photosynthesis, glucosinolate biosynthesis, and plant hormone signal transduction pathways. Meanwhile, long non-coding RNAs (lncRNAs) were identified after the assembly of the transcripts, from which 247 differentially expressed lncRNAs (DElncRNAs) and their potential target genes were predicted. 3,621 differentially alternatively spliced (DAS) genes related to RNA splicing and spliceosome were identified, indicating enhanced transcriptome complexity due to the alternative splicing (AS) in the cold. In addition, 739 cold-regulated transcription factors (TFs) belonging to 52 gene families were identified as well. This research analyzed the dynamic changes of the transcriptome landscape in response to cold stress, which reveals more complete transcriptional patterns during short- and long-term cold treatment and provides new insights into functional studies of that how plants are affected by cold stress.

The Arabidopsis floral repressor locus FLC is epigenetically silenced during winter cold to align flowering with spring. During weeks of cold exposure, FLC transcription is progressively reduced both by transcriptional repression mediated by FLC antisense transcription and epigenetic silencing implemented through a Polycomb-mediated epigenetic switch. In the warm, FLC is transcriptionally repressed by coordinated changes in transcription initiation and RNA PolII speed in a mechanism involving proximal termination. Whether similar mechanisms contribute to the cold-induced FLC transcriptional repression is unknown. Here, we combine mathematical modelling and transcription profiling to investigate FLC transcriptional changes during the cold. We find different dynamics of spliced and unspliced transcripts during cold exposure with only a small change in PolII speed. We also show that, unlike short-term cold, long-term cold temperatures drive an increase in splicing rates while simultaneously reducing productive transcription at FLC. This process is influenced by antisense COOLAIR transcription but does not rely on proximal COOLAIR termination. Cold-induced transcriptional repression of FLC thus involves a decoupling of changes in productive transcription initiation from PolII speed and rates of co-transcriptional splicing, a different mechanism from that repressing FLC in the warm.

Plants use seasonal cold to time the transition to reproductive development. Short- and long-term cold exposure is registered via parallel transcriptional shutdown and Polycomb-dependent epigenetic silencing of the Arabidopsis thaliana major flowering repressor locus FLOWERING LOCUS C ( FLC ). The cold-induced antisense transcripts ( COOLAIR ) determine the dynamics of FLC transcriptional shutdown, but the thermosensory mechanisms are still unresolved. Here, through a forward genetic screen, we identify a mutation that perturbs cold-induced COOLAIR expression and FLC repression. The mutation is a hypomorphic allele of SUPPRESSORS OF MEC-8 AND UNC-52 1 (SMU1), a conserved subunit of the spliceosomal B complex. SMU1 interacts in vivo with the proximal region of nascent COOLAIR and RNA 3′ processing/cotranscriptional regulators and enhances COOLAIR proximal intron splicing to promote specific COOLAIR isoforms. SMU1 also interacts with ELF7, an RNA Polymerase II Associated Factor (Paf1) component and limits COOLAIR transcription. Cold thus changes cotranscriptional splicing/RNA Pol II functionality in an SMU1-dependent mechanism to promote two different isoforms of COOLAIR that lead to reduced FLC transcription. Such cotranscriptional mechanisms are emerging as important regulators underlying plasticity in gene expression.

Transcription factors (TFs) tightly control plant development by regulating gene expression. The phase separation of TFs plays a vital role in gene regulation. Many plant TFs have the potential to form phase-separated protein condensates; however, little is known about which TFs are regulated by phase separation and how it affects their roles in plant development. Here, we report that the rice (Oryza sativa) single Myb TF TELOMERE REPEAT-BINDING FACTOR 2 (TRBF2) is highly expressed in fast-growing tissues at the seedling stage. TRBF2 is a transcriptional repressor that binds to the transcriptional start site of thousands of genes. Mutation of TRBF2 leads to pleiotropic developmental defects and misexpression of many genes. TRBF2 displays characteristics consistent with phase separation in vivo and forms phase-separated condensates in vitro. The H1/H5 domain of TRBF2 plays a crucial role in phase separation, chromatin targeting, and gene repression. Replacing the H1/H5 domain by a phase-separated intrinsically disordered region from Arabidopsis (Arabidopsis thaliana) AtSERRATE partially recovers the function of TRBF2 in gene repression in vitro and in transgenic plants. We also found that TRBF2 is required for trimethylation of histone H3 Lys27 (H3K27me3) deposition at specific genes and genome wide. Our findings reveal that phase separation of TRBF2 facilitates gene repression in rice development.