Qingzhu Zhang

Transgenerational epigenetic inheritance (TEI) enables plants to transmit adaptive chromatin states across generations. However, the mechanisms by which these states are maintained and stabilised during TEI remain unclear. Here, we investigate the TEI of repressive marks (H3K27me3 and DNA methylation) together with the active mark H3K4me3, which are associated with distinct reinforcement mechanisms, using reciprocal crosses of Arabidopsis ecotypes Col‐0 and C24. We show that all three marks undergo TEI but exhibit distinct inheritance patterns depending on their reinforcement mechanisms. These inheritance patterns are modulated by DDM1, which coordinates the propagation of repressive chromatin states. Our results indicate that chromatin remodelling, through its effects on nucleosome organisation and histone variant dynamics, plays a key role in shaping TEI via chromatin context in plants.

SUMMARY: Optimization of tree architecture is essential for advancing sustainable forestry, as appropriate canopy structure can contribute to growth and development. However, the molecular mechanisms that control tree architecture have not been fully characterized. While the putative NAD‐dependent histone deacetylase HST1 was shown to regulate branching architecture in multiple crop species, whether epigenetic mechanism also influence tree architecture is unknown. Here, we investigated the genetic regulation of branching angle in white birch ( Betula platyphylla Suk.), a pioneer tree of the temperate and boreal forests. Using bphst1 mutants generated via gene editing, we demonstrate that BpHST1 is involved in tree architecture by modulating branching angles. We provide evidence that BpHST1 is a histone deacetylase associated with altered H3K27ac levels and that it affects the expression of the cellulase gene CELLULASE 1 ( BpCEL1 ). Compared with the wild type , BpHST1 knockout and BpCEL1 overexpression both resulted in reduced branch angles, supporting BpCEL1 as a candidate downstream effector of BpHST1. Our study suggests that BpHST1 influences the birch architecture by altering H3K27 acetylation at the BpCEL1 locus, elucidating a previously unknown aspect of the epigenetic mechanisms that control tree architecture in white birch.

Although chromatin states are closely associated with epigenetic modifications, how they influence each other remains to be fully elucidated. In this study, we found that mutation of DECREASED IN DNA METHYLATION 1 (DDM1) in soybean leads to genome-wide chromatin homogenization, characterized by a loosening of heterochromatin and a tightening of euchromatin. This remodeling triggers 2 distinct molecular pathways: in heterochromatin, increased release of small RNAs activates the noncanonical RdDM pathway; while in euchromatin, transposable elements (TEs) are enriched with H3K9me2 modifications, which in turn activate the CMT2 pathway. Together, these pathways drive a pronounced burst of CHH methylation at the whole genome level. This epigenetic remodeling correlates with massive transcriptional dysregulation, upregulating stress responses and downregulating photosynthesis, linking local H3K9me2 changes on TEs, ultimately leading to severe phenotypes. Our findings reveal a unique, bidirectional pathway for CHH regulation in plants with complex chromatin states remodeling.

The plant kingdom works like a sophisticated chemical factory, where species ranging from dwarf herbs and shrubs to towering trees continuously synthesize a vast array of metabolites characterized by complex structures and diverse biological functions throughout their life (Weng et al., 2021). Traditionally, plant metabolism can be divided into primary and secondary metabolism, yet the boundary between these two has become increasingly difficult to distinguish (Palazon and Alcalde, 2025). These metabolites not only play a crucial role in plant growth and development but also serve as vital defense mechanisms enabling plants to cope with biotic and abiotic stresses and adapt to local climate change (Khan et al., 2025). The question now, however, is: How are this magical plant metabolites designed? In recent years, with the integration of multi-omics and molecular biology, scientists have been uncovering the blueprint of this metabolic biosynthesis at a high resolution, that is a "molecular architecture" governed by the genetic codes, transcriptional and epigenetic regulation. This editorial will focus on a series of recent studies that explore plant metabolic diversity with multi-omics methods, aiming to systematically elucidate the multi-layered complexity of its regulatory network and highlight tremendous potential for understanding plant chemical diversity.The core backbone of plant metabolic pathways is composed of a series of biosynthetic enzymes. For example, anthocyanins and lignin, key contributor to flower coloration and secondary wall formation, are synthesized through the phenylpropanoid pathway, in which chalcone synthase (CHS) play central role (Deng and Lu, 2017). Meanwhile, terpenoid compounds, which play roles in antioxidant defense, signal transduction, and stomatal movement, are derived from the mevalonate pathway involving farnesyl diphosphate synthase (FDPS) (Cheng et al., 2025). The variation in copy numbers, sequence diversity, gene family expansion or contraction of these functional genes encoding key biosynthetic enzymes constitute the fundamental genetic basis for chemical diversity both between and within plant species.In this editorial, Cao et al. (in this Research Topic) revealed that the mild aroma of Artemisia stolonifera results from the up-regulation of mevalonate pathway (e.g.， AACT1-4 and HMGR1-3) and sesquiterpene synthase genes, leading to the accumulation of sesquiterpenoids. In contrast, the wild aroma of A. argyi is attributed to the methylerythritol phosphate pathway (e.g, DXS2 and DXR1-5) and enhanced monoterpenoid and flavonoid biosynthesis, resulting in the enrichment of monoterpenoids and flavonoids. Wu et al. (in this Research Topic) found that the higher oxidation resistance of white Paeonia lactiflora compared to other varieties is linked to its higher content of paeoniflorin, polyphenols and flavonoids. Similarly, Zhang et al. (in this Research Topic) demonstrated that diverse sugarcane varieties adopted distinct adaptive molecular reprogramming strategies in response to ratooning decline. In addition, Liu et al. (in this Research Topic) identified a locus, UGT-Rd1, that is significantly associated with the protopanaxadiol ginsenoside Rd content. Its genetic variants not only obviously influence the efficiency of Rd ginsenoside biosynthesis but also exhibit specific genetic effects. Collectively, these findings suggest that metabolic diversity among different varieties is largely shaped by the genetic architecture of their biosynthetic enzymes. However, the 'chemical architecture' that is ultimately constructed also relies on higher-level and more dynamic regulatory mechanisms.Over the past decades, numerous transcription factors (TFs), such as MYB, bHLH, and WD40 members, have been demonstrated to play vital roles in regulating metabolic pathways including phenylpropanoid metabolism, the mevalonate pathway, alkaloid biosynthesis, epidermal wax biosynthesis, and glucosinolate biosynthesis (Xu et al., 2015). Such transcriptional regulation often shows tissue specificity. For example, Zhang et al. (in this Research Topic) discovered a molecular regulatory network directed by ARF, bHLH, GRAS, G2-like, and ARR-B TFs, which is significnatly associated with the spatially distribution patterns of auxin (IAA), gibberellin (GA), and cytokinin (CTK) in Cinnamomum burmanni. Furthermore, alternative splicing (AS) can also contribute to diversity in the protein structure and biological function of TFs. An et al. (in this Research Topic) found that the alternative transcripts of functional genes in the phenylpropanoid metabolism pathway including 4CL, CHS, F3H, DFR, GT, and ANR, as well as the regulatory factor bHLH, exhibit a significant positive correlation with flavonoid content in different tissues of Rosa roxburghii.Transcriptional regulation of plant metabolic diversity also exhibits time-course characteristics. For example, Zhang et al. (in this Research Topic) discovered that during the R3 stage of sugarcane ratoon decline, core genes such as galactinol synthase homologs, thiosulfate sulfurtransferase genes, and the E3 ubiquitin ligase gene may participate in mitigating the decline process through distinct molecular strategies involving the regulation of osmotic tolerance, oxidative defense, and protein homeostasis. This finding suggests that the reduction in sugarcane ratoon yield is closely related to a shift in root transcriptional regulation from growth maintenance toward senescence defense. In addition, Lei et al. (in this Research Topic) highlighted that the arginine and phenylalanine content in Amygdalus mongolica kernels increased along with their development, closely linked to dynamic changes in their biosynthesis genes such as glyA, SHMT, TYRAAT, YUCCA and SHMT, and their transcriptional regulation.Transcriptional regulation of plant metabolic diversity can be further affected by biotic and abiotic stresses. Bai et al. (in...

DNA methylation is a crucial epigenetic modification that is stably inherited across both mitotic and meiotic cell divisions in plants. It is regulated by multiple epigenetic pathways, and alterations in methylation can lead to phenotypic variation independent of changes in the DNA sequence. In this study, changes in DNA methylation triggered by the chromatin remodeler DDM1 (DECREASE IN DNA METHYLATION 1) were found to influence leaf phenotypes in Arabidopsis thaliana . The ddm1 mutation dramatically reduced genome‐wide DNA methylation, particularly in transposable elements (TEs). Hypomethylation of TEs activated downstream genes, including DPA4 ( DEVELOPMENT‐RELATED PCG TARGET IN THE APEX 4 ), which suppresses CUC2 ( CUP‐SHAPED COTYLEDON 2 ), a key regulator of leaf serration. Importantly, methylation changes in the DPA4 promoter were stably inherited in the F ₂ generation. This study identified DPA4 as a gene affected by the ddm1 mutation, which significantly affects leaf serration in A. thaliana . These findings highlight the impact of induced epigenetic modifications on plant development, providing a basis for further exploration of heritable epigenetic traits.

Chromatin remodeling factors efficiently and precisely establish, maintain, regulate, and distinguish between chromatin states in eukaryotes. DECREASE in DNA METHYLATION 1 (DDM1) is an important heterochromatin remodeling factor in plants that is responsible for maintaining heterochromatin DNA methylation and suppressing most transposable elements. Previous studies have predominantly focused on the effects of DDM1 on chromatin, with only a few focusing on its remodeling mechanisms. However, recent studies have greatly advanced understanding of the remodeling functions of DDM1 and, in particular, have clarified the mechanisms involved. In this review, we discuss the newly identified remodeling functions and mechanisms of DDM1. As DDM1 is closely involved in histone variant exchange, we first introduce the main histone variants associated with chromatin states in plants. Next, we focus on how DDM1 promotes the deposition of specific histone variants and describe its other remodeling functions. We propose that the core function of DDM1 is the regulation of histone variant distribution. DDM1 maintains heterochromatin by regulating the deposition of H2A and H3 variants, particularly by facilitating the exchange of specific histone variants.

Summary: FD, a conserved bZIP transcription factor, is well known for its role in promoting flowering. Here, we uncover that a short coding sequence of the Chrysanthemum morifolium FD gene, CmFDa, represses flowering. Interestingly, we identified CmFDa as a novel epiallele stringently regulated by DNA methylation in chrysanthemum for the first time. Epigenetic editing of the CmFDa promoter using the CRISPR‐dCas9‐TET1cd for demethylation or dCas9‐SunTag‐NtDRM2cd for methylation can, respectively, repress or promote flowering. CmFDa epigenetically represses the floral transition by suppressing the expression of the floral activators CmSOC1 and CmAP1. We show that CmFDa recruits the Polycomb‐repressive complex 2 (PRC2) to the CmSOC1 and CmAP1 promoters. These results reveal that CmFDa is an inhibitor of flowering by epigenetic repression of flowering integrator genes. This study provides a novel strategy for the epigenetic improvement of flowering time in plants.

Summary: Flower color is an important character of ornamental plants and one of the main target traits for variety innovation. We previously identified a CmMYB6 epigenetic allele that affects the flower color in chrysanthemum, and changes in flower color are caused by the DNA methylation level of this gene. However, it is still unknown which DNA methyltransferases are involved in modifying the DNA methylation levels of this gene. Here, we used dead Cas9 (dCas9) together with DNA methyltransferases that methylate cytosine residues in the CHH context to target the CmMYB6 promoter through transient and stable transformation methods. We found that CmDRM2a increased the DNA methylation level of the CmMYB6 promoter, the expression of CmMYB6 decreased and a lighter flower color resulted. By contrast, both CmDRM2b and CmCMT2 enhanced DNA methylation levels of the CmMYB6 promoter, the expression of CmMYB6 increased and a deeper flower color resulted. Furthermore, the regulatory mechanism of DNA methyltransferase in the formation of chrysanthemum flower color was investigated, pointing to a new strategy for silencing or activating CmMYB6 epiallele to regulate anthocyanin synthesis. This lays a solid foundation for regulating flower color in chrysanthemum through epigenetic breeding.