Samuel Burrows, Delfi Dorussen, Joseph Crudgington, Giorgia Di Santolo, James Simmonds, Marco Catoni, Philippa Borrill
{"title":"Partial redundancy buffers deleterious effects of mutating DNA methyltransferase 1-1 (MET1-1) in polyploid wheat.","authors":"Samuel Burrows, Delfi Dorussen, Joseph Crudgington, Giorgia Di Santolo, James Simmonds, Marco Catoni, Philippa Borrill","doi":"10.1093/jxb/eraf016","DOIUrl":"10.1093/jxb/eraf016","url":null,"abstract":"<p><p>DNA methylation plays important roles in gene expression, transposable element silencing, and genome stability. Altering DNA methylation could generate additional phenotypic variation for crop breeding, however the lethality of epigenetic mutants in crop species has hindered its investigation. Here, we exploit partial redundancy between homoeologues in polyploid wheat to generate viable mutants in the DNA methyltransferase 1-1 (MET1-1) gene with altered methylation profiles. In Triticum turgidum (tetraploid wheat) and Triticum aestivum (hexaploid wheat), we found under-representation of higher order mutants (5/6 and 6/6 mutant met1-1 copies in hexaploid wheat and 3/4 and 4/4 copies in tetraploid wheat) when genotyping segregating seeds and seedlings, due to reduced transmission of null mutant gametes from the paternal and maternal side. The loss of four or more functional copies of MET1-1 results in decreased CG methylation in hexaploid wheat. Changes to gene expression increase stepwise with the number of mutant alleles, suggesting a dosage-dependent effect. We identified heritable changes to flowering and awn phenotypes which segregate independently of MET1-1. Together our results demonstrate that polyploidy can be leveraged to generate quantitative changes to CG methylation without the lethal consequences observed in other crops.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2500-2516"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143795593","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Using targeted genome methylation for crop improvement.","authors":"Zhibo Wang, Rebecca S Bart","doi":"10.1093/jxb/eraf131","DOIUrl":"10.1093/jxb/eraf131","url":null,"abstract":"<p><p>Genome editing allows scientists to specifically change the DNA sequence of an organism. This powerful technology now fuels basic biology discovery and tangible crop improvement efforts. There is a less well understood layer of information encoded in genomes, known collectively as 'epigenetics', that impacts gene expression, without changing the DNA sequence. Epigenetic processes allow organisms to rapidly respond to environmental fluctuation. Like genome editing, recent advances have demonstrated that it is possible to edit the epigenome of a plant and cause heritable phenotypic changes. In this review, we aim to specifically consider the unique advantages that targeted epigenome editing might provide over existing biotechnology tools. This review is aimed at a broad audience. We begin with a high-level overview of the tools currently available for crop improvement. Next, we present a more detailed overview of the key discoveries that have been made in recent years, primarily using the model system Arabidopsis, new efforts to extend targeted methylation to crop plants, the current status of the technology, and the challenges that remain to realize the full potential of targeted epigenome editing. We end with a forward-looking commentary on how epi-alleles might interface with breeding programs across a variety of crops.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2394-2404"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143663508","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Cytidine analogs in plant epigenetic research and beyond.","authors":"Eva Dvořák Tomaštíková, Ales Pecinka","doi":"10.1093/jxb/erae522","DOIUrl":"10.1093/jxb/erae522","url":null,"abstract":"<p><p>Cytosine (DNA) methylation plays important roles in silencing transposable elements, plant development, genomic imprinting, stress responses, and maintenance of genome stability. To better understand the functions of this epigenetic modification, several tools have been developed to manipulate DNA methylation levels. These tools include mutants of DNA methylation writers and readers, targeted manipulation of locus-specific methylation, and the use of chemical inhibitors. Here, we summarize the effects of commonly used cytidine analog chemical inhibitors, represented by zebularine, 5-azacytidine, and their related compounds, on plants. These analogs are incorporated into chromosomal DNA, where they block the activity of the replicative CG DNA methyltransferase 1 (MET1). This leads to manifold alterations in the plant epigenome, modified developmental programs, or suppression of hybridization barriers. We also highlight the DNA-damaging effects of cytidine analogs, particularly the formation of stable DNA-protein crosslinks between DNA and MET1. This phenomenon sheds new light on specific phenotypes observed upon treatment with cytidine analogs. In conclusion, cytidine analogs are a vital tool for plant genome research and have the potential to open new promising avenues for applications in plant biotechnology and breeding.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2419-2432"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142895073","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Non-coding and epigenetic mechanisms in the regulation of seed germination in Arabidopsis thaliana.","authors":"Benjamin J M Tremblay, Julia I Qüesta","doi":"10.1093/jxb/eraf051","DOIUrl":"10.1093/jxb/eraf051","url":null,"abstract":"<p><p>Seed germination as a developmental process has been extensively studied using the model plant Arabidopsis thaliana. Its seed biology is generally well understood, from the regulation of seed maturation and dormancy to germination and the post-germinative transition. These events are the result of extensive transcriptional reprogramming mediated by essential epigenetic mechanisms such as DNA methylation, different histone variants and modifications, and non-coding regulatory RNAs. Studying these mechanisms is essential for understanding the regulation of gene expression during germination. In this review, we summarize our current knowledge of the mechanisms regulating seed biology in Arabidopsis and discuss aspects requiring further study.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2455-2467"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143365063","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"TORquing chromatin: the regulatory role of TOR kinase in chromatin function.","authors":"Yihan Dong, Fatemeh Aflaki, Iva Mozgova, Alexandre Berr","doi":"10.1093/jxb/erae474","DOIUrl":"10.1093/jxb/erae474","url":null,"abstract":"<p><p>The target of rapamycin (TOR) kinase is a critical regulator of plant growth and development, integrating environmental and internal signals to modulate cellular processes. This review explores the emerging role of TOR in chromatin regulation, focusing on its nuclear activities and interactions with chromatin remodeling factors. We highlight the mechanisms by which TOR influences chromatin structure and gene expression, including its involvement in histone modifications and DNA methylation. Additionally, we discuss the interplay between TOR signaling, the cytoskeleton, and nuclear functions, emphasizing the potential of TOR to act as a bridge between cytoskeletal dynamics and chromatin regulation. Finally, besides TOR-mediated cyto-nuclear shuttling and metabolic regulation, we address the translational control of chromatin components by TOR as additional layers impacting the chromatin landscape. We also propose future research directions to further elucidate the complex regulatory network governed by TOR in plant cells.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2405-2418"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142681819","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ashley Baldwin, Tamara Lechon, Angela Marchbank, Simon Scofield, Kerstin Lieu, Charlotte L Wilson, Richard A Ludlow, Robert J Herbert, Hans-Wilhelm Nützmann, Hilary J Rogers
{"title":"The H3K27me3 histone mark correlates with repression of colour and aroma development post-harvest in strawberry fruit.","authors":"Ashley Baldwin, Tamara Lechon, Angela Marchbank, Simon Scofield, Kerstin Lieu, Charlotte L Wilson, Richard A Ludlow, Robert J Herbert, Hans-Wilhelm Nützmann, Hilary J Rogers","doi":"10.1093/jxb/erae464","DOIUrl":"10.1093/jxb/erae464","url":null,"abstract":"<p><p>Strawberry ripening is non-climacteric, and post-harvest fruit enter senescence and deteriorate rapidly. Chilled storage induces transcriptome-wide changes in gene expression, including down-regulation of aroma-related genes. Histone marks are associated with transcriptional activation or repression; the H3K27me3 mark is mainly associated with repression of gene expression. Here genes associated with H3K27me3 were identified through ChIP-seq in ripe red strawberry fruit at harvest and after 5 d of chilled storage in the dark. The number of ChIP peaks increased with storage time, indicating an increased role for this mark in regulation of gene expression following chilled dark storage. Comparing ChIP-seq data with RNA-seq data from the same material identified 440 genes whose expression correlated with H3K27me3 repression. Abiotic stress genes, especially cold stress response genes, were down-regulated during storage. Increased association with the H3K27me3 mark indicated that they may be repressed via this epigenetic mark. Other functional groups included cell wall and carbohydrate metabolism. The association with the H3K27me3 mark of two transcription factor genes (FaHY5 and FaTRAB1) and of FaADH, involved in ester biosynthesis, was validated by ChIP-PCR. These three genes were all down-regulated during storage and indicated a network of H3K27me3 gene repression affecting both anthocyanin and ester biosynthesis.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2487-2499"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142639005","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"A complex interplay between histone variants and DNA methylation.","authors":"Alejandro Edera, Leandro Quadrana","doi":"10.1093/jxb/eraf030","DOIUrl":"10.1093/jxb/eraf030","url":null,"abstract":"<p><p>Nucleosomes, the chromatin building blocks, play an important role in controlling DNA and chromatin accessibility. Nucleosome remodeling and the incorporation of distinct histone variants confer unique structural and biochemical properties, influencing the targeting of multiple epigenetic pathways, particularly DNA methylation. This stable epigenetic mark suppresses transposable element expression in plants and mammals, serving as an additional layer of chromatin regulation. In this review, we explore recent advances in our understanding of the complex interplay between histone variants and DNA methylation in plants, and discuss the role that chromatin remodeling plays in coordinating histone exchange and methylation of DNA.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2468-2477"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143047099","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Non-CG DNA methylation represses SDC expression to modulate hypocotyl elongation during thermormorphogenesis in Arabidopsis.","authors":"Maián Garro, Eleonora Greco, Gustavo J Vannay, Aleksandra Leonova, Leonardo Bruno, Matías Capella","doi":"10.1093/jxb/eraf105","DOIUrl":"10.1093/jxb/eraf105","url":null,"abstract":"<p><p>Plants adapt to warm environments through physiological and morphological changes termed thermomorphogenesis, which involve transcriptional reprogramming exerted mainly by PHYTOCHROME INTERACTING FACTOR 4 (PIF4). Fluctuating temperatures can also influence the patterns of cytosine DNA methylation (DNAme), thereby influencing gene expression; however, whether these epigenetic changes provide an adaptative advantage remains unclear. Here, we provide evidence that DNAme is required to regulate thermomorphogenesis in Arabidopsis. Hypomethylated drm1 drm2 cmt3 mutants and seedlings treated with 5-azacytidine to block DNAme exhibited reduced hypocotyl growth at warm temperatures, primarily due to impaired cell elongation. Moreover, DNA hypomethylation compromised auxin biosynthesis and transport in response to warmth, partially by reducing PIF4 protein levels. Notably, the loss of DNAme led to increased expression of SUPPRESSOR OF drm1 drm2 cmt3 (SDC), which in turn restricted hypocotyl elongation during thermomorphogenesis. Finally, DNAme was found to regulate the inhibition of SDC expression to promote gibberellin biosynthesis. Our findings underscore the critical role of DNAme in modulating gene expression in response to temperature fluctuations and provide new insights into the epigenetic regulation of thermomorphogenesis.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2517-2534"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143597200","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"DNA methylation dynamics in the shoot apical meristem.","authors":"Jie Yang, Frank Johannes","doi":"10.1093/jxb/eraf024","DOIUrl":"10.1093/jxb/eraf024","url":null,"abstract":"<p><p>The shoot apical meristem (SAM) is pivotal for plant development, acting as the source of all aerial tissues and the origin of the gametes. Despite extensive knowledge of the regulation of stem cell pool size, organ initiation, and patterning at the SAM periphery, the epigenetic landscape of SAM cells remains largely unexplored. Here, we review recent attempts to characterize the spatio-temporal dynamics of DNA methylation in the SAM, including its role in stress responses, memory, control of the activity of transposable elements in the initiation of reproductive cell lineages, and its association with stem cell fate. We highlight several technological opportunities for future epigenetic studies of the SAM, especially at the single-cell level. These include the use of spatial DNA methylation sequencing, joint transcriptome-methylome analysis, and the use of stochastic DNA methylation changes for cell lineage tracing.</p>","PeriodicalId":15820,"journal":{"name":"Journal of Experimental Botany","volume":" ","pages":"2478-2486"},"PeriodicalIF":5.6,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143046325","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}