Histone dynamics responding to internal and external cues underlying plant development.

Plants necessitate a refined coordination of growth and development to effectively respond to external triggers for survival and successful reproduction. This intricate harmonization of plant developmental processes and adaptability hinges on significant alterations within their epigenetic landscapes. In this review, we first delve into recent strides made in comprehending underpinning the dynamics of histones, driven by both internal and external cues. We encapsulate the prevailing working models through which cis/trans elements navigate the acquisition and removal of histone modifications, as well as the substitution of histone variants. As we look ahead, we anticipate that delving deeper into the dynamics of epigenetic regulation at the level of individual cells or specific cell types will significantly enrich our comprehension of how plant development unfolds under the influence of internal and external cues. Such exploration holds the potential to provide unprecedented resolution in understanding the orchestration of plant growth and development.

Comprehensive regulatory networks for tomato organ development based on the genome and RNAome of MicroTom tomato.

MicroTom has a short growth cycle and high transformation efficiency, and is a prospective model plant for studying organ development, metabolism, and plant-microbe interactions. Here, with a newly assembled reference genome for this tomato cultivar and abundant RNA-seq data derived from tissues of different organs/developmental stages/treatments, we constructed multiple gene co-expression networks, which will provide valuable clues for the identification of important genes involved in diverse regulatory pathways during plant growth, e.g. arbuscular mycorrhizal symbiosis and fruit development. Additionally, non-coding RNAs, including miRNAs, lncRNAs, and circRNAs were also identified, together with their potential targets. Interacting networks between different types of non-coding RNAs (miRNA-lncRNA), and non-coding RNAs and genes (miRNA-mRNA and lncRNA-mRNA) were constructed as well. Our results and data will provide valuable information for the study of organ differentiation and development of this important fruit. Lastly, we established a database (http://eplant.njau.edu.cn/microTomBase/) with genomic and transcriptomic data, as well as details of gene co-expression and interacting networks on MicroTom, and this database should be of great value to those who want to adopt MicroTom as a model plant for research.

A robust mechanism for resetting juvenility during each generation in Arabidopsis.

Multicellular organisms undergo several developmental transitions during their life cycles. In contrast to animals, the plant germline is derived from adult somatic cells. As such, the juvenility of a plant must be reset in each generation. Previous studies have demonstrated that the decline in the levels of miR156/7 with age drives plant maturation. Here we show that the resetting of plant juvenility during each generation is mediated by de novo activation of MIR156/7 in Arabidopsis. Blocking this process leads to a shortened juvenile phase and premature flowering in the offspring. In particular, an Arabidopsis plant devoid of miR156/7 flowers even without formation of rosette leaves in long days. Mechanistically, we find that different MIR156/7 genes are reset at different developmental stages through distinct reprogramming routes. Among these genes, MIR156A, B and C are activated de novo during sexual reproduction and embryogenesis, while MIR157A and C are reset upon seed germination. This redundancy generates a robust reset mechanism that ensures accurate restoration of the juvenile phase in each plant generation.

Cell division in the shoot apical meristem is a trigger for miR156 decline and vegetative phase transition in Arabidopsis.

What determines the rate at which a multicellular organism matures is a fundamental question in biology. In plants, the decline of miR156 with age serves as an intrinsic, evolutionarily conserved timer for the juvenile-to-adult phase transition. However, the way in which age regulates miR156 abundance is poorly understood. Here, we show that the rate of decline in miR156 is correlated with developmental age rather than chronological age. Mechanistically, we found that cell division in the apical meristem is a trigger for miR156 decline. The transcriptional activity of MIR156 genes is gradually attenuated by the deposition of the repressive histone mark H3K27me3 along with cell division. Our findings thus provide a plausible explanation of why the maturation program of a multicellular organism is unidirectional and irreversible under normal growth conditions and suggest that cell quiescence is the fountain of youth in plants.

Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis.

The non-random three-dimensional organization of genomes is critical for many cellular processes. Recently, analyses of genome-wide chromatin packing in the model dicot plant Arabidopsis thaliana have been reported 1-4 . At a kilobase scale, the A. thaliana chromatin interaction network is highly correlated with a range of genomic and epigenomic features 1-4 . Surprisingly, topologically associated domains (TADs), which appear to be a prevalent structural feature of genome packing in many animal species, are not prominent in the A. thaliana genome 1,2,4-6 . Using a genome-wide chromatin conformation capture approach, Hi-C (ref. 7 ), we report high-resolution chromatin packing patterns of another model plant, rice. We unveil new structural features of chromatin organization at both chromosomal and local levels compared to A. thaliana, with thousands of distinct TADs that cover about a quarter of the rice genome. The rice TAD boundaries are associated with euchromatic epigenetic marks and active gene expression, and enriched with a sequence motif that can be recognized by plant-specific TCP proteins. In addition, we report chromosome decondensation in rice seedlings undergoing cold stress, despite local chromatin packing patterns remaining largely unchanged. The substantial variation found already in a comparison of two plant species suggests that chromatin organization in plants might be more diverse than in multicellular animals.

Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery.

The nuclear space is not a homogeneous biochemical environment. Many studies have demonstrated that the transcriptional activity of a gene is linked to its positioning within the nuclear space. Following the discovery of lamin-associated domains (LADs), which are transcriptionally repressed chromatin regions, the nonrandom positioning of chromatin at the nuclear periphery and its biological relevance have been studied extensively in animals. However, it remains unknown whether comparable chromatin organizations exist in plants. Here, using a strategy using restriction enzyme-mediated chromatin immunoprecipitation, we present genome-wide identification of nonrandom domain organization of chromatin at the peripheral zone of Arabidopsis thaliana nuclei. We show that in various tissues, 10%-20% of the regions on the chromosome arms are anchored at the nuclear periphery, and these regions largely overlap between different tissues. Unlike LADs in animals, the identified domains in plants are not gene-poor or A/T-rich. These domains are enriched with silenced protein-coding genes, transposable element genes, and heterochromatic marks, which collectively define a repressed environment. In addition, these domains strongly correlate with our genome-wide chromatin interaction data set (Hi-C) by largely explaining the patterns of chromatin compartments, revealed on Hi-C maps. Moreover, our results reveal a spatial compartment of different DNA methylation pathways that regulate silencing of transposable elements, where the CHH methylation of transposable elements located at the nuclear periphery and in the interior are preferentially mediated by CMT2 and DRM methyltransferases, respectively. Taken together, the results demonstrate functional partitioning of the Arabidopsis genome in the nuclear space.