Balancing growth amidst salt stress - lifestyle perspectives from the extremophyte model Schrenkiella parvula.

Schrenkiella parvula, a leading extremophyte model in Brassicaceae, can grow and complete its lifecycle under multiple environmental stresses, including high salinity. Yet, the key physiological and structural traits underlying its stress-adapted lifestyle are unknown along with trade-offs when surviving salt stress at the expense of growth and reproduction. We aimed to identify the influential adaptive trait responses that lead to stress-resilient and uncompromised growth across developmental stages when treated with salt at levels known to inhibit growth in Arabidopsis and most crops. Its resilient growth was promoted by traits that synergistically allowed primary root growth in seedlings, the expansion of xylem vessels across the root-shoot continuum, and a high capacity to maintain tissue water levels by developing thicker succulent leaves while enabling photosynthesis during salt stress. A successful transition from vegetative to reproductive phase was initiated by salt-induced early flowering, resulting in viable seeds. Self-fertilization in salt-induced early flowering was dependent upon filament elongation in flowers otherwise aborted in the absence of salt during comparable plant ages. The maintenance of leaf water status promoting growth, and early flowering to ensure reproductive success in a changing environment, were among the most influential traits that contributed to the extremophytic lifestyle of S. parvula.

H3K4 trimethylation dynamics impact diverse developmental and environmental responses in plants.

MAIN CONCLUSION: The H3K4me3 histone mark in plants functions in the regulation of gene expression and transcriptional memory, and influences numerous developmental processes and stress responses. Plants execute developmental programs and respond to changing environmental conditions via adjustments in gene expression, which are modulated in part by chromatin structure dynamics. Histone modifications alter chromatin in precise ways on a global scale, having the potential to influence the expression of numerous genes. Trimethylation of lysine 4 on histone H3 (H3K4me3) is a prominent histone modification that is dogmatically associated with gene activity, but more recently has also been linked to gene repression. As in other eukaryotes, the distribution of H3K4me3 in plant genomes suggests it plays a central role in gene expression regulation, however the underlying mechanisms are not fully understood. Transcript levels of many genes related to flowering, root, and shoot development are affected by dynamic H3K4me3 levels, as are those for a number of stress-responsive and stress memory-related genes. This review examines the current understanding of how H3K4me3 functions in modulating plant responses to developmental and environmental cues.

Low-Phosphate Chromatin Dynamics Predict a Cell Wall Remodeling Network in Rice Shoots.

Phosphorus (P) is an essential plant macronutrient vital to fundamental metabolic processes. Plant-available P is low in most soils, making it a frequent limiter of growth. Declining P reserves for fertilizer production exacerbates this agricultural challenge. Plants modulate complex responses to fluctuating P levels via global transcriptional regulatory networks. Although chromatin structure plays a substantial role in controlling gene expression, the chromatin dynamics involved in regulating P homeostasis have not been determined. Here we define distinct chromatin states across the rice (Oryza sativa) genome by integrating multiple chromatin marks, including the H2A.Z histone variant, H3K4me3 modification, and nucleosome positioning. In response to P starvation, 40% of all protein-coding genes exhibit a transition from one chromatin state to another at their transcription start site. Several of these transitions are enriched in subsets of genes differentially expressed under P deficiency. The most prominent subset supports the presence of a coordinated signaling network that targets cell wall structure and is regulated in part via a decrease of H3K4me3 at transcription start sites. The P starvation-induced chromatin dynamics and correlated genes identified here will aid in enhancing P use efficiency in crop plants, benefitting global agriculture.

Rice H2A.Z negatively regulates genes responsive to nutrient starvation but promotes expression of key housekeeping genes.

The H2A.Z histone variant plays a role in the modulation of environmental responses, but the nature of the associated mechanisms remains enigmatic. We investigated global H2A.Z deposition and transcriptomic changes in rice (Oryza sativa) upon exposure to phosphate (Pi) deficiency and in response to RNAi knockdown of OsARP6, which encodes a key component of the H2A.Z exchange complex. Both Pi deficiency and OsARP6-knockdown resulted in similar, profound effects on global H2A.Z distribution. H2A.Z in the gene body of stress-responsive genes was negatively correlated with gene expression, and this was more apparent in response to Pi deficiency. In contrast, the role of H2A.Z at the transcription start site (TSS) was more context dependent, acting as a repressor of some stress-responsive genes, but an activator of some genes with housekeeping functions. This was especially evident upon OsARP6-knockdown, which resulted in down-regulation of a number of genes linked to chloroplast function that contained decreases in H2A.Z at the TSS. Consistently, OsARP6-RNAi plants exhibited lower chlorophyll content relative to the wild-type. Our results demonstrate that gene body-localized H2A.Z plays a prominent role in repressing stress-responsive genes under non-inductive conditions, whereas H2A.Z at the TSS functions as a positive or negative regulator of transcription.

Replacement of Arabidopsis H2A.Z with human H2A.Z orthologs reveals extensive functional conservation and limited importance of the N-terminal tail sequence for Arabidopsis development.

The incorporation of histone variants, distinct paralogs of core histones, into chromatin affects all DNA-templated processes in the cell, including the regulation of transcription. In recent years, much research has been focused on H2A.Z, an evolutionarily conserved H2A variant found in all eukaryotes. In order to investigate the functional conservation of H2A.Z histones during eukaryotic evolution we transformed h2a.z deficient plants with three human H2A.Z proteins to assess their ability to rescue the mutant defects. We discovered that human H2A.Z.1 and H2A.Z.2.1 fully complement the phenotypic abnormalities of h2a.z plants despite the fact that Arabidopsis and human H2A.Z N-terminal tail sequences are quite divergent. In contrast, the brain-specific splice variant H2A.Z.2.2 has a dominant-negative effect in wild-type plants. Furthermore, H2A.Z.1 almost completely re-establishes normal H2A.Z chromatin occupancy in h2a.z plants and restores the transcript levels of more than 84 % of misexpressed genes. Finally, our hypothesis that the N-terminal tail of Arabidopsis H2A.Z is not crucial for its developmental functions was supported by the ability of N-terminal end truncations of Arabidopsis HTA11 to largely rescue the defects of h2a.z mutants.

Histone Variants in the Specialization of Plant Chromatin.

The basic unit of chromatin, the nucleosome, is an octamer of four core histone proteins (H2A, H2B, H3, and H4) and serves as a fundamental regulatory unit in all DNA-templated processes. The majority of nucleosome assembly occurs during DNA replication when these core histones are produced en masse to accommodate the nascent genome. In addition, there are a number of nonallelic sequence variants of H2A and H3 in particular, known as histone variants, that can be incorporated into nucleosomes in a targeted and replication-independent manner. By virtue of their sequence divergence from the replication-coupled histones, these histone variants can impart unique properties onto the nucleosomes they occupy and thereby influence transcription and epigenetic states, DNA repair, chromosome segregation, and other nuclear processes in ways that profoundly affect plant biology. In this review, we discuss the evolutionary origins of these variants in plants, their known roles in chromatin, and their impacts on plant development and stress responses. We focus on the individual and combined roles of histone variants in transcriptional regulation within euchromatic and heterochromatic genome regions. Finally, we highlight gaps in our understanding of plant variants at the molecular, cellular, and organismal levels, and we propose new directions for study in the field of plant histone variants.