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The greening of young seedling is light induced but vulnerable to photo-oxidative stress at the same time, due to the immature status of chloroplasts. Accumulation of anthocyanin is a protective response to high light, by absorbing excess energy and serving as antioxidant. In this work with Arabidopsis, we found that GARP family transcription factors GOLDEN2-LIKE 2 (GLK2), as a key regulator to chloroplast development, also plays an intensive role in regulating anthocyanin biosynthesis during seedling de-etiolation, especially under high light stress. We demonstrate that GLK2 positively regulates anthocyanin biosynthesis by directly activating the transcription of anthocyanin late biosynthetic genes (LBGs) as well asTRANSPARENT TESTA GLABRA 1(TTG1) gene, which encodes a key component of the regulatory MYB–bHLH–WDR (MBW) complex (which also activates LBGs). Our data further show that GLK2 and MBW each could activate the expression ofDFRgene (key LBG) independently, via distinct promoter regions. We therefore propose a multifaceted involvement of GLK2 in anthocyanin biosynthesis as an important protective measure for developing chloroplasts, against excessive light exposure during seedling photomorphogenesis.

The apoplast of plant leaf, the intercellular space between mesophyll cells, is normally largely filled with air with a minimal amount of water in it, which is essential for key physiological processes such as gas exchange to occur. Interestingly, phytopathogens exploit virulence factors to induce a water-rich environment, known as “water soaking”, in the apoplast of the infected leaf tissue to promote disease. We propose that plants evolved a “water soaking” pathway, which normally keeps a “minimized and balanced” water level in the leaf apoplast for plant growth but is disturbed by microbial pathogens to facilitate infection. Investigation of the “water soaking” pathway and leaf water control mechanisms is a fundamental, yet previously-overlooked, aspect of plant physiology. To identify key components in the “water soaking” pathway, we performed a genetic screen to isolate Arabidopsis severe water soaking (sws) mutants that show leaf water over-accumulation under high air humidity, a condition required for visible water soaking. Here we report the sws1 mutant, which displays rapid water soaking upon high humidity treatment due to a loss-of-function mutation in CURLY LEAF (CLF), encoding a histone methyl-transferase in the POLYCOMB REPRESSIVE COMPLEX 2 (PRC2). We found that the sws1 (clf) mutant exhibits an enhanced abscisic acid (ABA) level and stomatal closure, which are indispensable for its water soaking phenotype and mediated by CLF’s direct regulation of a group of ABA-associated NAC transcription factors, NAC019/055/072. Interestingly, the clf mutant showed a weakened immunity, which likely also contributes to the water soaking phenotype. In addition, the clf plant supports a significantly higher level of Pseudomonas syringae pathogen-induced water soaking and bacterial multiplication, in an ABA pathway and NAC019/055/072-dependent manner. Collectively, our study probes into a fundamental question in plant biology and demonstrates CLF as a key modulator of leaf water status via epigenetic regulation of ABA pathway and stomatal movement.

The juvenile-to-adult transition in plants involves changes in vegetative growth and plant architecture; the timing of this transition has important implications for agriculture. The microRNA miR156 regulates this transition and shoot maturation in plants. In Arabidopsis thaliana, deposition of histone H3 trimethylation on lysine 27 (H3K27me3, a repressive mark) at the MIR156A/C loci is regulated by Polycomb Repressive Complex 1 (PRC1) or PRC2, depending on the developmental stage. The levels of miR156 progressively decline during shoot maturation. The amount of H3K27me3 at MIR156A/C loci affects miR156 levels; however, whether this epigenetic regulation is conserved remains unclear. Here, we found that in rice (Oryza sativa), the putative PRC1 subunit LIKE HETEROCHROMATIN PROTEIN 1 (OsLHP1), with the miR156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) module, affects developmental phase transitions. Loss of OsLHP1 function results in ectopic expression of MIR156B/C/I/E, phenocopy of miR156 overexpression, and reduced H3k27me3 levels at MIR156B/C/I/E. This indicates that OsLHP1 has functionally diverged from Arabidopsis LHP1. Genetic and transcriptome analyses of wild-type, miR156b/c-overexpression, and Oslhp1-2 mutant plants suggest that OsLHP1 acts upstream of miR156 and SPL during the juvenile-to-adult transition. Therefore, modifying the OsLHP1-miR156-SPL pathway may enable alteration of the vegetative period and plant architecture.

A chromosome-level genome assembly of the bread wheat variety Chinese Spring (CS) has recently been published. Genome-wide identification of regulatory elements (REs) responsible for regulating gene activity is key to further mechanistic studies. Because epigenetic activity can reflect RE activity, defining chromatin states based on epigenomic features is an effective way to detect REs. Here, we present the web-based platform Chinese Spring chromatin state (CSCS), which provides CS chromatin signature information. CSCS includes 15 recently published epigenomic data sets including open chromatin and major chromatin marks, which are further partitioned into 15 distinct chromatin states. CSCS curates detailed information about these chromatin states, with trained self-organization mapping (SOM) for segments in all chromatin states and JBrowse visualization for genomic regions or genes. Motif analysis for genomic regions or genes, GO analysis for genes and SOM analysis for new epigenomic data sets are also integrated into CSCS. In summary, the CSCS database contains the combinatorial patterns of chromatin signatures in wheat and facilitates the detection of functional elements and further clarification of regulatory activities. We illustrate how CSCS enables biological insights using one example, demonstrating that CSCS is a highly useful resource for intensive data mining. CSCS is available at http://bioinfo.cemps.ac.cn/CSCS/. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s42994-021-00048-z.

Background Bread wheat is an allohexaploid species with a 16-Gb genome that has large intergenic regions, which presents a big challenge for pinpointing regulatory elements and further revealing the transcriptional regulatory mechanisms. Chromatin profiling to characterize the combinatorial patterns of chromatin signatures is a powerful means to detect functional elements and clarify regulatory activities in human studies. Results In the present study, through comprehensive analyses of the open chromatin, DNA methylome, seven major chromatin marks, and transcriptomic data generated for seedlings of allohexaploid wheat, we detected distinct chromatin architectural features surrounding various functional elements, including genes, promoters, enhancer-like elements, and transposons. Thousands of new genic regions and cis-regulatory elements are identified based on the combinatorial pattern of chromatin features. Roughly 1.5% of the genome encodes a subset of active regulatory elements, including promoters and enhancer-like elements, which are characterized by a high degree of chromatin openness and histone acetylation, an abundance of CpG islands, and low DNA methylation levels. A comparison across sub-genomes reveals that evolutionary selection on gene regulation is targeted at the sequence and chromatin feature levels. The divergent enrichment of cis-elements between enhancer-like sequences and promoters implies these functional elements are targeted by different transcription factors. Conclusions We herein present a systematic epigenomic map for the annotation of cis-regulatory elements in the bread wheat genome, which provides new insights into the connections between chromatin modifications and cis-regulatory activities in allohexaploid wheat. Electronic supplementary material The online version of this article (10.1186/s13059-019-1746-8) contains supplementary material, which is available to authorized users.

Triticeae species, including wheat, barley, and rye, are critical for global food security. Mapping agronomically important genes is crucial for elucidating molecular mechanisms and improving crops. However, Triticeae includes many wild relatives with desirable agronomic traits, and frequent introgressions occurred during Triticeae evolution and domestication. Thus, Triticeae genomes are generally large and complex, making the localization of genes or functional elements that control agronomic traits challenging. Here, we developed Triti-Map, which contains a suite of user-friendly computational packages specifically designed and optimized to overcome the obstacles of gene mapping in Triticeae, as well as a web interface integrating multi-omics data from Triticeae for the efficient mining of genes or functional elements that control particular traits. The Triti-Map pipeline accepts both DNA and RNA bulk-segregated sequencing data as well as traditional QTL data as inputs for locating genes and elucidating their functions. We illustrate the usage of Triti-Map with a combination of bulk-segregated ChIP-seq data to detect a wheat disease-resistance gene with its promoter sequence that is absent from the reference genome and clarify its evolutionary process. We hope that Triti-Map will facilitate gene isolation and accelerate Triticeae breeding.

The phytohormone abscisic acid (ABA)-induced leaf senescence facilitates nutrient reuse and potentially contributes to enhancing plant stress tolerance. However, excessive senescence causes serious reductions in crop yield, and the mechanism by which senescence is finely tuned at different levels is still insufficiently understood. Here, we found that the double mutant of core enzymes of the polycomb repressive complex 2 (PRC2) is hypersensitive to ABA in Arabidopsis thaliana. To elucidate the interplay between ABA and PRC2 at the genome level, we extensively profiled the transcriptomic and epigenomic changes triggered by ABA. We observed that H3K27me3 preferentially targets ABA-induced senescence-associated genes (SAGs). In the double, but not single, mutant of PRC2 enzymes, these SAGs were derepressed and could be more highly induced by ABA compared with the wild-type, suggesting a redundant role for the PRC2 enzymes in negatively regulating ABA-induced senescence. Contrary to the rapid transcriptomic changes triggered by ABA, the reduction of H3K27me3 at these SAGs falls far behind the induction of their expression, indicating that PRC2-mediated H3K27me3 contributed to long-term damping of ABA-induced senescence to prevent an oversensitive response. The findings of this study may serve as a paradigm for a global understanding of the interplay between the rapid effects of a phytohormone such as ABA and the long-term effects of the epigenetic machinery in regulating plant senescence processes and environmental responses.

More than 80% of the wheat genome consists of transposable elements (TEs), which act as major drivers of wheat genome evolution. However, their contributions to the regulatory evolution of wheat adaptations remain largely unclear. Here, we created genome-binding maps for 53 transcription factors (TFs) underlying environmental responses by leveraging DAP-seq in Triticum urartu, together with epigenomic profiles. Most TF binding sites (TFBSs) located distally from genes are embedded in TEs, whose functional relevance is supported by purifying selection and active epigenomic features. About 24% of the non-TE TFBSs share significantly high sequence similarity with TE-embedded TFBSs. These non-TE TFBSs have almost no homologous sequences in non-Triticeae species and are potentially derived from Triticeae-specific TEs. The expansion of TE-derived TFBS linked to wheat-specific gene responses, suggesting TEs are an important driving force for regulatory innovations. Altogether, TEs have been significantly and continuously shaping regulatory networks related to wheat genome evolution and adaptation.

Wheat (Triticum aestivum) has a large allohexaploid genome. Subgenome-divergent regulation contributed to genome plasticity and the domestication of polyploid wheat. However, the specificity encoded in the wheat genome determining subgenome-divergent spatio-temporal regulation has been largely unexplored. The considerable size and complexity of the genome are major obstacles to dissecting the regulatory specificity. Here, we compared the epigenomes and transcriptomes from a large set of samples under diverse developmental and environmental conditions. Thousands of distal epigenetic regulatory elements (distal-epiREs) were specifically linked to their target promoters with coordinated epigenomic changes. We revealed that subgenome-divergent activity of homologous regulatory elements is affected by specific epigenetic signatures. Subgenome-divergent epiRE regulation of tissue specificity is associated with dynamic modulation of H3K27me3 mediated by Polycomb complex and demethylases. Furthermore, quantitative epigenomic approaches detected key stress responsive cis- and trans-acting factors validated by DNA Affinity Purification and sequencing, and demonstrated the coordinated interplay between epiRE sequence contexts, epigenetic factors, and transcription factors in regulating subgenome divergent transcriptional responses to external changes. Together, this study provides a wealth of resources for elucidating the epiRE regulomics and subgenome-divergent regulation in hexaploid wheat, and gives new clues for interpreting genetic and epigenetic interplay in regulating the benefits of polyploid wheat.

High‐throughput technology has become a powerful approach for routine plant research. Interpreting the biological significance of high‐throughput data has largely focused on the functional characterization of a large gene list or genomic loci that involves the following two aspects: the functions of the genes or loci and how they are regulated as a whole, i.e. searching for the upstream regulators. Traditional platforms for functional annotation largely help resolving the first issue. Addressing the second issue is essential for a global understanding of the regulatory mechanism, but is more challenging, and requires additional high‐throughput experimental evidence and a unified statistical framework for data‐mining. The rapid accumulation of ’omics data provides a large amount of experimental data. We here present Plant Regulomics, an interface that integrates 19 925 transcriptomic and epigenomic data sets and diverse sources of functional evidence (58 112 terms and 695 414 protein−protein interactions) from six plant species along with the orthologous genes from 56 whole‐genome sequenced plant species. All pair‐wise transcriptomic comparisons with biological significance within the same study were performed, and all epigenomic data were processed to genomic loci targeted by various factors. These data were well organized to gene modules and loci lists, which were further implemented into the same statistical framework. For any input gene list or genomic loci, Plant Regulomics retrieves the upstream factors, treatments, and experimental/environmental conditions regulating the input from the integrated ’omics data. Additionally, multiple tools and an interactive visualization are available through a user‐friendly web interface. Plant Regulomics is available at http://bioinfo.sibs.ac.cn/plant-regulomics.

Review history (DOCX 1422 kb)

Formulae and definitions of the selected JIP-test fluorescence parameters used in this study. (DOCX 38 kb)

Background Recent studies have shown that C4-like photosynthetic pathways partly reside in photosynthetic cells surrounding the vascular system of C3 dicots. However, it is still unclear whether this is the case in C3 monocots, especially at the molecular level. Results In order to fill this gap, we investigated several characteristics required for C4 photosynthesis, including C4 pathway enzymes, cyclic/non-cyclic photophosphorylation rates, the levels and assembly state of photosynthetic machineries, in the mid-veins of C3 monocots rice with leaf laminae used as controls. The signature of photosystem photochemistry was also recorded via non-invasive chlorophyll a fluorescence and reflectance changes at 820 nm in vivo. Our results showed that rice mid-veins were photosynthetically active with higher levels of three C4 decarboxylases. Meanwhile, the linear electron transport chain was blocked in mid-veins due to the selective loss of dysfunctional photosystem II subunits. However, photosystem I was sufficient to support cyclic electron flow in mid-veins, reminiscent of the bundle sheath in C4 plants. Conclusions The photosynthetic attributes required for C4 photosynthesis were identified for the first time in the monocotyledon model crop rice, suggesting that this is likely a general innate characteristic of C3 plants which might be preconditioned for the C4 pathway evolution. Understanding these attributes would provide a base for improved strategies for engineering C4 photosynthetic pathways into rice. Electronic supplementary material The online version of this article (doi:10.1186/s12284-016-0094-5) contains supplementary material, which is available to authorized users.

Genetic diversity in plants is remarkably high. Recent whole genome sequencing (WGS) of 67 rice accessions recovered 10,872 novel genes. Comparison of the genetic architecture among divergent populations or between crops and wild relatives is essential for obtaining functional components determining crucial traits. However, many major crops have gigabase-scale genomes, which are not well-suited to WGS. Existing cost-effective sequencing approaches including re-sequencing, exome-sequencing and restriction enzyme-based methods all have difficulty in obtaining long novel genomic sequences from highly divergent population with large genome size. The present study presented a reference-independent core genome targeted sequencing approach, CGT-seq, which employed epigenomic information from both active and repressive epigenetic marks to guide the assembly of the core genome mainly composed of promoter and intragenic regions. This method was relatively easily implemented, and displayed high sensitivity and specificity for capturing the core genome of bread wheat. 95% intragenic and 89% promoter region from wheat were covered by CGT-seq read. We further demonstrated in rice that CGT-seq captured hundreds of novel genes and regulatory sequences from a previously unsequenced ecotype. Together, with specific enrichment and sequencing of regions within and nearby genes, CGT-seq is a time- and resource-effective approach to profiling functionally relevant regions in sequenced and non-sequenced populations with large genomes.