Plant Environmental Responses Research Articles

Organ-specific characteristics govern the relationship between histone code dynamics and transcriptional reprogramming during nitrogen response in tomato

Environmental stimuli trigger rapid transcriptional reprogramming of gene networks. These responses occur in the context of the local chromatin landscape, but the contribution of organ-specific dynamic chromatin modifications in responses to external signals remains largely unexplored. We treated tomato seedlings with a supply of nitrate and measured the genome-wide changes of four histone marks, the permissive marks H3K27ac, H3K4me3, and H3K36me3 and repressive mark H3K27me3, in shoots and roots separately, as well as H3K9me2 in shoots. Dynamic and organ-specific histone acetylation and methylation were observed at functionally relevant gene loci. Integration of transcriptomic and epigenomic datasets generated from the same organ revealed largely syngenetic relations between changes in transcript levels and histone modifications, with the exception of H3K27me3 in shoots, where an increased level of this repressive mark is observed at genes activated by nitrate. Application of a machine learning approach revealed organ-specific rules regarding the importance of individual histone marks, as H3K36me3 is the most successful mark in predicting gene regulation events in shoots, while H3K4me3 is the strongest individual predictor in roots. Our integrated study substantiates a view that during plant environmental responses, the relationships between histone code dynamics and gene regulation are highly dependent on organ-specific contexts.

A global LC-MS2 -based methodology to identify and quantify anionic phospholipids in plant samples.

Anionic phospholipids (PS, PA, PI, PIPs) are low-abundant phospholipids with impactful functions in cell signaling, membrane trafficking and cell differentiation processes. They can be quickly metabolized and can transiently accumulate at defined spots within the cell or an organ to respond to physiological or environmental stimuli. As even a small change in their composition profile will produce a significant effect on biological processes, it is crucial to develop a sensitive and optimized analytical method to accurately detect and quantify them. While thin-layer chromatography (TLC) separation coupled with gas chromatography (GC) detection methods already exist, they do not allow for precise, sensitive, and accurate quantification of all anionic phospholipid species. Here we developed a method based on high-performance liquid chromatography (HPLC) combined with two-dimensional mass spectrometry (MS2 ) by MRM mode to detect and quantify all molecular species and classes of anionic phospholipids in one shot. This method is based on a derivatization step by methylation that greatly enhances the ionization, the separation of each peak, the peak resolution as well as the limit of detection and quantification for each individual molecular species, and more particularly for PA and PS. Our method universally works in various plant samples. Remarkably, we identified that PS is enriched with very long chain fatty acids in the roots but not in aerial organs of Arabidopsis thaliana. Our work thus paves the way for new studies on how the composition of anionic lipids is finely tuned during plant development and environmental responses.

Low phosphorus promotes NSP1–NSP2 heterodimerization to enhance strigolactone biosynthesis and regulate shoot and root architecture in rice

Phosphorus is an essential macronutrient for plant development and metabolism, and plants have evolved ingenious mechanisms to overcome phosphate (Pi) starvation. However, the molecular mechanisms underlying the regulation of shoot and root architecture by low phosphorus conditions and the coordinated utilization of Pi and nitrogen remain largely unclear. Here, we show that Nodulation Signaling Pathway 1 (NSP1) and NSP2 regulate rice tiller number by promoting the biosynthesis of strigolactones (SLs), a class of phytohormones with fundamental effects on plant architecture and environmental responses. We found that NSP1 and NSP2 are induced by Oryza sativa PHOSPHATE STARVATION RESPONSE2 (OsPHR2) in response to low-Pi stress and form a complex to directly bind the promoters of SL biosynthesis genes, thus markedly increasing SL biosynthesis in rice. Interestingly, the NSP1/2–SL signaling module represses the expression of CROWN ROOTLESS 1 (CRL1), a newly identified early SL-responsive gene in roots, to restrain lateral root density under Pi deficiency. We also demonstrated that GR244DO treatment under normal conditions inhibits the expression of OsNRTs and OsAMTs to suppress nitrogen absorption but enhances the expression of OsPTs to promote Pi absorption, thus facilitating the balance between nitrogen and phosphorus uptake in rice. Importantly, we found that NSP1p:NSP1 and NSP2p:NSP2 transgenic plants show improved agronomic traits and grain yield under low- and medium-phosphorus conditions. Taken together, these results revealed a novel regulatory mechanism of SL biosynthesis and signaling in response to Pi starvation, providing genetic resources for improving plant architecture and nutrient-use efficiency in low-Pi environments.

Genome-Wide Identification and Analysis of Catharanthus roseus Receptor-like Kinase 1-like Proteins in Eggplant.

As an important member of the plant receptor-like kinases, Catharanthus roseus receptor-like kinase 1-like (CrRLK1L) plays vital roles in plant growth and development, as well as biotic and abiotic stress response. Numerous CrRLK1Ls have been identified and analyzed in various plant species, while our knowledge about eggplant (Solanum melongena L.) CrRLK1Ls is still scarce. Utilizing state-of-the-art genomic data, we conducted the first genome-wide identification and analysis of CrRLK1L proteins in eggplant. In this study, 32 CrRLK1L proteins were identified and analyzed in eggplant. A subsequent gene structure and protein domain analysis showed that the identified eggplant CrRLK1Ls possessed typical features of CrRLK1Ls. A subcellular localization prediction demonstrated that these proteins mostly localized on the plasma membrane. A collinearity analysis showed that some eggplant CrRLK1L genes had predicted intraspecies or interspecies evolutionary duplication events. Promoter analysis suggests that eggplant CrRLK1Ls may be involved in plant hormone signaling, host-pathogen interactions, and environmental responses. Based on transcriptomic gene expression analysis, it is indicated that eggplant CrRLK1Ls may be involved in the resistance response of eggplant to Botrytis cinerea. Together, these results will give us a theoretical foundation and guidance for elaborating the biological functions of CrRLK1Ls in eggplant growth, development, and resistance response.

The plant noncoding transcriptome: a versatile environmental sensor.

Plant noncoding RNA transcripts have gained increasing attention in recent years due to growing evidence that they can regulate developmental plasticity. In this review article, we comprehensively analyze the relationship between noncoding RNA transcripts in plants and their response to environmental cues. We first provide an overview of the various noncoding transcript types, including long and small RNAs, and how the environment modulates their performance. We then highlight the importance of noncoding RNA secondary structure for their molecular and biological functions. Finally, we discuss recent studies that have unveiled the functional significance of specific long noncoding transcripts and their molecular partners within ribonucleoprotein complexes during development and in response to biotic and abiotic stress. Overall, this review sheds light on the fascinating and complex relationship between dynamic noncoding transcription and plant environmental responses, and highlights the need for further research to uncover the underlying molecular mechanisms and exploit the potential of noncoding transcripts for crop resilience in the context of global warming.

Highly sex specific gene expression in Jojoba

BackgroundDioecious plants have male and female flowers on separate plants. Jojoba is a dioecious plant that is drought-tolerant and native to arid areas. The genome sequence of male and female plants was recently reported and revealed an X and Y chromosome system, with two large male-specific insertions in the Y chromosome.ResultsA total of 16,923 differentially expressed genes (DEG) were identified between the flowers of the male and female jojoba plants. This represented 40% of the annotated genes in the genome. Many genes, including those responsible for plant environmental responses and those encoding transcription factors (TFs), were specific to male or female reproductive organs. Genes involved in plant hormone metabolism were also found to be associated with flower and pollen development. A total of 8938 up-regulated and 7985 down-regulated genes were identified in comparison between male and female flowers, including many novel genes specific to the jojoba plant. The most differentially expressed genes were associated with reproductive organ development. The highest number of DEG were linked with the Y chromosome in male plants. The male specific parts of the Y chromosome encoded 12 very highly expressed genes including 9 novel genes and 3 known genes associated with TFs and a plant hormone which may play an important role in flower development.ConclusionMany genes, largely with unknown functions, may explain the sexual dimorphisms in jojoba plants and the differentiation of male and female flowers.

Transcriptome Analysis Reveals Long Non-Coding RNAs Involved in Shade-Induced Growth Promotion in Pinellia ternata.

High temperature and drought environments are important limiting factors for Pinellia ternata growth, whereas shading can promote growth by relieving these stresses. However, the mechanism of growth promotion by shading in P. ternata is unknown. Long non-coding RNAs (lncRNAs) play important roles in the plant's growth and environmental response, but few analyses of lncRNAs in P. ternata have been reported. We performed lncRNAs analysis of P. ternata in response to shading using RNA-seq data from our previous studies. A total of 13,927 lncRNAs were identified, and 145 differentially expressed lncRNAs (DELs) were obtained from the comparisons of 5 days shade (D5S) vs. 5 days of natural light (D5CK), 20 days of shade (D20S) vs. 20 days of natural light (D20CK), D20S vs. D5S, and D20CK vs. D5CK. Of these, 119 DELs (82.07%) were generated from the D20S vs. D20CK comparison. Gene ontology (GO) analysis indicated that the reactive oxygen (ROS) metabolism and programmed cell death (PCD) processes might regulate shade-induced growth promotion. The "signal transduction" and "environmental adaptation" in the Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis were used for lncRNA-mRNA regulatory network construction and showed that the lncRNAs might mediate P. ternata growth by regulating ROS accumulation and light signals. This study explores lncRNAs' functions and regulatory mechanisms related to P. ternata growth and lays a foundation for further research on P. ternata.

What, where, and how: Regulation of translation and the translational landscape in plants.

Translation is a crucial step in gene expression and plays a vital role in regulating various aspects of plant development and environmental responses. It is a dynamic and complex program that involves interactions between mRNAs, transfer RNAs, and the ribosome machinery through both cis- and trans-regulation while integrating internal and external signals. Translational control can act in a global (transcriptome-wide) or mRNA-specific manner. Recent advances in genome-wide techniques, particularly ribosome profiling and proteomics, have led to numerous exciting discoveries in both global and mRNA-specific translation. In this review, we aim to provide a "primer" that introduces readers to this fascinating yet complex cellular process and provide a big picture of how essential components connect within the network. We begin with an overview of mRNA translation, followed by a discussion of the experimental approaches and recent findings in the field, focusing on unannotated translation events and translational control through cis-regulatory elements on mRNAs and trans-acting factors, as well as signaling networks through 3 conserved translational regulators TOR, SnRK1, and GCN2. Finally, we briefly touch on the spatial regulation of mRNAs in translational control. Here, we focus on cytosolic mRNAs; translation in organelles and viruses is not covered in this review.

Unraveling the Pomegranate Genome: Comprehensive Analysis of R2R3-MYB Transcription Factors

R2R3-MYB TFs represent one of the most extensive gene families in plants and play a crucial role in regulating plant development, metabolite accumulation, and defense responses. Nevertheless, there has been no systematic investigation into the pomegranate R2R3-MYB family. In this study, 186 R2R3-MYB genes were identified from the pomegranate genome and grouped into 34 subgroups based on phylogenetic analysis. Gene structure analysis showed that the PgR2R3-MYB family in the same subgroup had a similar structure. Gene duplication event analysis revealed that the amplification of the PgMYB family was driven by Whole Genome Duplication (WGD) and dispersed duplication. In the upstream promoter sequence of the PgMYB gene, we identified a large number of plant hormones and environmental response elements. Using phylogenetic analysis and RNA-seq analysis, we identified three PgMYB TFs that may be involved in the regulation of lignin synthesis. Their expression patterns were verified by qPCR experiments. This study provides a solid foundation for further studies on the function of the R2R3-MYB gene and the molecular mechanism of lignin synthesis.

Golgi-localized MORN1 promotes lipid droplet abundance and enhances tolerance to multiple stresses in Arabidopsis.

Lipid droplet (LD) in vegetative tissues has recently been implicated in environmental responses in plants, but its regulation and its function in stress tolerance are not well understood. Here, we identified a Membrane Occupation and Recognition Nexus 1 (MORN1) gene as a contributor to natural variations of stress tolerance through genome-wide association study in Arabidopsis thaliana. Characterization of its loss-of-function mutant and natural variants revealed that the MORN1 gene is a positive regulator of plant growth, disease resistance, cold tolerance, and heat tolerance. The MORN1 protein is associated with the Golgi and is also partly associated with LD. Protein truncations that disrupt these associations abolished the biological function of the MORN1 protein. Furthermore, the MORN1 gene is a positive regulator of LD abundance, and its role in LD number regulation and stress tolerance is highly linked. Therefore, this study identifies MORN1 as a positive regulator of LD abundance and a contributor to natural variations of stress tolerance. It implicates a potential involvement of Golgi in LD biogenesis and strongly suggests a contribution of LD to diverse processes of plant growth and stress responses.

Long-read direct RNA sequencing reveals epigenetic regulation of chimeric gene-transposon transcripts in Arabidopsis thaliana

Transposable elements (TEs) are accumulated in both intergenic and intragenic regions in plant genomes. Intragenic TEs often act as regulatory elements of associated genes and are also co-transcribed with genes, generating chimeric TE-gene transcripts. Despite the potential impact on mRNA regulation and gene function, the prevalence and transcriptional regulation of TE-gene transcripts are poorly understood. By long-read direct RNA sequencing and a dedicated bioinformatics pipeline, ParasiTE, we investigated the transcription and RNA processing of TE-gene transcripts in Arabidopsis thaliana. We identified a global production of TE-gene transcripts in thousands of A. thaliana gene loci, with TE sequences often being associated with alternative transcription start sites or transcription termination sites. The epigenetic state of intragenic TEs affects RNAPII elongation and usage of alternative poly(A) signals within TE sequences, regulating alternative TE-gene isoform production. Co-transcription and inclusion of TE-derived sequences into gene transcripts impact regulation of RNA stability and environmental responses of some loci. Our study provides insights into TE-gene interactions that contributes to mRNA regulation, transcriptome diversity, and environmental responses in plants.

Transcriptomic analysis reveals the functions of H2S as a gasotransmitter independently of Cys in Arabidopsis.

Numerous studies have revealed the gasotransmitter functions of hydrogen sulfide (H2S) in various biological processes. However, the involvement of H2S in sulfur metabolism and/or Cys synthesis makes its role as a signaling molecule ambiguous. The generation of endogenous H2S in plants is closely related to the metabolism of Cys, which play roles in a variety of signaling pathway occurring in various cellular processes. Here, we found that exogenous H2S fumigation and Cys treatment modulated the production rate and content of endogenous H2S and Cys to various degrees. Furthermore, we provided comprehensive transcriptomic analysis to support the gasotransmitter role of H2S besides as a substrate for Cys synthesis. Comparison of the differentially expressed genes (DEGs) between H2S and Cys treated seedlings indicated that H2S fumigation and Cys treatment caused different influences on gene profiles during seedlings development. A total of 261 genes were identified to respond to H2S fumigation, among which 72 genes were co-regulated by Cys treatment. GO and KEGG enrichment analysis of the 189 genes, H2S but not Cys regulated DEGs, indicated that these genes mainly involved in plant hormone signal transduction, plant-pathogen interaction, phenylpropanoid biosynthesis, and MAPK signaling pathway. Most of these genes encoded proteins having DNA binding and transcription factor activities that play roles in a variety of plant developmental and environmental responses. Many stress-responsive genes and some Ca2+ signal associated genes were also included. Consequently, H2S regulated gene expression through its role as a gasotransmitter, rather than just as a substrate for Cys biogenesis, and these 189 genes were far more likely to function in H2S signal transduction independently of Cys. Our data will provide insights for revealing and enriching H2S signaling networks.

Genome-Wide Analysis of WRKY Transcription Factors Involved in Abiotic Stress and ABA Response in Caragana korshinskii.

The WRKY transcription factor family plays a vital role in plant development and environmental response. However, the information of WRKY genes at the genome-wide level is rarely reported in Caragana korshinskii. In this study, we identified and renamed 86 CkWRKY genes, which were further classified into three groups through phylogenetic analysis. Most of these WRKY genes were clustered and distributed on eight chromosomes. Multiple sequence alignment revealed that the conserved domain (WRKYGQK) of the CkWRKYs was basically consistent, but there were also six variation types (WRKYGKK, GRKYGQK, WRMYGQK, WRKYGHK, WKKYEEK and RRKYGQK) that appeared. The motif composition of the CkWRKYs was quite conservative in each group. In general, the number of WRKY genes gradually increased from lower to higher plant species in the evolutionary analysis of 28 species, with some exceptions. Transcriptomics data and RT-qPCR analysis showed that the CkWRKYs in different groups were involved in abiotic stresses and ABA response. Our results provided a basis for the functional characterization of the CkWRKYs involved in stress resistance in C. korshinskii.

Role of F-box E3-ubiquitin ligases in plant development and stress responses.

F-box E3-ubiquitin ligases regulate critical biological processes in plant development and stress responses. Future research could elucidate why and how plants have acquired a large number of F-box genes. The ubiquitin-proteasome system (UPS) is a predominant regulatory mechanism employed by plants to maintain the protein turnover in the cells and involves the interplay of three classes of enzymes, E1 (ubiquitin-activating), E2 (ubiquitin-conjugating), and E3 ligases. The diverse and most prominent protein family among eukaryotes, F-box proteins, are a vital component of the multi-subunit SCF (Skp1-Cullin 1-F-box) complex among E3 ligases. Several F-box proteins with multifarious functions in different plant systems have evolved rapidly over time within closely related species, but only a small part has been characterized. We need to advance our understanding of substrate-recognition regulation and the involvement of F-box proteins in biological processes and environmental adaptation. This review presents a background of E3 ligases with particular emphasis on the F-box proteins, their structural assembly, and their mechanism of action during substrate recognition. We discuss how the F-box proteins regulate and participate in the signaling mechanisms of plant development and environmental responses. We highlight an urgent need for research on the molecular basis of the F-box E3-ubiquitin ligases in plant physiology, systems biology, and biotechnology. Further, the developments and outlooks of the potential technologies targeting the E3-ubiquitin ligases for developing crop improvement strategies have been discussed.

Chemical screening approach using single leaves identifies compounds that affect cold signaling in Arabidopsis.

The identification of chemical compounds that affect intracellular processes has greatly contributed to our understanding of plant growth and development. In most cases, these compounds have been identified in germinated seedlings. However, chemical screening using mature plants would benefit and advance our understanding of environmental responses. In this study, we developed a high-throughput screening method using single leaves of mature plants to identify small molecules that affect cold-regulated gene expression. A single excised leaf of Arabidopsis (Arabidopsis thaliana) grown in submerged cultures responded to low temperatures in terms of COLD-REGULATED (COR) gene expression. We used transgenic Arabidopsis harboring a COLD-REGULATED 15A (COR15A) promoter::luciferase (COR15Apro::LUC) construct to screen natural compounds that affect the cold induction of COR15Apro::LUC. This approach allowed us to identify derivatives of 1,4-naphthoquinone as specific inhibitors of COR gene expression. Moreover, 1,4-naphthoquinones appeared to inhibit the rapid induction of upstream C-REPEAT BINDING FACTOR (CBF) transcription factors upon exposure to low temperature, suggesting that 1,4-naphthoquinones alter upstream signaling processes. Our study offers a chemical screening scheme for identifying compounds that affect environmental responses in mature plants. This type of analysis is likely to reveal an unprecedented link between certain compounds and plant environmental responses.

Plant Small RNAs: Their Biogenesis, Regulatory Roles, and Functions.

Plant cells accumulate small RNA molecules that regulate plant development, genome stability, and environmental responses. These small RNAs fall into three major classes based on their function and mechanisms of biogenesis-microRNAs, heterochromatic small interfering RNAs, and secondary small interfering RNAs-plus several other less well-characterized categories. Biogenesis of each small RNA class requires a pathway of factors, some specific to each pathway and others involved in multiple pathways. Diverse sequenced plant genomes, along with rapid developments in sequencing, imaging, and genetic transformation techniques, have enabled significant progress in understanding the biogenesis, functions, and evolution of plant small RNAs, including those that had been poorly characterized because they were absent or had low representation in Arabidopsis (Arabidopsis thaliana). Here, we review recent findings about plant small RNAs and discuss our current understanding of their biogenesis mechanisms, targets, modes of action, mobility, and functions in Arabidopsis and other plant species, including economically important crops.

Coupling epigenetics and RNA polyadenylation: missing links.

Precise regulation of gene expression is crucial for plant survival. As a cotranscriptional regulatory mechanism, pre-mRNA polyadenylation is essential for fine-tuning gene expression. Polyadenylation can be alternatively projected at various sites of a transcript, which contributes to transcriptome diversity. Epigenetic modification is another mechanism of transcriptional control. Recent studies have uncovered crosstalk between cotranscriptional polyadenylation processes and both epigenomic and epitranscriptomic markers. Genetic analyses have demonstrated that DNA methylation, histone modifications, and epitranscriptomic modification are involved in regulating polyadenylation in plants. Here we summarize current understanding of the links between epigenetics and polyadenylation and their novel biological efficacy for plant development and environmental responses. Unresolved issues and future directions are discussed to shed light on the field.

The Arabidopsis thaliana trehalose-6-phosphate phosphatase gene AtTPPI regulates primary root growth and lateral root elongation.

Roots are the main organs through which plants absorb water and nutrients. As the key phytohormone involved in root growth, auxin functions in plant environmental responses by modulating auxin synthesis, distribution and polar transport. The Arabidopsis thaliana trehalose-6-phosphate phosphatase gene AtTPPI can improve root architecture, and tppi1 mutants have significantly shortened primary roots. However, the mechanism underlying the short roots of the tppi1 mutant and the upstream signaling pathway and downstream genes regulated by AtTPPI are unclear. Here, we demonstrated that the AtTPPI gene could promote auxin accumulation in AtTPPI-overexpressing plants. By comparing the transcriptomic data of tppi1 and wild-type roots, we found several upregulations of auxin-related genes, including GH3.3, GH3.9 and GH3.12, may play an important role in the AtTPPI gene-mediated auxin transport signaling pathway, ultimately leading to changes in auxin content and primary root length. Moreover, increased AtTPPI expression can regulate primary root growth and lateral root elongation under different concentration of nitrate conditions. Overall, constitutive expression of AtTPPI increased auxin contents and improved lateral root elongation, constituting a new method for improving the nitrogen utilization efficiency of plants.

Cis-Regulatory Elements in Plant Development, Adaptation, and Evolution.

cis-Regulatory elements encode the genomic blueprints that ensure the proper spatiotemporal patterning of gene expression necessary for appropriate development and responses to the environment. Accumulating evidence implicates changes to gene expression as a major source of phenotypic novelty in eukaryotes, including acute phenotypes such as disease and cancer in mammals. Moreover, genetic and epigenetic variation affecting cis-regulatory sequences over longer evolutionary timescales has become a recurring theme in studies of morphological divergence and local adaptation. Here, we discuss the functions of and methods used to identify various classes of cis-regulatory elements, as well as their role in plant development and response to the environment. We highlight opportunities to exploit cis-regulatory variants underlying plant development and environmental responses for crop improvement efforts. Although a comprehensive understanding of cis-regulatory mechanisms in plants has lagged behind that in animals, we showcase several breakthrough findings that have profoundly influenced plant biology and shaped the overall understanding of transcriptional regulation in eukaryotes.

Epigenetic modifications: Allusive clues of lncRNA functions in plants

Long non-coding RNAs (lncRNAs) have been verified as flexible and important factors in various biological processes of multicellular eukaryotes, including plants. The respective intricate crosstalk among multiple epigenetic modifications has been examined to some extent. However, only a small proportion of lncRNAs has been functionally well characterized. Moreover, the relationship between lncRNAs and other epigenetic modifications has not been systematically studied. In this mini-review, we briefly summarize the representative biological functions of lncRNAs in developmental programs and environmental responses in plants. In addition, we particularly discuss the intimate relationship between lncRNAs and other epigenetic modifications, and we outline the underlying avenues and challenges for future research on plant lncRNAs.