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DOE OSTI2022

ADAR activation by inducing a syn conformation at guanosine adjacent to an editing site

Abstract ADARs (adenosine deaminases acting on RNA) can be directed to sites in the transcriptome by complementary guide strands allowing for the correction of disease-causing mutations at the RNA level. However, ADARs show bias against editing adenosines with a guanosine 5′ nearest neighbor (5′-GA sites), limiting the scope of this approach. Earlier studies suggested this effect arises from a clash in the RNA minor groove involving the 2-amino group of the guanosine adjacent to an editing site. Here we show that nucleosides capable of pairing with guanosine in a syn conformation enhance editing for 5′-GA sites. We describe the crystal structure of a fragment of human ADAR2 bound to RNA bearing a G:G pair adjacent to an editing site. The two guanosines form a Gsyn:Ganti pair solving the steric problem by flipping the 2-amino group of the guanosine adjacent to the editing site into the major groove. Also, duplexes with 2′-deoxyadenosine and 3-deaza-2′-deoxyadenosine displayed increased editing efficiency, suggesting the formation of a Gsyn:AH+anti pair. This was supported by X-ray crystallography of an ADAR complex with RNA bearing a G:3-deaza dA pair. This study shows how non-Watson–Crick pairing in duplex RNA can facilitate ADAR editing enabling the design of next generation guide strands for therapeutic RNA editing.

Doherty, Erin E.↗

DOE OSTI2023

TroR is the primary regulator of the iron homeostasis transcription network in the halophilic archaeon Haloferax volcanii

Abstract Maintaining the intracellular iron concentration within the homeostatic range is vital to meet cellular metabolic needs and reduce oxidative stress. Previous research revealed that the haloarchaeon Halobacterium salinarum encodes four diphtheria toxin repressor (DtxR) family transcription factors (TFs) that together regulate the iron response through an interconnected transcriptional regulatory network (TRN). However, the conservation of the TRN and the metal specificity of DtxR TFs remained poorly understood. Here we identified and characterized the TRN of Haloferax volcanii for comparison. Genetic analysis demonstrated that Hfx. volcanii relies on three DtxR transcriptional regulators (Idr, SirR, and TroR), with TroR as the primary regulator of iron homeostasis. Bioinformatics and molecular approaches revealed that TroR binds a conserved cis-regulatory motif located ∼100 nt upstream of the start codon of iron-related target genes. Transcriptomics analysis demonstrated that, under conditions of iron sufficiency, TroR repressed iron uptake and induced iron storage mechanisms. TroR repressed the expression of one other DtxR TF, Idr. This reduced DtxR TRN complexity relative to that of Hbt. salinarum appeared correlated with natural variations in iron availability. Based on these data, we hypothesize that variable environmental conditions such as iron availability appear to select for increasing TRN complexity.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Altering translation allows E. coli to overcome G-quadruplex stabilizers

G-quadruplex (G4) structures can form in guanine-rich DNA or RNA and have been found to modulate cellular processes, including replication, transcription, and translation. Many studies on the cellular roles of G4s have focused on eukaryotic systems, with far fewer probing bacterial G4s. Using a chemical-genetic approach, we identified genes in Escherichia coli that are important for growth in G4-stabilizing conditions. Reducing levels of translation elongation factor Tu or slowing translation initiation or elongation with kasugamycin, chloramphenicol, or spectinomycin suppress the effects of G4-stabilizing compounds. In contrast, reducing the expression of specific translation termination or ribosome recycling proteins is detrimental to growth in G4-stabilizing conditions. Proteomic and transcriptomic analyses reveal decreased protein and transcript levels, respectively, for ribosome assembly factors and proteins associated with translation in the presence of G4 stabilizer. Our results support a model in which reducing the rate of translation by altering translation initiation, translation elongation, or ribosome assembly can compensate for G4-related stress in E. coli.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2011

Gcn4 misregulation reveals a direct role for the evolutionary conserved $\mathrm{EKC/KEOPS}$ in the t 6 A modification of t$\mathrm{RNA}$s

The EKC/KEOPS complex is universally conserved in Archaea and Eukarya and has been implicated in several cellular processes, including transcription, telomere homeostasis and genomic instability. However, the molecular function of the complex has remained elusive so far. We analyzed the transcriptome of EKC/KEOPS mutants and observed a specific profile that is highly enriched in targets of the Gcn4p transcriptional activator. GCN4 expression was found to be activated at the translational level in mutants via the defective recognition of the inhibitory upstream ORFs (uORFs) present in its leader. We show that EKC/KEOPS mutants are defective for the N6-threonylcarbamoyl adenosine modification at position 37 (t 6 A 37 ) of tRNAs decoding ANN codons, which affects initiation at the inhibitory uORFs and provokes Gcn4 de-repression. Structural modeling reveals similarities between Kae1 and bacterial enzymes involved in carbamoylation reactions analogous to t 6 A 37 formation, supporting a direct role for the EKC in tRNA modification. These findings are further supported by strong genetic interactions of EKC mutants with a translation initiation factor and with threonine biosynthesis genes. Overall, our data provide a novel twist to understanding the primary function of the EKC/KEOPS and its impact on several essential cellular functions like transcription and telomere homeostasis.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2012

Global transcriptional control by glucose and carbon regulator CcpA in Clostridium difficile

The catabolite control protein CcpA is a pleiotropic regulator that mediates the global transcriptional response to rapidly catabolizable carbohydrates, like glucose in Gram-positive bacteria. By whole transcriptome analyses, we characterized glucose-dependent and CcpA-dependent gene regulation in Clostridium difficile . About 18% of all C. difficile genes are regulated by glucose, for which 50% depend on CcpA for regulation. The CcpA regulon comprises genes involved in sugar uptake, fermentation and amino acids metabolism, confirming the role of CcpA as a link between carbon and nitrogen pathways. Using combination of chromatin immunoprecipitation and genome sequence analysis, we detected 55 CcpA binding sites corresponding to ~140 genes directly controlled by CcpA. We defined the C. difficile CcpA consensus binding site ( cre CD motif), that is, ‘RRGAAAANGTTTTCWW’. Binding of purified CcpA protein to 19 target cre CD sites was demonstrated by electrophoretic mobility shift assay. CcpA also directly represses key factors in early steps of sporulation (Spo0A and SigF). Furthermore, the C. difficile toxin genes ( tcdA and tcdB ) and their regulators ( tcdR and tcdC ) are direct CcpA targets. Finally, CcpA controls a complex and extended regulatory network through the modulation of a large set of regulators.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2014

A dynamic alternative splicing program regulates gene expression during terminal erythropoiesis

Alternative pre-messenger RNA splicing remodels the human transcriptome in a spatiotemporal manner during normal development and differentiation. Here we explored the landscape of transcript diversity in the erythroid lineage by RNA-seq analysis of five highly purified populations of morphologically distinct human erythroblasts, representing the last four cell divisions before enucleation. In this unique differentiation system, we found evidence of an extensive and dynamic alternative splicing program encompassing genes with many diverse functions. Alternative splicing was particularly enriched in genes controlling cell cycle, organelle organization, chromatin function and RNA processing. Many alternative exons exhibited differentiation-associated switches in splicing efficiency, mostly in late-stage polychromatophilic and orthochromatophilic erythroblasts, in concert with extensive cellular remodeling that precedes enucleation. A subset of alternative splicing switches introduces premature translation termination codons into selected transcripts in a differentiation stage-specific manner, supporting the hypothesis that alternative splicing-coupled nonsense-mediated decay contributes to regulation of erythroid-expressed genes as a novel part of the overall differentiation program. We conclude that a highly dynamic alternative splicing program in terminally differentiating erythroblasts plays a major role in regulating gene expression to ensure synthesis of appropriate proteome at each stage as the cells remodel in preparation for production of mature red cells.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2013

Two RNA-binding motifs in eIF3 direct HCV IRES-dependent translation

The initiation of protein synthesis plays an essential regulatory role in human biology. At the center of the initiation pathway, the 13-subunit eukaryotic translation initiation factor 3 (eIF3) controls access of other initiation factors and mRNA to the ribosome by unknown mechanisms. Using electron microscopy (EM), bioinformatics and biochemical experiments, we identify two highly conserved RNA-binding motifs in eIF3 that direct translation initiation from the hepatitis C virus internal ribosome entry site (HCV IRES) RNA. Mutations in the RNA-binding motif of subunit eIF3a weaken eIF3 binding to the HCV IRES and the 40S ribosomal subunit, thereby suppressing eIF2-dependent recognition of the start codon. Mutations in the eIF3c RNA-binding motif also reduce 40S ribosomal subunit binding to eIF3, and inhibit eIF5B-dependent steps downstream of start codon recognition. These results provide the first connection between the structure of the central translation initiation factor eIF3 and recognition of the HCV genomic RNA start codon, molecular interactions that likely extend to the human transcriptome.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2013

Soybean knowledge base (SoyKB): a web resource for integration of soybean translational genomics and molecular breeding

Soybean Knowledge Base (http://soykb.org) is a comprehensive web resource developed for bridging soybean translational genomics and molecular breeding research. It provides information for six entities including genes/proteins, microRNAs/sRNAs, metabolites, single nucleotide polymorphisms, plant introduction lines and traits. It also incorporates many multi-omics datasets including transcriptomics, proteomics, metabolomics and molecular breeding data, such as quantitative trait loci, traits and germplasm information. Soybean Knowledge Base has a new suite of tools such as In Silico Breeding Program for soybean breeding, which includes a graphical chromosome visualizer for ease of navigation. It integrates quantitative trait loci, traits and germplasm information along with genomic variation data, such as single nucleotide polymorphisms, insertions, deletions and genome-wide association studies data, from multiple soybean cultivars and Glycine soja.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

Identification and functional analysis of strigolactone pathway genes regulating tillering traits in sugarcane

Abstract Saccharum officinarum and Saccharum spontaneum are two fundamental species of modern sugarcane cultivars, exhibiting divergent tillering patterns crucial for sugarcane architecture and yield. Strigolactones (SLs), a class of plant hormones, are considered to play a central role in shaping plant form and regulating tillering. Our study highlights the distinct tillering patterns observed between S. officinarum and S. spontaneum and implicates significant differences in SL levels in root exudates between the two species. Treatment with rac-GR24 (an artificial SL analog) suppressed tillering in S. spontaneum. Based on transcriptome analysis, we focused on two genes, TRANSCRIPTION ELONGATION FACTOR 1 (TEF1) and CIRCADIAN CLOCK ASSOCIATED1 (CCA1), which show higher expression in S. spontaneum or S. officinarum, respectively. While the overexpression of SoCCA1 did not lead to significant phenotypic differences, overexpression of SsTEF1 in rice stimulated tillering and inhibited plant height, demonstrating its role in tillering regulation. However, the overexpression of suggests that SoCCA1 may not be the key regulator of sugarcane tillering. Yeast one-hybrid assays identified four transcription factors (TFs) regulating SsTEF1 and four and five TFs regulating SsCCA1 and SoCCA1. This study provides a theoretical foundation for deciphering the molecular mechanisms underlying the different tillering behaviors between S. officinarum and S. spontaneum, providing valuable insights for the molecular-based design of sugarcane breeding strategies.

Qi, Yiying↗

DOE OSTI2021

Single-cell RNA sequencing of batch Chlamydomonas cultures reveals heterogeneity in their diurnal cycle phase

The photosynthetic unicellular alga Chlamydomonas (Chlamydomonas reinhardtii) is a versatile reference for algal biology because of its ease of culture in the laboratory. Genomic and systems biology approaches have previously described transcriptome responses to environmental changes using bulk data, thus representing the average behavior from pools of cells. Here, we apply single-cell RNA sequencing (scRNA-seq) to probe the heterogeneity of Chlamydomonas cell populations under three environments and in two genotypes differing by the presence of a cell wall. First, we determined that RNA can be extracted from single algal cells with or without a cell wall, offering the possibility to sample natural algal communities. Second, scRNA-seq successfully separated single cells into nonoverlapping cell clusters according to their growth conditions. Cells exposed to iron or nitrogen deficiency were easily distinguished despite a shared tendency to arrest photosynthesis and cell division to economize resources. Notably, these groups of cells not only recapitulated known patterns observed with bulk RNA-seq but also revealed their inherent heterogeneity. A substantial source of variation between cells originated from their endogenous diurnal phase, although cultures were grown in constant light. We exploited this result to show that circadian iron responses may be conserved from algae to land plants. We document experimentally that bulk RNA-seq data represent an average of typically hidden heterogeneity in the population.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

The N-terminal domains of NLR immune receptors exhibit structural and functional similarities across divergent plant lineages

Nucleotide-binding domain and leucine-rich repeat (NLR) proteins are a prominent class of intracellular immune receptors in plants. However, our understanding of plant NLR structure and function is limited to the evolutionarily young flowering plant clade. Here, we describe an extended spectrum of NLR diversity across divergent plant lineages and demonstrate the structural and functional similarities of N-terminal domains that trigger immune responses. We show that the broadly distributed coiled-coil (CC) and toll/interleukin-1 receptor (TIR) domain families of nonflowering plants retain immune-related functions through translineage activation of cell death in the angiosperm Nicotiana benthamiana. We further examined a CC subfamily specific to nonflowering lineages and uncovered an essential N-terminal MAEPL motif that is functionally comparable with motifs in resistosome-forming CC-NLRs. Consistent with a conserved role in immunity, the ectopic activation of CC MAEPL in the nonflowering liverwort Marchantia polymorpha led to profound growth inhibition, defense gene activation, and signatures of cell death. Moreover, comparative transcriptomic analyses of CC MAEPL activity delineated a common CC-mediated immune program shared across evolutionarily divergent nonflowering and flowering plants. Collectively, our findings highlight the ancestral nature of NLR-mediated immunity during plant evolution that dates its origin to at least ~500 million years ago.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

The DYRKP1 kinase regulates cell wall degradation in Chlamydomonas by inducing matrix metalloproteinase expression

Abstract The cell wall of plants and algae is an important cell structure that protects cells from changes in the external physical and chemical environment. This extracellular matrix, composed of polysaccharides and glycoproteins, must be constantly remodeled throughout the life cycle. However, compared to matrix polysaccharides, little is known about the mechanisms regulating the formation and degradation of matrix glycoproteins. We report here that a plant kinase belonging to the dual-specificity tyrosine phosphorylation-regulated kinase (DYRKP1) family present in all eukaryotes regulates cell wall degradation after mitosis of Chlamydomonas reinhardtii by inducing the expression of matrix metalloproteinases. Without DYRKP1, daughter cells cannot disassemble parental cell walls and remain trapped inside for more than 10 days. On the other hand, the dual-specificity tyrosine phosphorylation-regulated kinase complementation lines show normal degradation of the parental cell wall. Transcriptomic and proteomic analyses indicate a marked downregulation of MMP gene expression and accumulation, respectively, in the dyrkp1 mutants. The mutants deficient in matrix metalloproteinases retain palmelloid structures for a longer time than the background strain, like dyrkp1 mutants. Our findings show that dual-specificity tyrosine phosphorylation-regulated kinase, by ensuring timely MMP expression, enables the successful execution of the cell cycle. Altogether, this study provides insight into the life cycle regulation in plants and algae.

Kim, Minjae (ORCID:0000000223561295)↗

DOE OSTI2025

Too dim, too bright, and just right: Systems analysis of the Chlamydomonas diurnal program under limiting and excess light

Photosynthetic organisms coordinate their metabolism and growth with diurnal light, which can range in intensity from limiting to excessive. Little is known about how light intensity impacts the diurnal program in Chlamydomonas reinhardtii, or how diurnal rhythms in gene expression and metabolism shape photoprotective responses at different times of day. To address these questions, we performed a systems analysis of synchronized Chlamydomonas populations acclimated to low, moderate, and high diurnal light. Transcriptomic and proteomic data revealed that the Chlamydomonas rhythmic gene expression program is resilient to limiting and excess light: genome-wide, waves of transcripts, and proteins peak at the same times in populations acclimated to stressful light intensities as in populations acclimated to moderate light. Yet, diurnal photoacclimation gives rise to hundreds of gene expression changes, even at night. Time course measurements of photosynthetic efficiency and pigments responsive to excess light showed that high light-acclimated cells partially overcome photodamage in the latter half of the day prior to cell division. Although gene expression and photodamage are dynamic over the diurnal cycle, Chlamydomonas populations acclimated to low and high diurnal light maintain altered photosystem abundance, thylakoid architecture, and non-photochemical quenching capacity through the night phase. This suggests that cells remember or anticipate the light intensities that they have typically encountered during the day. The integrated data constitute an excellent resource for understanding photoacclimation in eukaryotes under environmentally relevant conditions.

Dupuis, Sunnyjoy↗

DOE OSTI2026

Gene and genome duplications have contrasting impacts on biosynthetic and flower developmental pathways in California poppy

Benzylisoquinoline alkaloids (BIAs) represent a vast group of specialized plant metabolites with diverse pharmaceutical applications, synthesized by a variety of gene families. Among the multiple plant lineages that produce BIAs, the most notable is the poppy family (Papaveraceae), with California poppy (Eschscholzia californica) emerging as a model organism. Here, we report a haplotype-resolved genome assembly, in combination with a high-density expression atlas, for California poppy. Genome analyses reveal recent diversification of BIA biosynthesis genes in poppy through localized duplications. Furthermore, we demonstrate that the degree of phylogenetic relatedness among paralogs within BIA biosynthesis-associated gene families correlates with similarities in gene expression. In contrast, gene families involved in carotenoid biosynthesis, which contributes to the intense orange petal pigmentation, are not phylogenetically clustered, and floral developmental regulators exhibit a high degree of retention of gene duplicates associated with ancient polyploidy events. These findings illustrate alternative roles for gene and genome duplications as drivers of trait evolution. Given the position of California poppy in the angiosperm phylogeny, the high-quality genomic resources generated for this work constitute a valuable resource for comparative genomic and transcriptomic analyses for poppies and flowering plants more generally.

Rössner, Le-Han [Justus-Liebig University, Giessen↗

DOE OSTI2021

Machine learning-enabled phenotyping for GWAS and TWAS of WUE traits in 869 field-grown sorghum accessions

Abstract Sorghum (Sorghum bicolor) is a model C4 crop made experimentally tractable by extensive genomic and genetic resources. Biomass sorghum is studied as a feedstock for biofuel and forage. Mechanistic modeling suggests that reducing stomatal conductance (gs) could improve sorghum intrinsic water use efficiency (iWUE) and biomass production. Phenotyping to discover genotype-to-phenotype associations remains a bottleneck in understanding the mechanistic basis for natural variation in gs and iWUE. This study addressed multiple methodological limitations. Optical tomography and a machine learning tool were combined to measure stomatal density (SD). This was combined with rapid measurements of leaf photosynthetic gas exchange and specific leaf area (SLA). These traits were the subject of genome-wide association study and transcriptome-wide association study across 869 field-grown biomass sorghum accessions. The ratio of intracellular to ambient CO2 was genetically correlated with SD, SLA, gs, and biomass production. Plasticity in SD and SLA was interrelated with each other and with productivity across wet and dry growing seasons. Moderate-to-high heritability of traits studied across the large mapping population validated associations between DNA sequence variation or RNA transcript abundance and trait variation. A total of 394 unique genes underpinning variation in WUE-related traits are described with higher confidence because they were identified in multiple independent tests. This list was enriched in genes whose Arabidopsis (Arabidopsis thaliana) putative orthologs have functions related to stomatal or leaf development and leaf gas exchange, as well as genes with nonsynonymous/missense variants. These advances in methodology and knowledge will facilitate improving C4 crop WUE.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2021

Phenotyping stomatal closure by thermal imaging for GWAS and TWAS of water use efficiency-related genes

Abstract Stomata allow CO2 uptake by leaves for photosynthetic assimilation at the cost of water vapor loss to the atmosphere. The opening and closing of stomata in response to fluctuations in light intensity regulate CO2 and water fluxes and are essential for maintaining water-use efficiency (WUE). However, a little is known about the genetic basis for natural variation in stomatal movement, especially in C4 crops. This is partly because the stomatal response to a change in light intensity is difficult to measure at the scale required for association studies. Here, we used high-throughput thermal imaging to bypass the phenotyping bottleneck and assess 10 traits describing stomatal conductance (gs) before, during and after a stepwise decrease in light intensity for a diversity panel of 659 sorghum (Sorghum bicolor) accessions. Results from thermal imaging significantly correlated with photosynthetic gas exchange measurements. gs traits varied substantially across the population and were moderately heritable (h2 up to 0.72). An integrated genome-wide and transcriptome-wide association study identified candidate genes putatively driving variation in stomatal conductance traits. Of the 239 unique candidate genes identified with the greatest confidence, 77 were putative orthologs of Arabidopsis (Arabidopsis thaliana) genes related to functions implicated in WUE, including stomatal opening/closing (24 genes), stomatal/epidermal cell development (35 genes), leaf/vasculature development (12 genes), or chlorophyll metabolism/photosynthesis (8 genes). These findings demonstrate an approach to finding genotype-to-phenotype relationships for a challenging trait as well as candidate genes for further investigation of the genetic basis of WUE in a model C4 grass for bioenergy, food, and forage production.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2022

Transcript and metabolite network perturbations in lignin biosynthetic mutants of Arabidopsis

Abstract Lignin, one of the most abundant polymers in plants, is derived from the phenylpropanoid pathway, which also gives rise to an array of metabolites that are essential for plant fitness. Genetic engineering of lignification can cause drastic changes in transcription and metabolite accumulation with or without an accompanying development phenotype. To understand the impact of lignin perturbation, we analyzed transcriptome and metabolite data from the rapidly lignifying stem tissue in 13 selected phenylpropanoid mutants and wild-type Arabidopsis (Arabidopsis thaliana). Our dataset contains 20,974 expressed genes, of which over 26% had altered transcript levels in at least one mutant, and 18 targeted metabolites, all of which displayed altered accumulation in at least one mutant. We found that lignin biosynthesis and phenylalanine supply via the shikimate pathway are tightly co-regulated at the transcriptional level. The hierarchical clustering analysis of differentially expressed genes (DEGs) grouped the 13 mutants into 5 subgroups with similar profiles of mis-regulated genes. Functional analysis of the DEGs in these mutants and correlation between gene expression and metabolite accumulation revealed system-wide effects on transcripts involved in multiple biological processes.

Plant Sciences↗

DOE OSTI2024

A maize semi-dwarf mutant reveals a GRAS transcription factor involved in brassinosteroid signaling

Brassinosteroids (BR) and gibberellins (GA) regulate plant height and leaf angle in maize (Zea mays). Mutants with defects in BR or GA biosynthesis or signaling identify components of these pathways and enhance our knowledge about plant growth and development. In this study, we characterized three recessive mutant alleles of GRAS transcription factor 42 (gras42) in maize, a GRAS transcription factor gene orthologous to the DWARF AND LOW TILLERING (DLT) gene of rice (Oryza sativa). These maize mutants exhibited semi-dwarf stature, shorter and wider leaves, and more upright leaf angle. Transcriptome analysis revealed a role for GRAS42 as a determinant of BR signaling. Analysis of the expression consequences from loss of GRAS42 in the gras42-mu1021149 mutant indicated a weak loss of BR signaling in the mutant, consistent with its previously demonstrated role in BR signaling in rice. Loss of BR signaling was also evident by the enhancement of weak BR biosynthetic mutant alleles in double mutants of nana plant1-1 and gras42-mu1021149. The gras42-mu1021149 mutant had little effect on GA-regulated gene expression, suggesting that GRAS42 is not a regulator of core GA signaling genes in maize. Single-cell expression data identified gras42 expressed among cells in the G2/M phase of the cell cycle consistent with its previously demonstrated role in cell cycle gene expression in Arabidopsis (Arabidopsis thaliana). Cis-acting natural variation controlling GRAS42 transcript accumulation was identified by expression genome-wide association study (eGWAS) in maize. Our results demonstrate a conserved role for GRAS42/SCARECROW-LIKE 28 (SCL28)/DLT in BR signaling, clarify the role of this gene in GA signaling, and suggest mechanisms of tillering and leaf angle control by BR.

54 ENVIRONMENTAL SCIENCES↗