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Salinity-induced accumulation of certain microRNAs accompanied by gaseous phytohormone ethylene production has been recognized as a mechanism of plant salt tolerance. MicroRNA319 (miR319) has been characterized as an important player in abiotic stress resistance in some C3 plants, such as Arabidopsis thaliana and rice. However, its role in the dedicated biomass plant switchgrass (Panicum virgatum L.), a C4 plant, has not been reported. Here, we show crosstalk between miR319 and ethylene (ET) for increasing salt tolerance. By overexpressing Osa-MIR319b and a target mimicry form of miR319 (MIM319), we showed that miR319 positively regulated ET synthesis and salt tolerance in switchgrass. By experimental treatments, we demonstrated that ET-mediated salt tolerance in switchgrass was dose-dependent, and miR319 regulated the switchgrass salt response by fine-tuning ET synthesis. Further experiments showed that the repression of a miR319 target, PvPCF5, in switchgrass also led to enhanced ethylene accumulation and salt tolerance in transgenic plants. Genome-wide transcriptome analysis demonstrated that overexpression of miR319 (OE-miR319) down-regulated the expression of key genes in the methionine (Met) cycle but promoted the expression of genes in ethylene synthesis. The results enrich our understanding of the synergistic effects of the miR319-PvPCF5 module and ethylene synthesis in the salt tolerance of switchgrass, a C4 bioenergy plant.
Salt stress limits the productivity of crops grown under saline conditions, leading to substantial losses of yield in saline soils and under brackish and saline irrigation. Salt tolerant crops could alleviate these losses while both increasing irrigation opportunities and reducing agricultural demands on dwindling freshwater resources. However, despite significant efforts, progress towards this goal has been limited, largely because of the genetic complexity of salt tolerance for agronomically important yield-related traits. Consequently, the focus is shifting to the study of traits that contribute to overall tolerance, thus breaking down salt tolerance into components that are more genetically tractable. Greater consideration of the plasticity of salt tolerance mechanisms throughout development and across environmental conditions furthers this dissection. The demand for more sophisticated and comprehensive methodologies is being met by parallel advances in high-throughput phenotyping and sequencing technologies that are enabling the multivariate characterisation of vast germplasm resources. Alongside steady improvements in statistical genetics models, forward genetics approaches for elucidating salt tolerance mechanisms are gaining momentum. Subsequent quantitative trait locus and gene validation has also become more accessible, most recently through advanced techniques in molecular biology and genomic analysis, facilitating the translation of findings to the field. Besides fuelling the improvement of established crop species, this progress also facilitates the domestication of naturally salt tolerant orphan crops. Taken together, these advances herald a promising era of discovery for research into the genetics of salt tolerance in plants.
Salt is harmful to crop production. Therefore, it is important to understand the mechanism of salt tolerance in rice. CIPK genes have various functions, including regulating salt tolerance and other types of stress and nitrogen use efficiency. In rice, OsCIPK24 is known to regulate salt tolerance, but other OsCIPKs could also function in salt tolerance. In this study, we identified another OsCIPK-OsCIPK9-that can regulate salt tolerance. Knockout of OsCIPK9 in rice could improve salt tolerance. Through expression analyses, OsCIPK9 was found to be mainly expressed in the roots and less expressed in mature leaves. Meanwhile, OsCIPK9 had the highest expression 6 h after salt treatment. In addition, we proved the interaction between OsCIPK9 and OsSOS3. The RNA-seq data showed that OsCIPK9 strongly responded to salt treatment, and the transporters related to salt tolerance may be downstream genes of OsCIPK9. Finally, haplotype analyses revealed that Hap6 and Hap8 mainly exist in indica, potentially providing a higher salt tolerance. Overall, a negative regulator of salt tolerance, OsCIPK9, which interacted with OsSOS3 similarly to OsCIPK24 and influenced salt-related transporters, was identified, and editing OsCIPK9 potentially could be helpful for breeding salt-tolerant rice.
Salt stress is a major constraint on plant growth and yield. Nitrogen (N) fertilizers are known to alleviate salt stress. However, the underlying molecular mechanisms remain unclear. Here, we show that nitrate-dependent salt tolerance is mediated by OsMADS27 in rice. The expression of OsMADS27 is specifically induced by nitrate. The salt-inducible expression of OsMADS27 is also nitrate dependent. OsMADS27 knockout mutants are more sensitive to salt stress than the wild type, whereas OsMADS27 overexpression lines are more tolerant. Transcriptomic analyses revealed that OsMADS27 upregulates the expression of a number of known stress-responsive genes as well as those involved in ion homeostasis and antioxidation. We demonstrate that OsMADS27 directly binds to the promoters of OsHKT1.1 and OsSPL7 to regulate their expression. Notably, OsMADS27-mediated salt tolerance is nitrate dependent and positively correlated with nitrate concentration. Our results reveal the role of nitrate-responsive OsMADS27 and its downstream target genes in salt tolerance, providing a molecular mechanism for the enhancement of salt tolerance by nitrogen fertilizers in rice. OsMADS27 overexpression increased grain yield under salt stress in the presence of sufficient nitrate, suggesting that OsMADS27 is a promising candidate for the improvement of salt tolerance in rice.
Salt stress causes significant reductions in rice production worldwide; thus, improving salt tolerance is a promising approach to meet the increasing food demand. Wild rice germplasm is considered a valuable genetic resource for improving rice cultivars. However, information regarding the improvement of salt tolerance in cultivated rice using wild rice genes is limited. In this study, we identified a salt-tolerant line Dongxiang/Ningjing 15 (DJ15) under salt-stress field conditions from the population of a salt tolerant Dongxiang wild rice × a cultivated rice variety Ningjing16 (NJ16). Genomic resequencing analysis of NJ16, DJ15 and Dongxiang wild rice revealed that the introgressed genomic fragments were unevenly distributed over the 12 chromosomes (Chr.) and mainly identified on Chr. 6, 7, 10, and 11. Using quantitative trait locus (QTL) mapping, we found 9 QTL for salt tolerance (qST) at the seedling stage located on Chr. 1, 3, 4, 5, 6, 8, and 10. In addition, sequence variant analysis within the QTL regions demonstrated that SKC1/HKT8/HKT1;5 and HAK6 transporters along with numerous transcriptional factors were the candidate genes for the salt tolerant QTL. The DJ15/Koshihikari recombinant inbred lines that contained both qST1.2 and qST6, two QTL with the highest effect for salt tolerance, were more tolerant than the parental lines under salt-stress field conditions. Furthermore, the qST6 near-isogenic lines with IR29 background were more tolerant than IR29, indicating that qST1.2 and qST6 could improve salt tolerance in rice. Overall, our study indicates that wild rice genes could markedly improve the salt tolerance of cultivated rice.
Soil salinization is an increasingly serious threat that limits plant growth and development. Class I transporters of the high-affinity K⁺ transporter (HKT) family have been demonstrated to be involved in salt tolerance by contributing to Na⁺ exclusion from roots and shoots. Here, we isolated the PeHKT1;1 gene from hybrid poplar based on the sequences of the Populus trichocarpa genome. The full-length PeHKT1;1 gene was 2173 bp, including a 1608 bp open reading frame (ORF) encoding 535 amino acids and containing eight distinct transmembrane domains. Multiple sequence alignment and phylogenetic analysis suggested that the PeHKT1;1 protein had a typical S⁻G⁻G⁻G signature for the P-loop domains and belonged to class I of HKT transporters. PeHKT1;1 transcripts were mainly detected in stem and root, and were remarkably induced by salt stress treatment. In further characterization of its functions, overexpression of PeHKT1;1 in Populus davidiana × Populus bolleana resulted in a better relative growth rate in phenotypic analysis, including root and plant height, and exhibited higher catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD) activities than non-transgenic poplar under salt stress conditions. These observations indicated that PeHKT1;1 may enhance salt tolerance by improving the efficiency of antioxidant systems. Together, these data suggest that PeHKT1;1 plays an important role in response to salt stress in Populus.
Ethylene biosynthesis and the ethylene signaling pathway regulate plant salt tolerance by activating the expression of downstream target genes such as those related to ROS and Na+/K+ homeostasis. The Salt Overly Sensitive (SOS) pathway regulates Na+/K+ homeostasis in Arabidopsis under salt stress. However, the connection between these two pathways is unclear. Through genetic screening, we identified two sos2 alleles as salt sensitive mutants in the ein3-1 background. Neither Ethylene-Insensitive 2 (EIN2) nor EIN3 changed the expression patterns of SOS genes including SOS1, SOS2, SOS3 and SOS3-like Calcium Binding Protein 8 (SCaBP8), but SOS2 activated the expression of one target gene of EIN3, Ethylene and Salt-inducible ERF 1 (ESE1). Moreover, Ser/Thr protein kinase SOS2 phosphorylated EIN3 in vitro mainly at the S325 site and weakly at the S35, T42 and S606 sites. EIN3 S325A mutation reduced its transcriptional activating activity on ESE1 promoter:GUS in a transient GUS assay, and impaired its ability to rescue ein3-1 salt hypersensitivity. Furthermore, SOS2 activated salt-responsive ESE1 target gene expression under salt stress. Therefore, EIN3-SOS2 might link the ethylene signaling pathway and the SOS pathway in Arabidopsis salt responses.
The WRKY transcription factor superfamily is known to participate in plant growth and stress response. However, the role of this family in wheat (Triticum aestivum L.) is largely unknown. Here, a salt-induced gene TaWRKY13 was identified in an RNA-Seq data set from salt-treated wheat. The results of RT-qPCR analysis showed that TaWRKY13 was significantly induced in NaCl-treated wheat and reached an expression level of about 22-fold of the untreated wheat. Then, a further functional identification was performed in both Arabidopsis thaliana and Oryza sativa L. Subcellular localization analysis indicated that TaWRKY13 is a nuclear-localized protein. Moreover, various stress-related regulatory elements were predicted in the promoter. Expression pattern analysis revealed that TaWRKY13 can also be induced by polyethylene glycol (PEG), exogenous abscisic acid (ABA), and cold stress. After NaCl treatment, overexpressed Arabidopsis lines of TaWRKY13 have a longer root and a larger root surface area than the control (Columbia-0). Furthermore, TaWRKY13 overexpression rice lines exhibited salt tolerance compared with the control, as evidenced by increased proline (Pro) and decreased malondialdehyde (MDA) contents under salt treatment. The roots of overexpression lines were also more developed. These results demonstrate that TaWRKY13 plays a positive role in salt stress.
Salt stress is one of the key abiotic stresses that causes great loss of yield and serious decrease in quality in maize (Zea mays L.). Therefore, it is very important to reveal the molecular mechanism of salt tolerance in maize. To acknowledge the molecular mechanisms underlying maize salt tolerance, two maize inbred lines, including salt-tolerant 8723 and salt-sensitive P138, were used in this study. Comparative proteomics of seedling roots from two maize inbred lines under 180 mM salt stress for 10 days were performed by the isobaric tags for relative and absolute quantitation (iTRAQ) approach. A total of 1056 differentially expressed proteins (DEPs) were identified. In total, 626 DEPs were identified in line 8723 under salt stress, among them, 378 up-regulated and 248 down-regulated. There were 473 DEPs identified in P138, of which 212 were up-regulated and 261 were down-regulated. Venn diagram analysis showed that 17 DEPs were up-regulated and 12 DEPs were down-regulated in the two inbred lines. In addition, 8 DEPs were up-regulated in line 8723 but down-regulated in P138, 6 DEPs were down-regulated in line 8723 but up-regulated in P138. In salt-stressed 8723, the DEPs were primarily associated with phenylpropanoid biosynthesis, starch and sucrose metabolism, and the mitogen-activated protein kinase (MAPK) signaling pathway. Intriguingly, the DEPs were only associated with the nitrogen metabolism pathway in P138. Compared to P138, the root response to salt stress in 8723 could maintain stronger water retention capacity, osmotic regulation ability, synergistic effects of antioxidant enzymes, energy supply capacity, signal transduction, ammonia detoxification ability, lipid metabolism, and nucleic acid synthesis. Based on the proteome sequencing information, changes of 8 DEPs abundance were related to the corresponding mRNA levels by quantitative real-time PCR (qRT-PCR). Our results from this study may elucidate some details of salt tolerance mechanisms and salt tolerance breeding of maize.
Plants have evolved various strategies to sense and respond to saline environments, which severely reduce plant growth and limit agricultural productivity. Alteration to the cell wall is one strategy that helps plants adapt to salt stress. However, the physiological mechanism of how the cell wall components respond to salt stress is not fully understood. Here, we show that expression of XTH30, encoding xyloglucan endotransglucosylase-hydrolase30, is strongly up-regulated in response to salt stress in Arabidopsis. Loss-of-function of XTH30 leads to increased salt tolerance and overexpression of XTH30 results in salt hypersensitivity. XTH30 is located in the plasma membrane and is highly expressed in the root, flower, stem, and etiolated hypocotyl. The NaCl-induced increase in xyloglucan (XyG)-derived oligosaccharide (XLFG) of the wild type is partly blocked in xth30 mutants. Loss-of-function of XTH30 slows down the decrease of crystalline cellulose content and the depolymerization of microtubules caused by salt stress. Moreover, lower Na+ accumulation in shoot and lower H2O2 content are found in xth30 mutants in response to salt stress. Taken together, these results indicate that XTH30 modulates XyG side chains, altered abundance of XLFG, cellulose synthesis, and cortical microtubule stability, and negatively affecting salt tolerance.
Apple trees are often subject to severe salt stress in China as well as in the world that results in significant loss of apple production. Therefore this study was carried out to evaluate the response of apple seedlings inoculated with abuscular mycorrhizal fungi under 0, 2‰, 4‰ and 6‰ salinity stress levels and further to conclude the upper threshold of mycorrhizal salinity tolerance.
Soil salinity is a major abiotic stress, limiting lentil productivity worldwide. Understanding the genetic basis of salt tolerance is vital to develop tolerant varieties. A diversity panel consisting of 276 lentil accessions was screened in a previous study through traditional and image-based approaches to quantify growth under salt stress. Genotyping was performed using two contrasting methods, targeted (tGBS) and transcriptome (GBS-t) genotyping-by-sequencing, to evaluate the most appropriate methodology. tGBS revealed the highest number of single-base variants (SNPs) (c. 56,349), and markers were more evenly distributed across the genome compared to GBS-t. A genome-wide association study (GWAS) was conducted using a mixed linear model. Significant marker-trait associations were observed on Chromosome 2 as well as Chromosome 4, and a range of candidate genes was identified from the reference genome, the most plausible being potassium transporters, which are known to be involved in salt tolerance in related species. Detailed mineral composition performed on salt-treated and control plant tissues revealed the salt tolerance mechanism in lentil, in which tolerant accessions do not transport Na+ ions around the plant instead localize within the root tissues. The pedigree analysis identified two parental accessions that could have been the key sources of tolerance in this dataset.
Isocitrate lyase (ICL) is a key enzyme in the glyoxylate cycle. In a previous study in rice, the expression of the ICL-encoding gene (OsICL) was highly induced by salt stress and its expression was enhanced in transgenic rice lines overexpressing OsCam1-1, a calmodulin (CaM)-encoding gene. CaM has been implicated in salt tolerance mechanisms in plants; however, the cellular mechanisms mediated by CaM are not clearly understood. In this study, the role of OsICL in plant salt tolerance mechanisms and the possible involvement of CaM were investigated using transgenic plants expressing OsICL or OsCam1-1.
Protein kinases are major signal transduction factors that have a central role in mediating acclimation to environmental changes in eukaryotic organisms. In this study, we cloned and identified three salt overly sensitive 2 (SOS2) genes in the woody plant Populus trichocarpa, designated as PtSOS2.1, PtSOS2.2, and PtSOS2.3, which were transformed into hybrid poplar clone T89 (Populus tremula× Populus tremuloides Michx clone T89) mediated by Agrobacterium tumefaciens. Southern and northern blot analyses verified that the three genes integrated into the plant genome, and were expressed at a stable transcription level. Meanwhile, overexpression of all three PtSOS2 genes did not retard the growth of plants under normal conditions. Instead, it promoted growth in both agar-medium and soil conditions in response to salinity stress. Under salt stress, overexpression of PtSOS2.1, PtSOS2.2, and PtSOS2.3 increased the concentrations of proline and photosynthetic pigments, and the relative water content (RWC), and the activity of antioxidant enzymes, and decreased the malondialdehyde (MDA) concentrations in transgenic lines compared to the control. These results suggest that overexpression of PtSOS2 plays a significant role in improving the salt tolerance of poplars, reducing the damage to membrane structures, and enhancing osmotic adjustment and antioxidative enzyme regulation under salt stress.
Mesembryanthemum crystallinum (common ice plant) is a halophyte species that has adapted to extreme conditions. In this study, we cloned a McHB7 transcription factor gene from the ice plant. The expression of McHB7 was significantly induced by 500 mM NaCl and it reached the peak under salt treatment for 7 days. The McHB7 protein was targeted to the nucleus. McHB7-overexpressing in ice plant leaves through Agrobacterium-mediated transformation led to 25 times more McHB7 transcripts than the non-transformed wild type (WT). After 500 mM NaCl treatment for 7 days, the activities of superoxide dismutase (SOD) and peroxidase (POD) and water content of the transgenic plants were higher than the WT, while malondialdehyde (MDA) was decreased in the transgenic plants. A total of 1082 and 1072 proteins were profiled by proteomics under control and salt treatment, respectively, with 22 and 11 proteins uniquely identified under control and salt stress, respectively. Among the 11 proteins, 7 were increased and 4 were decreased after salt treatment. Most of the proteins whose expression increased in the McHB7 overexpression (OE) ice plants under high salinity were involved in transport regulation, catalytic activities, biosynthesis of secondary metabolites, and response to stimulus. The results demonstrate that the McHB7 transcription factor plays a positive role in improving plant salt tolerance.
The CONSTANS-LIKE (COL) transcription factor has been reported to play important roles in regulating plant flowering and the response to abiotic stress. To clone and screen COL genes with excellent salt tolerance from the woody halophyte Tamarix hispida, 8 ThCOL genes were identified in this study. The expression patterns of these genes under different abiotic stresses (high salt, osmotic, and heavy metal) and abscisic acid (ABA) treatment were detected using quantitative real-time PCR (qRT-PCR). The expression levels of 8 ThCOL genes changed significantly after exposure to one or more stresses, indicating that these genes were all stress-responsive genes and may be involved in the stress resistance response of T. hispida. In particular, the expression level of ThCOL2 changed significantly at most time points in the roots and leaves of T. hispida under salt stress and after ABA treatments, which may play an important role in the response process of salt stress through a mechanism dependent on the ABA pathway. The recombinant vectors pROKII-ThCOL2 and pFGC5941-ThCOL2 were constructed for the transient transformation of T. hispida, and the transient infection of T. hispida with the pROKII empty vector was used as the control to further verify whether the ThCOL2 gene was involved in the regulation of the salt tolerance response of T. hispida. Overexpression of the ThCOL2 gene in plants under 150 mM NaCl stress increased the ability of transgenic T. hispida cells to remove reactive oxygen species (ROS) by regulating the activity of protective enzymes and promoting a decrease in the accumulation of O2- and H2O2, thereby reducing cell damage or cell death and enhancing salt tolerance. The ThCOL2 gene may be a candidate gene associated with excellent salt tolerance. Furthermore, the expression levels of some genes related to the ABA pathway were analyzed using qRT-PCR. The results showed that the expressions of ThNCED1 and ThNCED4 were significantly higher, and the expressions of ThNCED3, ThZEP, and ThAAO3 were not significantly altered in OE compared with CON under normal conditions. But after 24 h of salt stress, the expressions of all five studied genes all were lower than the normal condition. In the future, the downstream genes directly regulated by the ThCOL2 transcription factor will be searched and identified to analyze the salt tolerance regulatory network of ThCOL2.
Soybean [Glycine max (L.) Merr.] is an important crop for oil and protein resources worldwide, and its farming is impacted by increasing soil salinity levels. In Arabidopsis the gene EARLY FLOWERING 3 (ELF3), increased salt tolerance by suppressing salt stress response pathways. J is the ortholog of AtELF3 in soybean, and loss-of-function J-alleles greatly prolong soybean maturity and enhance grain yield. The exact role of J in abiotic stress response in soybean, however, remains unclear. In this study, we showed that J expression was induced by NaCl treatment and that the J protein was located in the nucleus. Compared to NIL-J, tolerance to NaCl was significantly lower in the NIL-j mutant. We also demonstrated that overexpression of J increased NaCl tolerance in transgenic soybean hairy roots. J positively regulated expression of downstream salt stress response genes, including GmWRKY12, GmWRKY27, GmWRKY54, GmNAC, and GmSIN1. Our study disclosed a mechanism in soybean for regulation of the salt stress response. Manipulation of these genes should facilitate improvements in salt tolerance in soybean.
Salinity stress challenges agriculture and food security globally. Upon salt stress, plant growth slows down, nutrients are recycled, osmolytes are produced, and reallocation of Na+ takes place. Since autophagy is a high-throughput degradation pathway that contributes to nutrient remobilization in plants, we explored the involvement of autophagic flux in salt stress response of Arabidopsis with various approaches. Confocal microscopy of GFP-ATG8a in transgenic Arabidopsis showed that autophagosome formation is induced shortly after salt treatment. Immunoblotting of ATG8s and the autophagy receptor NBR1 confirmed that the level of autophagy peaks within 30 min of salt stress, and then settles to a new homeostasis in Arabidopsis. Such an induction is absent in mutants defective in autophagy. Within 3 h of salt treatment, accumulation of oxidized proteins is alleviated in the wild-type; however, such a reduction is not seen in atg2 or atg7. Consistently, the Arabidopsis atg mutants are hypersensitive to both salt and osmotic stresses, and plants overexpressing ATG8 perform better than the wild-type in germination assays. Quantification of compatible osmolytes further confirmed that the autophagic flux contributes to salt stress adaptation. Imaging of intracellular Na+ revealed that autophagy is required for Na+ sequestration in the central vacuole of root cortex cells following salt treatment. These data suggest that rapid protein turnover through autophagy is a prerequisite for salt stress tolerance in Arabidopsis.
Soil salinity severely hampers agricultural productivity. Under salt stress, excess Na+ accumulation causes cellular damage and plant growth retardation, and membrane Na+ transporters play central roles in Na+ uptake and exclusion to mitigate these adverse effects. In this study, we performed sos1 suppressor mutant (named sup) screening to uncover potential genetic interactors of SOS1 and additional salt tolerance mechanisms. Map-based cloning and sequencing identified a group of mutants harboring dominant gain-of-function mutations in the vacuolar Na+/H+ antiporter gene AtNHX1. The gain-of-function variants of AtNHX1 showed enhanced transporter activities in yeast cells and increased salt tolerance in Arabidopsis wild type plants. Ion content measurements indicated that at the cellular level, these gain-of-function mutations resulted in increased cellular Na+ accumulation likely due to enhanced vacuolar Na+ sequestration. However, the gain-of-function suppressor mutants showed reduced shoot Na+ but increased root Na+ accumulation under salt stress, indicating a role of AtNHX1 in limiting Na+ translocation from root to shoot. We also identified another group of sos1 suppressors with loss-of-function mutations in the Na+ transporter gene AtHKT1. Loss-of-function mutations in AtHKT1 and gain-of-function mutations in AtNHX1 additively suppressed sos1 salt sensitivity, which indicates that the three transporters, SOS1, AtNHX1 and AtHKT1 function independently but coordinately in controlling Na+ homeostasis and salt tolerance in Arabidopsis. Our findings provide valuable information about the target amino acids in NHX1 for gene editing to improve salt tolerance in crops.
Salt stress is one of the major environmental threats to plant growth and development. However, the mechanisms of plants responding to salt stress are not fully understood. Through genetic screening, we identified and characterized a salt-sensitive mutant, ses5 (sensitive to salt 5), in Arabidopsis thaliana. Positional cloning revealed that the decreased salt-tolerance of ses5 was caused by a mutation in the transcription factor BP (BREVIPEDICELLUS). BP regulates various developmental processes in plants. However, the biological function of BP in abiotic stress-signaling and tolerance are still not clear. Compared with wild-type plants, the bp mutant exhibited a much shorter primary-root and lower survival rate under salt treatment, while the BP overexpressors were more tolerant. Further analysis showed that BP could directly bind to the promoter of XTH7 (xyloglucan endotransglucosylase/hydrolase 7) and activate its expression. Resembling the bp mutant, the disruption of XTH7 gave rise to salt sensitivity. These results uncovered novel roles of BP in positively modulating salt-stress tolerance, and illustrated a putative working mechanism.
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