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Evidence for an increase in cannabis use in Iran – A systematic review and trend analysis
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Official websites use. Share sensitive information only on official, secure websites. Cannabis sativa has a complex history reflected in both selection on naturally occurring compounds and historical trade routes among humans. Iran is a rich resource of natural populationswhich hold the promise to characterize historical patterns of population structure and genetic diversity within Cannabis. Recent advances in high-throughput DNA sequencing technologies have dramatically increased our ability to produce information to the point that it is now feasible to inexpensively obtain population level genotype information at a large scale. We genotyped 98 cannabis samples 36 from Iranian locations and 26 accessions from two germplasm collections. However, single nucleotide variant analysis uncovered a relatively moderate level of variation among Iranian cannabis. Cannabis sativa L. Humans have cultivated the plant as a source of fiber, food, medicines, intoxicants and oils for thousands of years 1 , 2. This use and breeding has led to the selection of two distinct types of C. While these types are morphologically similar, they are distinguished by the type and level of cannabinoids produced. Levels of two types of cannabinoids in particular are used to distinguish marijuana and hemp C. First, Dtetrahydrocannabinol THC is a psychoactive compound 3 found in leaves and inflorescences but not seeds of juvenile and mature plants. The second compound, cannabidiol CBD , is an isomer of THC found in all plant tissues, however, this cannabinoid does not activate cannabinoid receptors 1 , 4 , 5. Marijuana varieties used for drug consumption are characterized by a high THC content, whereas fibre varieties hemp produce CBD as the predominant cannabinoid 6 , 7. Archaeological and palaeobotanical evidence supports the cultivation and use of Cannabis since the Neolithic period with subsequent secondary domestication events in geographical regions outside of the accepted native range 8 — For instance, archaeological evidence for the pharmaceutical or shamanistic use of Cannabis has been found in cave artifacts that include a large cache of Cannabis dating to ca. This long history of use has resulted in a complex biogeographical history for this species. Based on polymorphism in RAPD markers, the Eurasian Steppe region of Central Asia has been recognized as a putative center of origin for Cannabis , spreading from there to the Mediterranean as well as Eastern and Central European countries, in particular, Afghanistan and Pakistan However, the genus has also been described has having two centers of diversity, Hindustani and European—Siberian As with other cultivated plants it is difficult to pinpoint the exact place of origin for C. It is likely that Cannabis spread to ancient Persia very early, assisted by Aryan and Scythian tribes expanding westward from central Asia. Evidence for this early spread comes from archeological studies of the Scythians, who occupied an area encompassing large swathes of what is now northwest Iran from the 7th century BCE to the 4th century CE, this culture was known to use Cannabis for entertainment and spiritual purposes. While all Iranian cannabis has been described as a complex of landraces of C. Currently, the most important topics in C. A draft genome and accompanying transcriptome of C. Nevertheless, the phylogeography and domestication history of Cannabis remains poorly understood, in part due to limited access to genetic material from natural populations. Given that Cannabis is a native plant with a long history of cultural use in Iran, it is surprising that no studies of Cannabis diversity using molecular markers exist. Here we present an initial description of population structure and genetic diversity, between Iranian and global collections of Cannabis as well as within the Iranian collection. Specifically, we leverage genotyping-by-sequencing GBS 32 to generate single nucleotide polymorphisms SNPs across a large collection of Iranian cannabis. GBS provides a robust, cost-effective alternative to other approaches and provide greater power to detect genome wide patterns associated with population structure and demographics than other molecular markers 33 , In total 98 cannabis samples were digested, sequenced, and genotyped these included, 70 samples representing 35 locations in Iran Fig. For each location or accession one female and male plant was sampled. After quality filtering a total The remaining samples were represented by a mean of 4. These uniquely mapped sequence reads covered approximately 0. Geographical distribution of samples across Iran. This figure was produced using the R software version 3. These differences may arise from differences in sequencing depth across regions, excessive amplification in the PCR step, short read length, or problems with the sequencing platform The number of markers ranged from 2. After quality filtering, 24, high-quality SNPs were identified across all samples and 29, SNPs were identified for 68 Iranian individuals, including one Afghanistan sample. The transition:transversion ratio was 1. The majority of SNPs The ratio of transitions to transversions is consistent with other studies in various species 36 — S2 and a mean of 0. This pattern is common among groups that experience heterozygote advantage, wherein rare alleles are retained at low frequencies. Average heterozygosity was estimated at 0. This estimate of heterozygosity is similar to that found by Sawler et al. Heterozygosity per location. Triangles represent male samples and circles represent female samples. Population differentiation resulting from genetic structure was estimated using F ST. Low values indicate that genetic diversity is higher within individuals from these locations than between locations, a pattern consistent with gene flow between populations. F ST estimates above 0 indicate a reduction in genetic exchange between population with a value of 1 indicating complete isolation. Across all individuals the maximum F ST , 0. CAN37 was previously described as hemp type and originating in France, however, Sawler et al. We also estimated genetic differentiation among marijuana and hemp accessions and Iranian samples and found a larger F ST across hemp 0. Similar to Sawler et al. Marijuana and Iranian cannabis clustered together with genetic distances of 0. Overall, these results suggest that Iranian collections are more genetically similar to marijuana collections than hemp. It is important to note that neither of the reference genomes used in this study were from a male plant. Our approach failed to identify sex specific alleles at high frequency outside of the sex determining region. Previous analyses have shown that marijuana and fibre types differ across the genome and not just at specific loci. Our approach failed to identify positions with significant deviations in allele frequency among 19, SNPs between types. Sawler et al. Our reanalysis of these data identified 9 SNPs with allele frequencies of 1 for hemp and 0 for marijuana and 92 SNPs with allele frequency 0 for hemp and 1 for marijuana. All positions and their frequencies are supplied in Table S3. An initial analysis of population structure was performed using individual-based principal component analysis PCA. This plot revealed two nonconforming individuals CANM and ArdF that failed to group with the two main clusters. Previous outliers from Sawler et al. Visualisation of DAPC results using the first 22 principal components clearly clusters, marijuana, hemp, germplasm collections, and Iranian collections Fig. Principle components analysis of 95 samples from Iranian collection, 43 hemp and 71 marijuana samples using 13, SNPs. Hemp samples are colored blue and marijuana samples are colored red. D stand for New Data and P. D stand for previously analyzed data. Discriminant analysis of principal components DAPC results. B Scatterplot based on the DAPC output for four assigned genetic clusters, each indicated by different colours. Dots represent different individuals. PCA within the Iranian collection identified two primary clusters Fig. This pattern is consistent with reduced gene flow from cluster 1 which includes 18 samples Fig. S4 , Table S5. According to these results we can define distinct genetic clusters for locations Neyriz, Piranshahr, Gahwareh, Arak, Urmia and Abhar. This pattern is consistent with perennial dioecious plants wherein the majority of variation is harbored within populations Together these suggest that Iranian cannabis populations tend to share more DNA with geographically proximate populations where may have genomes made up of mixtures of inferred source populations, while our simulation incorporated drift between locations, but not admixture. Individual-based principal components analysis for 35 Iranian regions and Afghanistan using 29, SNPs. Male plants are colored blue and female plants are colored red. Cannabis , both marijuana and fibre types, is a globally important plant, driving a multi-billion dollar industry. Unraveling the population genomic parameters of natural populations can help identify sources of genetic diversity, as well as describing patterns of domestication for this widely used plant. In this study, we have found that natural populations of Cannabis in Iran are more closely related to marijuana than hemp, and that these populations harbor unique pools of genetic diversity. Taken together these data support the hypothesis that reduced diversity across fibre types suggests that hemp cultivars are derived from marijuana Population analyses among all accessions sampled defined 4 distinct genetic clusters Figs 3 , 4 and 5. These analyses support previous findings Sawler et al. This evidence provides support for the hypothesis that Iranian cannabis harbors unique genetic diversity and may represent a distinct genetic lineage of marijuana. Heterozygosity indicates levels of genetic diversity within populations, and has also been used to estimate genetic distance between populations 49 , Consistent with genetic diversity levels in the present study, previous estimates of heterozygosity across diverse marker types e. However, it should be noted that one study found lower levels of heterozygosity in hemp varieties across samples and SNPs It has been suggested that this may result from limited hemp sample representation in the collection Heterozygosity estimates within our Iranian collection were similar to those found by Sawler et al. If, as we surmise, Iranian cannabis are marijuana accessions, then these accessions likely represent remnants of cultivated germplasm from the other regions, possibly through migration of Cannabis from neighboring countries like Afghanistan and Pakistan into Iran. These results demonstrate that Iran is a public repository of marijuana genetic diversity; however, the loss of this unique germplasm is of great concern as there are no breeding programs and growing Cannabis is associated with strict legal penalties. These observations reveal that Iranian cannabis, despite clear evidence of admixture likely the result of breeding , harbors distinguishable pools of genetic diversity. The lack of strong population differentiation is unsurprising since, all known cultivars of Cannabis are wind-pollinated and highly heterozygous confirmed by AMOVA, Table S6. Population structure is further complicated by the fact that marijuana cultivars are clonally propagated in order to retain high-levels of THC production. Intentionally growing Cannabis plants in Iran is punishable by prison sentence, populations of plants are more likely to have arisen from seed and therefore represent more natural populations. Although Iranian cannabis is not likely a subspecies it does represent a genetically unique variety of marijuana, and thus provides a novel source of genetic material for cultivar development. In plants, the sex determination system is important for two reasons; first, understanding the role of sex determination in shaping plant evolution, and second, diversity in the mechanisms through which sex is determined. There have been many studies on gender in Cannabis , including whether a plant should be classified as female or male, and in addition to the identification of sex chromosomes 21 , some male-specific DNA markers have been identified in C. Sex determination in Cannabis is a complex process and can be modified or reversed by environmental factors and chemical treatment 55 , Additionally, male flowers are able to develop on female plants under extreme conditions Because confirmed sex-associated DNA markers such as MADC2 sometimes fail to discriminate sex phenotype 22 , we attempted to identify sex associated markers from autosomal regions. While our study generated thousands of differentiating markers, we failed to find sex locus specific SNPs. This is likely because no male reference genome is available and the proportion of coding regions covered by the GBS derived SNPs. Future studies can capitalize on the utility of high-throughput sequencing technologies to look for markers associated with sex-determining loci, in particular coding derived SNPs e. We were able, however, to identify marijuana and fibre type specific markers through reanalysis of previously published data. Our conclusions, consistent with previous studies, show that genetic differences between hemp and marijuana accessions are widely distributed across the genome Comparative analysis of Purple Kush marijuana and Finola fibre genomes revealed highly discriminative SNPs that are distributed across the genome and are not restricted to particular loci e. In this study, we identified SNPs that appear to be tightly linked to type, and are outside of cannabinoid genes, which should prove useful for future research. More immediately, these markers can be validated for early and rapid identification of marijuana and fibre type plants for current breeding programs. Natural populations of Cannabis in Iran were identified and seeds were collected for growing in the field in university of Tehran. Sex identities were verified using taxonomic keys. Figure 1 was produced using the R software version 3. Additionally Dplyr version 0. DNA was extracted using a Qiagen DNeasy plant mini-kit, from leaf tissue of one female and one male plant from each location. We performed in silico digestion of the Cannabis genome sequence with Pst I and Apek I to select the best restriction enzyme library preparation. Libraries were prepared using the GBS protocol published by Sonah et al. High-throughput was performed on an Illumina Hiseq. After unzipping fastq. To elucidate the relationship of Iranian cannabis with marijuana and fibre type accessions, we merged our data with marijuana and hemp data prepared by Sawler et al. In a high-throughput genotyping workflow, alignment of short reads to a reference genome is the first step after read processing and filtering. BWA 62 was used to map reads of the individual genotypes to the reference genome with the default parameters. Reads mapped to Purple Kush canSat3: a special variety of hemp and Finola finola1: a special variety of marijuana C. The mapping outputs were used for removing unmapped reads to produce BAM files using Samtools 63 and only reads mapping to a unique location in the genome were retained. FreeBayes was run using default parameters. This was performed for or males and females and drug and non-drug types separately to find positions linked to gender and type. Bi-allelic, missingness, quality, and depth were filtered. Bi-allelic markers were identified by a command-line written in our lab. This package can filter each position for each individual. After screening a few markers we found that read depth and quality were not being appropriately filtered for our data set and therefore we opted to use vcflib. Finally, summary statistics were collected using vcf-stats before and after data filtering. Identification of DNA markers associated with gender and type was carried out based on comparison of SNP allele frequency differences between each group female-male and marijuana-fibre. To do this, we called SNPs for sample pairs female and male, marijuana and fibre, separately using FreeBayes We computed the fixation index F ST using VCFtools 66 among all wise locations in the Iranian collection and also between marijuana and hemp types. Estimation of heterozygosity for each individual was conducted with custom command-line scripts by dividing the number of heterozygous sites by the number of non-missing genotypes. The number of heterozygous sites was counted by vcflib tools. Plotting PCA results was completed via the ggplot2 59 package in Rstudio version 0. We also applied discriminant analysis DA of principal components 44 using the adegenet package Discriminant analysis can ascribe relationships for pre-defined groups without relying on a particular population genetics mode Files were read using the function read. In DAPC, data is first transformed using a principal components analysis PCA and subsequently the number of genetic clusters was assessed using the find. For k-means clustering, all of the principal components were retained. The K value with the lowest BIC was selected as the optimal number of clusters. DAPC was implemented using the optimized number of principal components as determined by the optim. Other values of K were tested not shown , but did not provide further optimization or descriptive value. MIGRATE-N was implemented with following parameters: the Bayesian inference strategy, for number of recorded steps in chain, a burn-in of for each chain and a full migration model with two population sizes and two migration rates. Significance levels for variance components and F-statistics were estimated using permutations. The authors are grateful to the Ministry of Science, Research and Technology of Iran as a funding source of this project. Special thanks to Dr. All the authors participated in the discussion of the results and writing of the article. Supplementary information accompanies this paper at Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This section collects any data citations, data availability statements, or supplementary materials included in this article. As a library, NLM provides access to scientific literature. Sci Rep. Find articles by Aboozar Soorni. Find articles by Reza Fatahi. Find articles by David C Haak. Find articles by Seyed Alireza Salami. Find articles by Aureliano Bombarely. Received May 23; Accepted Nov 1; Collection date Open in a new tab. Supplementary Information Supplementary Table S1 Supplementary Table S2 Supplementary Table S3 31KB, xls. Electronic supplementary material Supplementary information accompanies this paper at Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel.
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Assessment of Genetic Diversity and Population Structure in Iranian Cannabis Germplasm
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Evidence for an increase in cannabis use in Iran – A systematic review and trend analysis
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