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Gene direction, which is important for function, has not been subjected to statistical testing for randomness and for the degree of evolutionary changes. We analyzed 747 sequenced species and 2,061 genomes/ chromosomes and detected clear differences in gene direction between kingdoms. All the archaeans, bacteria, and protozoa analyzed have genes characterized mainly by same-direction neighbors (i.e., in head-to-foot or foot-to-head order), with up to 391 genes in tandem in protozoan Leishmania<span class="external-identifiers"> <a target="_blank" rel="external noopener noreferrer" href="https://doi.org/10.1038/srep00982">doi:10.1038/srep00982</a> <a target="_blank" rel="external noopener" href="https://fatcat.wiki/release/cto2gu4nhfed3kro3g255swgae">fatcat:cto2gu4nhfed3kro3g255swgae</a> </span>
more »... nfantum. Fungi and photosynthetic protists have genes characterized by opposite-direction neighbors, except chromosome VII of Ashbya gossypii, a progenitor fungus. The gene direction analysis suggests that the same-direction dominance originated from the last common ancestor of these living organisms, then was strengthened in protozoa, but weakened or lost in fungi, photosynthetic protists and some plants/animals, giving chromosomes/genomes with gene opposite-direction dominance (i.e., towards the random use of both DNA strands). N eighborhood conservation of gene arrangement was found in various bacteria 1 and eukaryotic organisms 2-8 from studying specific species or a group of genes. Gene direction is important for gene arrangement and function. Since random arrangement of a large number of genes along the chromosomes can theoretically generate a multiplicity of gene direction orders, a statistical test of gene direction randomness is required. To the best of our knowledge, however, there are no literature reports on algorithms suitable for testing gene direction randomness, likely because of the lack of a readily available algorithms for testing whether a series of two numbers or two letters (e.g., 1 for forward, 2 for backward) is random. Research is needed to develop a statistical algorithm to test gene direction randomness and to analyze many genomes for general information on gene direction distribution. Genes with similar function or coordinated expression seem to be clustered in sequenced genomes 3 . Furthermore, the order of transcriptionally and functionally linked genes was found to be conserved in some eukaryotes, in a study using various analysis methods, including protein sequence BLAST searches, gene ontology assignments, and phylogenetic tree reconstruction 4 . It has been proposed that the range for which DNA neighborhood optimizes biochemical interactions might therefore be defined by DNA topology 1 . Recently, the notion that expression neighborhoods are a feature of eukaryotic genome organization necessary for correct gene expression was publically challenged because a targeted separation of one well-defined gene expression neighborhood in the Drosophila genome did not significantly alter gene expression 9 . Since gene direction order is an important aspect of gene order and architecture, an analysis of the gene direction in a large number of genomes may provide insights into whether gene neighborhoods are random, or likely the result of selection and inheritance. In this study, we developed a statistical approach to test the significance of gene direction order. Since an intergenic region can have four possible configurations, that is, FF, BB, FB, and BF, where F denotes forward gene direction and B backward gene direction (i.e., on the complementary strand), the probability of occurrence of these four types of intergenic regions should be approximately equal if gene order on the annotated DNA sequence of a chromosome is random. The chi-square test approach can test the randomness of these four configurations. We tested the randomness of the direction of annotated genes on chromosomes (GenBank full version files; see Tables S1-S7 for sequence ID list) of all or nearly all complete and annotated genomes of bacteria, archaeans, protists, fungi, plants, and animals available in NCBI GenBank (http://www.ncbi.nlm.nih. gov/), and present the findings below.
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