Gene clustering pattern, promoter architecture, and gene expression stability in eukaryotic genomes

Woo, Yong; Li, Wen-Hsiung

doi:10.1073/pnas.1100210108

Cited by 33 publications

(28 citation statements)

References 34 publications

(52 reference statements)

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“…Remarkably, the median intergenic distance within gene-dense regions of P. infestans is even less than that of most yeasts [25], [44]. The ratio of adjacent P. infestans genes that are transcribed in the same direction versus from a shared or adjacent promoter region is 1.43, which is higher than that of S. cerevisiae and A. thaliana [45]. This presumably reflects functional constraints associated with having small adjacent promoters, which is reflected in the co-expression or anti-correlated profiles of about 10% of adjacent P. infestans genes.…”

Section: Discussionmentioning

confidence: 86%

Genome-wide Prediction and Functional Validation of Promoter Motifs Regulating Gene Expression in Spore and Infection Stages of Phytophthora infestans

2013

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Most eukaryotic pathogens have complex life cycles in which gene expression networks orchestrate the formation of cells specialized for dissemination or host colonization. In the oomycete Phytophthora infestans, the potato late blight pathogen, major shifts in mRNA profiles during developmental transitions were identified using microarrays. We used those data with search algorithms to discover about 100 motifs that are over-represented in promoters of genes up-regulated in hyphae, sporangia, sporangia undergoing zoosporogenesis, swimming zoospores, or germinated cysts forming appressoria (infection structures). Most of the putative stage-specific transcription factor binding sites (TFBSs) thus identified had features typical of TFBSs such as position or orientation bias, palindromy, and conservation in related species. Each of six motifs tested in P. infestans transformants using the GUS reporter gene conferred the expected stage-specific expression pattern, and several were shown to bind nuclear proteins in gel-shift assays. Motifs linked to the appressoria-forming stage, including a functionally validated TFBS, were over-represented in promoters of genes encoding effectors and other pathogenesis-related proteins. To understand how promoter and genome architecture influence expression, we also mapped transcription patterns to the P. infestans genome assembly. Adjacent genes were not typically induced in the same stage, including genes transcribed in opposite directions from small intergenic regions, but co-regulated gene pairs occurred more than expected by random chance. These data help illuminate the processes regulating development and pathogenesis, and will enable future attempts to purify the cognate transcription factors.

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Section: Discussionmentioning

confidence: 86%

Genome-wide Prediction and Functional Validation of Promoter Motifs Regulating Gene Expression in Spore and Infection Stages of Phytophthora infestans

2013

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“…This strategy could be positive in terms of the economics of regulation [11], but negative in terms of functional conflicts, e.g., need of bipolarity in genome-wide transcription [12,13], presence of gene classes requiring precise but plastic expression [14], etc. An additional question is to what extent a demand for variation acts as a central force for the organization of genomes and vice versa, i.e., whether structural genomic features constrain variation [15][16][17].…”

Section: Introductionmentioning

confidence: 99%

Balancing noise and plasticity in eukaryotic gene expression

Bajić

Poyatos

2012

BMC Genomics

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BackgroundCoupling the control of expression stochasticity (noise) to the ability of expression change (plasticity) can alter gene function and influence adaptation. A number of factors, such as transcription re-initiation, strong chromatin regulation or genome neighboring organization, underlie this coupling. However, these factors do not necessarily combine in equivalent ways and strengths in all genes. Can we identify then alternative architectures that modulate in distinct ways the linkage of noise and plasticity?ResultsHere we first show that strong chromatin regulation, commonly viewed as a source of coupling, can lead to plasticity without noise. The nature of this regulation is relevant too, with plastic but noiseless genes being subjected to general activators whereas plastic and noisy genes experience more specific repression. Contrarily, in genes exhibiting poor transcriptional control, it is translational efficiency what separates noise from plasticity, a pattern related to transcript length. This additionally implies that genome neighboring organization –as modifier– appears only effective in highly plastic genes. In this class, we confirm bidirectional promoters (bipromoters) as a configuration capable to reduce coupling by abating noise but also reveal an important trade-off, since bipromoters also decrease plasticity. This presents ultimately a paradox between intergenic distances and modulation, with short intergenic distances both associated and disassociated to noise at different plasticity levels.ConclusionsBalancing the coupling among different types of expression variability appears as a potential shaping force of genome regulation and organization. This is reflected in the use of different control strategies at genes with different sets of functional constraints.

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“…Recently in yeast, bidirectional promoters were shown to have greater nucleosome depletion and to be flanked by strongly positioned nucleosomes, possibly resulting in lower gene expression variability of the bidirectional gene pairs (Woo and Li, 2011). Detailed nucleosome positioning of human bidirectional promoters remains to be clarified, which might explain the minor peak (51 kb) of the length of bidirectional promoters (Figure 2).…”

Section: Chromatin Structure and Epigenetic Modificationmentioning

confidence: 99%

“…For example, transcriptional interference, which is the suppressive influence of one transcriptional process on a second transcriptional process, can act on adjacent gene pairs (Shearwin et al, 2005) and might have greater influence on HT pairs (Franck et al, 2008). Moreover, the length of 3' UTR has increased drastically in mammals and these increased regulatory complexity at the 3' end of genes might cause greater loss of HT pairs (Woo and Li, 2011). Another possibility is that there have been many chances to give rise to bidirectional gene pairs compared to other gene pairs by some unknown reasons, resulting in the enrichment of bidirectional gene pairs.…”

Section: Evolutionary Force Forming Overrepresentation Of Bidirectionmentioning

confidence: 99%

Bidirectional Gene Pairs in the Human Genome

Koyanagi

Imanishi

Gojobori

2013

Encyclopedia of Life Sciences

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Bidirectional gene pairs, also called head‐to‐head gene pairs, are defined as two genes on different strands with adjacent 5′‐ends. They are transcribed divergently in a variety of coordinated fashion. The region between a bidirectional gene pair is designated as a putative bidirectional promoter, which is suggested to coordinately regulate the expression of the pair. The closely located bidirectional gene pairs and their bidirectional promoters were recently found to be enriched in the human genome. Despite substantial interests in these gene pairs and their expression regulation through bidirectional promoters, their biological significance is not well understood. Furthermore, it is of particular interest to know when and how the bidirectional gene arrangement evolved. Here the current understanding of these pairs is reviewed: bidirectional gene pairs may have great biological significance, and the bidirectional gene arrangement has evolved during the evolution of vertebrates leading to mammals by relocation of existing genes. Key Concepts: Closely located bidirectional gene pairs are enriched in the human genome. Bidirectional gene pairs show correlated expression pattern. Bidirectional gene pairs tend to have basic function in cells such as DNA repair. Bidirectional promoters lack TATA boxes and are enriched in CpG islands. Specific transcription factors are overrepresented in bidirectional promoters. Bidirectional genes pairs tend to transcribe actively. Bidirectional gene arrangement has evolved during the evolution of vertebrates leading to mammals by relocation of existing genes. Detailed mechanisms of bidirectional transcription and the evolutionary forces that shaped the bidirectional arrangement in the human genome remain to be elucidated.

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Gene clustering pattern, promoter architecture, and gene expression stability in eukaryotic genomes

Cited by 33 publications

References 34 publications

Genome-wide Prediction and Functional Validation of Promoter Motifs Regulating Gene Expression in Spore and Infection Stages of Phytophthora infestans

Genome-wide Prediction and Functional Validation of Promoter Motifs Regulating Gene Expression in Spore and Infection Stages of Phytophthora infestans

Balancing noise and plasticity in eukaryotic gene expression

Bidirectional Gene Pairs in the Human Genome

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