A novel method for cross-species gene expression analysis

Kristiansson, Erik; Österlund, Tobias; Gunnarsson, Lars; Arne, Gabriella; Larsson, D. G. Joakim; Nerman, Olle

doi:10.1186/1471-2105-14-70

Cited by 46 publications

(49 citation statements)

References 82 publications

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“…EOGs were obtained from OrthoDB (21) (accessed October 15, 2013). To use a broad criterion for homology, we retained all paralogs (74), ultimately selecting the paralog showing the highest degree of differential expression between experimental and control conditions as the species representative for each homologous triplet. Homologous triplet combined significance scores were calculated using Fisher's method [R package MADAM (75)].…”

Section: Methodsmentioning

confidence: 99%

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Rittschof

Bukhari

Sloofman

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

142

196

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Certain complex phenotypes appear repeatedly across diverse species due to processes of evolutionary conservation and convergence. In some contexts like developmental body patterning, there is increased appreciation that common molecular mechanisms underlie common phenotypes; these molecular mechanisms include highly conserved genes and networks that may be modified by lineage-specific mutations. However, the existence of deeply conserved mechanisms for social behaviors has not yet been demonstrated. We used a comparative genomics approach to determine whether shared neuromolecular mechanisms could underlie behavioral response to territory intrusion across species spanning a broad phylogenetic range: house mouse (Mus musculus), stickleback fish (Gasterosteus aculeatus), and honey bee (Apis mellifera). Territory intrusion modulated similar brain functional processes in each species, including those associated with hormone-mediated signal transduction and neurodevelopment. Changes in chromosome organization and energy metabolism appear to be core, conserved processes involved in the response to territory intrusion. We also found that several homologous transcription factors that are typically associated with neural development were modulated across all three species, suggesting that shared neuronal effects may involve transcriptional cascades of evolutionarily conserved genes. Furthermore, immunohistochemical analyses of a subset of these transcription factors in mouse again implicated modulation of energy metabolism in the behavioral response. These results provide support for conserved genetic "toolkits" that are used in independent evolutions of the response to social challenge in diverse taxa.genetic hotspot | NF-κB signaling | brain metabolism | aggression S imilar phenotypes can have a shared molecular basis, even among distantly related species (1-3). This phenomenon has been observed for an array of traits, including morphological adaptations like coat color or wing patterning, rapid adaptations like drug resistance, and artificially selected phenological traits like flowering time (reviewed in ref. 2). Shared molecular mechanisms can arise convergently as a result of de novo mutations at genetic hotspots (2) or as a result of conservation. Both of these processes result in "genetic toolkits" or genes that are repeatedly used over evolutionary time to give rise to similar phenotypes (3). The phenomenon of genetic toolkits challenges fundamental notions about evolutionary convergence, conservation, and the origins of biodiversity.The role of genetic toolkits in shaping behavioral phenotypes is unclear (4, 5). Behaviors are typically polygenic (6) and they show great nuance and plasticity within a species, raising the possibility that cross-species similarities in behavior are superficial. Social behaviors in particular present a challenge to the genetic toolkit concept: these behaviors are critical to survival and reproductive success, but across species there is significant variation in the contexts for an...

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Section: Methodsmentioning

confidence: 99%

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Rittschof

Bukhari

Sloofman

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

142

196

View full text Add to dashboard Cite

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“…Extending such approaches to infer genome-scale networks for a large phylogeny with complex orthologies can be computationally expensive. While a number of studies have compared gene expression profiles across multiple species (Bergmann et al, 2003; Ihmels et al, 2005; Kristiansson et al, 2013; Roy et al, 2013b), these approaches typically identify gene modules that are conserved or diverged across species and do not provide fine-grained regulatory network connectivity information. Such information is critical to identify specific regulatory connections evolution must have made and broken as the species diverged.…”

Section: Introductionmentioning

confidence: 99%

Inference and Evolutionary Analysis of Genome-Scale Regulatory Networks in Large Phylogenies

et al. 2017

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SUMMARYChanges in transcriptional regulatory networks can significantly contribute to species evolution and adaptation. However, identification of genome-scale regulatory networks is an open challenge, especially in non-model organisms. Here, we introduce multi-species regulatory network learning (MRTLE), a computational approach that uses phylogenetic structure, sequence-specific motifs, and transcriptomic data, to infer the regulatory networks in different species. Using simulated data from known networks and transcriptomic data from six divergent yeasts, we demonstrate that MRTLE predicts networks with greater accuracy than existing methods because it incorporates phylogenetic information. We used MRTLE to infer the structure of the transcriptional networks that control the osmotic stress responses of divergent, non-model yeast species and then validated our predictions experimentally. Interrogating these networks reveals that gene duplication promotes network divergence across evolution. Taken together, our approach facilitates study of regulatory network evolutionary dynamics across multiple poorly studied species.

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“…We analysed genegroups for GO category enrichment, KEGG enrichment and transcription factors (as above). We then determined differentially expressed gene-groups across Andropogon and Sorghastrum with respect to treatment using the meta-level analytic method described inKristiansson et al (2013). This technique is powerful for deducing species by environment interactions where multiple orthologs and paralogs are found within each gene-group, as would be expected comparing species of different ploidies.…”

mentioning

confidence: 99%

Gene expression differs in codominant prairie grasses under drought

Hoffman

Smith

2017

Molecular Ecology Resources

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Grasslands of the central United States are expected to experience severe droughts and other climate extremes in the future, yet we know little about how these grasses will respond in terms of gene expression. We compared gene expression in Andropogon gerardii and Sorghastrum nutans, two closely related codominant C grasses responsible for the majority of ecosystem function, using RNA-seq. We compared Trinity assemblies within each species to determine annotated functions of transcripts responding to drought. Subsequently, we compared homologous annotated gene-groups across the two species using cross-species meta-level analysis and functional clustering based on key terms. The majority of variation was found between species, as opposed to between drought and watered treatments. However, there is evidence for differential responses; Andropogon allocated gene expression differently compared to Sorghastrum, suggesting Andropogon focuses on stress alleviation (such as oxygen radical scavenging) rather than prevention. In contrast, Sorghastrum may employ a drought avoidance strategy by modulating osmotic response, especially with hormonal regulation. We found Sorghastrum tended to be more sensitive within 10 key gene-groups related to stress, abscisic acid and trichomes, suggesting gene expression may mechanistically parallel sensitivity at the physiological level. Our findings corroborate phenotypic and physiological differences in the field and may help explain the phenotypic mechanisms of these two species in the tallgrass prairie community under future drought scenarios.

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A novel method for cross-species gene expression analysis

Cited by 46 publications

References 82 publications

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Inference and Evolutionary Analysis of Genome-Scale Regulatory Networks in Large Phylogenies

Gene expression differs in codominant prairie grasses under drought

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