More Like this

1. Immune System Promiscuity in Human and Nonhuman Primate Evolution

   Brinkworth, J.F.; Babbitt, C.C. (October 2019, Human biology)

   Many genes that respond to infection have functions outside of immunity and have been found to be under natural selection. Pathogens may therefore incidentally alter nonimmune physiology through engagement with immune system genes. This raises a logical question of how genetically promiscuous the immune system is, here defijined as how heavily cross-referenced the immune system is into other physiological systems. This work examined immune gene promiscuity across physiological systems in primates by assessing the baseline (unperturbed) expression of key tissue and cell types for diffferences, and primate genomes for signatures of selection. These effforts revealed “immune” gene expression to be cross-referenced extensively in other physiological systems in primates. When immune and nonim-mune tissues diverge in expression, the diffferentially expressed genes at baseline are enriched for cell biological activities not immediately identifijiable as immune function based. Individual comparisons of immune and nonimmune tissues in primates revealed low divergence in gene expression between tissues, with the exception of whole blood. Immune gene promiscuity increases over evolutionary time, with hominoids exhibiting the most cross-referencing of such genes among primates. An assessment of genetic sequences also found positive selection in the coding regions of diffferentially expressed genes between tissues functionally associated with immunity. This suggests that, with increasing promiscuity, divergent gene expression between the immune system and other physiological systems tends to be adaptive and enriched for immune functions in hominoids. 

   more » « less
2. Differential gene expression in response to fungal pathogen exposure in the aquatic invertebrate, Daphnia dentifera

   https://doi.org/10.1002/ece3.10354  

   Terrill Sondag, Emily_E; Stewart Merrill, Tara_E; Drnevich, Jenny; Holmes, Jessica_R; Fischer, Eva_K; Cáceres, Carla_E; Strickland, Lynette_R (July 2023, Ecology and Evolution)

   Abstract While vertebrate immune systems are appreciated for their complexity and adaptability, invertebrate immunity is often considered to be less complex. However, immune responses in many invertebrates likely involve sophisticated processes. Interactions between the crustacean hostDaphnia dentiferaand its fungal pathogenMetschnikowia bicuspidataprovide an excellent model for exploring the mechanisms underlying crustacean immunity. To explore the genomic basis of immunity inDaphnia, we used RNA‐sequencing technology to quantify differential gene expression between individuals of a single host genotype exposed or unexposed toM. bicuspidataover 24 h. Transcriptomic analyses showed that the number of differentially expressed genes between the control (unexposed) and experimental (exposed) groups increased over time. Gene ontology enrichment analysis revealed that differentially expressed genes were enriched for immune‐related molecules and processes, such as cuticle development, prostaglandin, and defense response processes. Our findings provide a suite of immunologically relevant genes and suggest the presence of a rapidly upregulated immune response involving the cuticle inDaphnia. Studies involving gene expression responses to pathogen exposure shine a light on the processes occurring during the course of infection. By leveraging knowledge on the genetic basis for immunity, immune mechanisms can be more thoroughly understood to refine our understanding of disease spread within invertebrate populations. 

   more » « less
3. Immune Gene Expression Covaries with Gut Microbiome Composition in Stickleback

   https://doi.org/10.1128/mBio.00145-21  

   Fuess, Lauren E.; den Haan, Stijn; Ling, Fei; Weber, Jesse N.; Steinel, Natalie C.; Bolnick, Daniel I. (January 2021, mBio)

   Rawls, John F.; McFall-Ngai, Margaret J. (Ed.)

   ABSTRACT Commensal microbial communities have immense effects on their vertebrate hosts, contributing to a number of physiological functions, as well as host fitness. In particular, host immunity is strongly linked to microbiota composition through poorly understood bi-directional links. Gene expression may be a potential mediator of these links between microbial communities and host function. However, few studies have investigated connections between microbiota composition and expression of host immune genes in complex systems. Here, we leverage a large study of laboratory-raised fish from the species Gasterosteus aculeatus (three-spined stickleback) to document correlations between gene expression and microbiome composition. First, we examined correlations between microbiome alpha diversity and gene expression. Our results demonstrate robust positive associations between microbial alpha diversity and expression of host immune genes. Next, we examined correlations between host gene expression and abundance of microbial taxa. We identified 15 microbial families that were highly correlated with host gene expression. These families were all tightly correlated with host expression of immune genes and processes, falling into one of three categories—those positively correlated, negatively correlated, and neutrally related to immune processes. Furthermore, we highlight several important immune processes that are commonly associated with the abundance of these taxa, including both macrophage and B cell functions. Further functional characterization of microbial taxa will help disentangle the mechanisms of the correlations described here. In sum, our study supports prevailing hypotheses of intimate links between host immunity and gut microbiome composition. IMPORTANCE Here, we document associations between host gene expression and gut microbiome composition in a nonmammalian vertebrate species. We highlight associations between expression of immune genes and both microbiome diversity and abundance of specific microbial taxa. These findings support other findings from model systems which have suggested that gut microbiome composition and host immunity are intimately linked. Furthermore, we demonstrate that these correlations are truly systemic; the gene expression detailed here was collected from an important fish immune organ (the head kidney) that is anatomically distant from the gut. This emphasizes the systemic impact of connections between gut microbiota and host immune function. Our work is a significant advancement in the understanding of immune-microbiome links in nonmodel, natural systems. 

   more » « less
4. Convergent Loss of an EDS1/PAD4 Signaling Pathway in Several Plant Lineages Reveals Coevolved Components of Plant Immunity and Drought Response

   https://doi.org/10.1105/tpc.19.00903  

   Baggs, Erin L.; Monroe, J. Grey; Thanki, Anil S.; O’Grady, Ruby; Schudoma, Christian; Haerty, Wilfried; Krasileva, Ksenia V. (May 2020, The Plant Cell)

   Abstract Plant innate immunity relies on nucleotide binding leucine-rich repeat receptors (NLRs) that recognize pathogen-derived molecules and activate downstream signaling pathways. We analyzed the variation in NLR gene copy number and identified plants with a low number of NLR genes relative to sister species. We specifically focused on four plants from two distinct lineages, one monocot lineage (Alismatales) and one eudicot lineage (Lentibulariaceae). In these lineages, the loss of NLR genes coincides with loss of the well-known downstream immune signaling complex ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1)/PHYTOALEXIN DEFICIENT 4 (PAD4). We expanded our analysis across whole proteomes and found that other characterized immune genes were absent only in Lentibulariaceae and Alismatales. Additionally, we identified genes of unknown function that were convergently lost together with EDS1/PAD4 in five plant species. Gene expression analyses in Arabidopsis (Arabidopsis thaliana) and Oryza sativa revealed that several homologs of the candidates are differentially expressed during pathogen infection, drought, and abscisic acid treatment. Our analysis provides evolutionary evidence for the rewiring of plant immunity in some plant lineages, as well as the coevolution of the EDS1/PAD4 pathway and drought responses. 

   more » « less
5. Gene expression signatures between Limia perugiae (Poeciliidae) populations from freshwater and hypersaline habitats, with comparisons to other teleosts

   https://doi.org/10.1371/journal.pone.0315014  

   Wilson, Elizabeth J; Barts, Nick; Coffin, John L; Johnson, James B; Rodríguez_Peña, Carlos M; Kelley, Joanna L; Tobler, Michael; Greenway, Ryan (December 2024, PLOS ONE)

   Chen, Tzong-Yueh (Ed.)

   Salinity gradients act as strong environmental barriers that limit the distribution of aquatic organisms. Changes in gene expression associated with transitions between freshwater and saltwater environments can provide insights into organismal responses to variation in salinity. We used RNA-sequencing (RNA-seq) to investigate genome-wide variation in gene expression between a hypersaline population and a freshwater population of the livebearing fish speciesLimia perugiae(Poeciliidae). Our analyses of gill gene expression revealed potential molecular mechanisms underlying salinity tolerance in this species, including the enrichment of genes involved in ion transport, maintenance of chemical homeostasis, and cell signaling in the hypersaline population. We also found differences in gene expression patterns associated with cell-cycle and protein-folding processes between the hypersaline and freshwaterL.perugiae. Bidirectional freshwater-saltwater transitions have occurred repeatedly during the diversification of fishes, allowing for broad-scale examination of repeatable patterns in evolution. Therefore, we compared transcriptomic variation inL.perugiaewith other teleosts that have made freshwater-saltwater transitions to test for convergence in gene expression. Among the four distantly related population pairs from high- and low-salinity environments that we included in our analysis, we found only ten shared differentially expressed genes, indicating little evidence for convergence. However, we found that differentially expressed genes shared among three or more lineages were functionally enriched for ion transport and immune functioning. Overall, our results—in conjunction with other recent studies—suggest that different genes are involved in salinity transitions across disparate lineages of teleost fishes. 

   more » « less