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1. Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance

   https://doi.org/10.1371/journal.ppat.1011567  

   Cabrera, Kevin; Hoard, Duncan S.; Gibson, Olivia; Martinez, Daniel I.; Wunderlich, Zeba (August 2023, PLOS Pathogens)

   Garsin, Danielle A. (Ed.)

   Innate immune priming increases an organism’s survival of a second infection after an initial, non-lethal infection. We usedDrosophila melanogasterand an insect-derived strain ofEnterococcus faecalisto study transcriptional control of priming. In contrast to other pathogens, the enhanced survival in primed animals does not correlate with decreasedE.faecalisload. Further analysis shows that primed organisms tolerate, rather than resist infection. Using RNA-seq of immune tissues, we found many genes were upregulated in only primed flies, suggesting a distinct transcriptional program in response to initial and secondary infections. In contrast, few genes continuously express throughout the experiment or more efficiently re-activate upon reinfection. Priming experiments in immune deficient mutants revealed Imd is largely dispensable for responding to a single infection but needed to fully prime. Together, this indicates the fly’s innate immune response is plastic—differing in immune strategy, transcriptional program, and pathway use depending on infection history. 

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2. Natural variation in the contribution of microbial density to inducible immune dynamics

   https://doi.org/10.1111/mec.15293  

   Jent, Derrick; Perry, Abby; Critchlow, Justin; Tate, Ann T. (November 2019, Molecular Ecology)

   Abstract Immune responses evolve to balance the benefits of microbial killing against the costs of autoimmunity and energetic resource use. Models that explore the evolution of optimal immune responses generally include a term for constitutive immunity, or the level of immunological investment prior to microbial exposure, and for inducible immunity, or investment in immune function after microbial challenge. However, studies rarely consider the functional form of inducible immune responses with respect to microbial density, despite the theoretical dependence of immune system evolution on microbe‐ versus immune‐mediated damage to the host. In this study, we analyse antimicrobial peptide (AMP) gene expression from seven wild‐caught flour beetle populations (Triboliumspp.) during acute infection with the virulent bacteriaBacillus thuringiensis(Bt) andPhotorhabdus luminescens(P.lum) to demonstrate that inducible immune responses mediated by the humoral IMD pathway exhibit natural variation in both microbe density‐dependent and independent temporal dynamics. Beetle populations that exhibited greater AMP expression sensitivity to Bt density were also more likely to die from infection, while populations that exhibited higher microbe density‐independent AMP expression were more likely to surviveP. luminescensinfection. Reduction in pathway signalling efficiency through RNAi‐mediated knockdown of theimdgene reduced the magnitude of both microbe‐independent and dependent responses and reduced host resistance to Bt growth, but had no net effect on host survival. This study provides a framework for understanding natural variation in the flexibility of investment in inducible immune responses and should inform theory on the contribution of nonequilibrium host‐microbe dynamics to immune system evolution. 

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3. Mapping responsive genomic elements to heat stress in a maize diversity panel

   https://doi.org/10.1186/s13059-022-02807-7  

   Liang, Zhikai; Myers, Zachary A.; Petrella, Dominic; Engelhorn, Julia; Hartwig, Thomas; Springer, Nathan M. (November 2022, Genome Biology)

   Abstract BackgroundMany plant species exhibit genetic variation for coping with environmental stress. However, there are still limited approaches to effectively uncover the genomic region that regulates distinct responsive patterns of the gene across multiple varieties within the same species under abiotic stress. ResultsBy analyzing the transcriptomes of more than 100 maize inbreds, we reveal manycis- andtrans-acting eQTLs that influence the expression response to heat stress. Thecis-acting eQTLs in response to heat stress are identified in genes with differential responses to heat stress between genotypes as well as genes that are only expressed under heat stress. Thecis-acting variants for heat stress-responsive expression likely result from distinct promoter activities, and the differential heat responses of the alleles are confirmed for selected genes using transient expression assays. Global footprinting of transcription factor binding is performed in control and heat stress conditions to document regions with heat-enriched transcription factor binding occupancies. ConclusionsFootprints enriched near proximal regions of characterized heat-responsive genes in a large association panel can be utilized for prioritizing functional genomic regions that regulate genotype-specific responses under heat stress. 

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4. Inherent constraints on a polyfunctional tissue lead to a reproduction-immunity tradeoff

   https://doi.org/10.1186/s12915-022-01328-w  

   Gupta, Vanika; Frank, Ashley M.; Matolka, Nick; Lazzaro, Brian P. (December 2022, BMC Biology)

   Abstract Background Single tissues can have multiple functions, which can result in constraints, impaired function, and tradeoffs. The insect fat body performs remarkably diverse functions including metabolic control, reproductive provisioning, and systemic immune responses. How polyfunctional tissues simultaneously execute multiple distinct physiological functions is generally unknown. Immunity and reproduction are observed to trade off in many organisms but the mechanistic basis for this tradeoff is also typically not known. Here we investigate constraints and trade-offs in the polyfunctional insect fat body. Results Using single-nucleus sequencing, we determined that the Drosophila melanogaster fat body executes diverse basal functions with heterogenous cellular subpopulations. The size and identity of these subpopulations are remarkably stable between virgin and mated flies, as well as before and after infection. However, as an emergency function, the immune response engages the entire tissue and all cellular subpopulations produce induce expression of defense genes. We found that reproductively active females who were given bacterial infection exhibited signatures of ER stress and impaired capacity to synthesize new protein in response to infection, including decreased capacity to produce antimicrobial peptides. Transient provision of a reversible translation inhibitor to mated females prior to infection rescued general protein synthesis, specific production of antimicrobial peptides, and survival of infection. Conclusions The commonly observed tradeoff between reproduction and immunity appears to be driven, in D. melanogaster , by a failure of the fat body to be able to handle simultaneous protein translation demands of reproductive provisioning and immune defense. We suggest that inherent cellular limitations in tissues that perform multiple functions may provide a general explanation for the wide prevalence of physiological and evolutionary tradeoffs. 

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5. Induction of Multiple Immune Signaling Pathways in Gryllodes sigillatus Crickets during Overt Viral Infections

   https://doi.org/10.3390/v14122712  

   Duffield, Kristin R.; Foquet, Bert; Stasko, Judith A.; Hunt, John; Sadd, Ben M.; Sakaluk, Scott K.; Ramirez, José L. (December 2022, Viruses)

   Despite decades of focus on crickets (family: Gryllidae) as a popular commodity and model organism, we still know very little about their immune responses to microbial pathogens. Previous studies have measured downstream immune effects (e.g., encapsulation response, circulating hemocytes) following an immune challenge in crickets, but almost none have identified and quantified the expression of immune genes during an active pathogenic infection. Furthermore, the prevalence of covert (i.e., asymptomatic) infections within insect populations is becoming increasingly apparent, yet we do not fully understand the mechanisms that maintain low viral loads. In the present study, we measured the expression of several genes across multiple immune pathways in Gryllodes sigillatus crickets with an overt or covert infection of cricket iridovirus (CrIV). Crickets with overt infections had higher relative expression of key pathway component genes across the Toll, Imd, Jak/STAT, and RNAi pathways. These results suggests that crickets can tolerate low viral infections but can mount a robust immune response during an overt CrIV infection. Moreover, this study provides insight into the immune strategy of crickets following viral infection and will aid future studies looking to quantify immune investment and improve resistance to pathogens. 

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