Recurrent loss of an immunity gene that protects <i>Drosophila</i> against a major natural parasite

Arunkumar, Ramesh; Zhou, Shuyu Olivia; Day, Jonathan P.; Bakare, Sherifat; Pitton, Simone; Hsing, Chi-Yun; Boyle, Sinead O; Pascual-Gil, Juan; Clark, Belinda; Chandler, Rachael J.; Leitão, Alexandre B.; Jiggins, Francis M.

doi:10.1101/2022.05.27.493757

Cited by 4 publications

(15 citation statements)

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“…We have previously found that the expression of lectin-24A increases resistance to parasitoids, and the Drosophila Genetic Reference Panel (DGRP) line 437 carries a resistant allele of the gene whereas the DGRP-892 line carries a susceptible allele [12]. These two alleles differed in their expression levels, where the resistant allele is expressed at a higher level than the susceptible one in homeostasis and when the lectin-24A is upregulated after infection [12]. To investigate if the proximal upstream region of the lectin-24A gene responds specifically to parasitoid wasp infection, we infected D. melanogaster larvae expressing a lectin-24A reporter driven by 444 bp of sequence upstream from the transcription start site (TSS) of the resistant DGRP-437 allele ( Venus LP437 ) [12].…”

Section: Resultsmentioning

confidence: 99%

“…These two alleles differed in their expression levels, where the resistant allele is expressed at a higher level than the susceptible one in homeostasis and when the lectin-24A is upregulated after infection [12]. To investigate if the proximal upstream region of the lectin-24A gene responds specifically to parasitoid wasp infection, we infected D. melanogaster larvae expressing a lectin-24A reporter driven by 444 bp of sequence upstream from the transcription start site (TSS) of the resistant DGRP-437 allele ( Venus LP437 ) [12]. This upstream region was chosen because it is the entire intergenic sequence between lectin-24A and its adjacent gene Shaw .…”

Section: Resultsmentioning

confidence: 99%

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A humoral immune response to parasitoid wasps inDrosophilais regulated by JAK/STAT, NF-κB and GATA

Zhou,

Day,

Deplancke

et al. 2024

Preprint

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The two arms of innate immunity consist of the cell-mediated cellular defenses and the systemic humoral immune responses.Drosophilahumoral immune defenses in the context of antimicrobial immunity, particularly the regulation and activation of antimicrobial peptide secretion from the fat body, have been studied extensively. HowDrosophilaregulates humoral immunity against another major natural enemy, the parasitoid wasp, is less well-characterized. In this study, we focused on a gene crucial in anti-parasitoid immunity,lectin-24A, which is specifically induced following parasitization. We found that a fluorescent reporter driven by the region upstream oflectin-24Ashowed localized posterior expression in the larval fat body, theDrosophilatissue mediating humoral immunity. Furthermore, with RNA sequencing of the anterior and posterior fat body sections, we found that components of JAK/STAT, GATA, and Toll pathways were regulated differentially in the anterior-posterior axis of the fat body and/or by infection. Predicted binding motifs for transcription factors in all three of these pathways were identified in the 444bp upstream region of thelectin-24Agene, where scrambling these motifs leads to reduced basal or induced expression of the fluorescent reporter. Investigating each of these pathways, we found that JAK/STAT, the GATA factor Pannier, and the NF-κB factor dorsal all modulate the expression oflectin-24A. The binding motifs associated with these transcription factors were also enriched in the upstream sequences of parasitism-induced genes in the fat body. Taken together, these results indicate that JAK/STAT, Pannier, and NF-κB signaling are involved in the regulation oflectin-24Aand, more generally,Drosophilahumoral anti-parasitoid immunity after infection.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

A humoral immune response to parasitoid wasps inDrosophilais regulated by JAK/STAT, NF-κB and GATA

Zhou,

Day,

Deplancke

et al. 2024

Preprint

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“…While there is extensive literature describing humoral responses to parasitoid attack, these generally refer to compounds that do not have clear anti-parasitoid roles, such as the production of anti-microbial peptides (AMPs) 16 that are instead likely to be activated in response to the introduction of microbes during oviposition by wasps or reactive oxygen species generated by prophenoloxidase enzymes produced by specialized hemocytes. Other fat body factors implicated in parasitoid defense in D. melanogaster influence hemocyte production (e.g., Edin) 54 , or encourage recruitment of hemocytes to the wasp egg (e.g., Lectin24A) 55,56 . Similar to aphids, some Drosophila species have adopted facultative symbioses with bacteria like Spiroplasma, which express RIPs to protect against parasitoid challenge 21,57 .…”

Section: Discussionmentioning

confidence: 99%

Retracing the horizontal transfer of a novel innate immune factor inDrosophila

Tarnopol,

Tamsil,

Cinege

et al. 2024

Preprint

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SummaryImmune systems are among the most dynamically evolving traits across the tree of life, and long-lived macroparasites play an outsized role in shaping animal immunity. Even without adaptive immunity, insects have evolved potent innate immune strategies to neutralize such enemies, including nematodes and parasitoid wasps. One such strategy relies on endosymbioses between insects and toxin-expressing bacteria. Here, we use genome editing inDrosophila melanogasterto retrace the evolution of two of such toxins —cytolethal distending toxin B(cdtB) andapoptosis inducing protein of 56kDa(aip56) — that were horizontally transferred from bacteriophages to insects. We found that acdtB::aip56fusion gene (fusionB), which is conserved inDrosophila ananassaesubgroup species, dramatically promoted fly survival and suppressed wasp development when expressed inD. melanogasterimmune tissues. FusionB, a functional nuclease, was secreted into the host hemolymph where it targeted the parasitoid embryo’s serosal tissue and is to our knowledge the first humoral anti-parasitoid toxin inDrosophila. When expressed ubiquitously,fusionBslowed development in late stage fly larvae and eventually killed flies, pointing to the salience of regulatory constraint in preventing autoimmunity. Our findings demonstrate how horizontal gene transfer, in the right regulatory context, can instantly provide new and potent innate immune modules in animals.

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“…On the other hand, it was concluded that selection for loss-of-function mutations had no prominent role in chicken domestication [8,9]. However, accumulating genomic evidence supports loss-offunction mutations as a major driving force for the evolution (for a review, see [10][11][12]) of animals [13][14][15][16][17] and plants [18] as well as for the domestication (for a review, see [19,20]) of many farm animals [21] and crops [22,23].…”

Section: Introductionmentioning

confidence: 99%

Large scale loss-of-function mutations during chicken evolution and domestication

Wu,

Wang,

et al. 2024

Preprint

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Despite recent progresses, the driving force of evolution and domestication of chickens remains poorly understood. To fill this gap, we recently sequenced and assembled genomes of four distinct indigenous chickens from Yunnan, China. Unexpectedly, we found large numbers of pseudogenes which have lost their functions and are fixed in their corresponding populations, and we also found highly variable proteomes in the genomes of the four indigenous chickens as well as the sequenced wild red jungle fowl (RJF) (GRCg6a). Although the four indigenous chicken breeds are closely related to the G. g. spadiceous subspecies, for the first time, we found that the RJF (GRCg6a) is of the G. g. bankiva origin. Thus, the five chicken share the most recent common ancestor (MRCA) before subspeciation. Our results support a scenario that the MRCA of the four indigenous chickens and the RJF possessed at least 21,972 genes, of which 7,993 are dispensable. Each chicken has lost functions of thousands of the dispensable genes during their evolution and domestication via complete gene loss and pseudogenization. The occurring pattens of completely lost genes and pseudogenes segregate the chickens as their phylogenetic tree does. Therefore, loss-of-function mutations might play important roles in chicken evolution and domestication.

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Recurrent loss of an immunity gene that protects Drosophila against a major natural parasite

Cited by 4 publications

References 87 publications

A humoral immune response to parasitoid wasps inDrosophilais regulated by JAK/STAT, NF-κB and GATA

A humoral immune response to parasitoid wasps inDrosophilais regulated by JAK/STAT, NF-κB and GATA

Retracing the horizontal transfer of a novel innate immune factor inDrosophila

Large scale loss-of-function mutations during chicken evolution and domestication

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