Gene copy number and function of the APL1 immune factor changed during Anopheles evolution

Autor: Abbasali Raz, Christian Mitri, Emma Brito-Fravallo, Kenneth D. Vernick, Emmanuel Bischoff, Constentin Dieme, Inge Holm, Sedigheh Zakeri, Michelle M. Riehle, Karin Eiglmeier, Mahdokht I. K. Nejad, Navid Dinparast Djadid
Přispěvatelé: Génétique et Génomique des Insectes Vecteurs, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Génétique des Génomes Bactériens, Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris], Malaria and Vector Research Group (MVRG), Institut Pasteur d'Iran, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP), Medical College of Wisconsin [Milwaukee] (MCW), This study received financial support to KDV from the European Commission, Horizon 2020 Infrastructures #731060 Infravec2, European Research Council, Support for frontier research, Advanced Grant #323173 AnoPath, Agence Nationale de la Recherche, #ANR-19-CE35-0004 ArboVec, and French Laboratoire d’Excellence 'Integrative Biology of Emerging Infectious Diseases' #ANR-10-LABX-62-IBEID and to MMR from National Institutes of Health, NIAID #AI121587. Funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript., ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010), European Project: 731060,INFRAVEC2(2017), European Project: 323173,EC:FP7:ERC,ERC-2012-ADG_20120314,ANOPATH(2013), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)
Jazyk: angličtina
Rok vydání: 2020
Předmět:
0301 basic medicine
Anopheles gambiae
[SDV]Life Sciences [q-bio]
Gene Dosage
MESH: Gene Dosage
0302 clinical medicine
Mosquito
MESH: Insect Proteins
MESH: Animals
Copy-number variation
MESH: Peptide Fragments
MESH: Phylogeny
Phylogeny
Gene essentiality
MESH: Evolution
Molecular
Genetics
Gene neofunctionalization
MESH: Immunologic Factors
Anopheles
3. Good health
Infectious Diseases
MESH: Longevity
Insect immunity
Insect Proteins
030231 tropical medicine
Longevity
MESH: Malaria
Locus (genetics)
MESH: Insect Vectors
Biology
lcsh:Infectious and parasitic diseases
Evolution
Molecular
MESH: Anopheles
03 medical and health sciences
parasitic diseases
Gene silencing
Gene family
Animals
Immunologic Factors
lcsh:RC109-216
Gene
Anopheles stephensi
[SDV.GEN]Life Sciences [q-bio]/Genetics
Research
fungi
Chaperonin 60
biology.organism_classification
Peptide Fragments
Insect Vectors
Malaria
030104 developmental biology
MESH: Chaperonin 60
Parasitology
Zdroj: Parasites and Vectors
Parasites and Vectors, BioMed Central, 2020, 13 (1), pp.18. ⟨10.1186/s13071-019-3868-y⟩
Parasites & Vectors
Parasites & Vectors, 2020, 13 (1), pp.18. ⟨10.1186/s13071-019-3868-y⟩
Parasites & Vectors, Vol 13, Iss 1, Pp 1-12 (2020)
ISSN: 1756-3305
DOI: 10.1186/s13071-019-3868-y⟩
Popis: Background The recent reference genome assembly and annotation of the Asian malaria vector Anopheles stephensi detected only one gene encoding the leucine-rich repeat immune factor APL1, while in the Anopheles gambiae and sibling Anopheles coluzzii, APL1 factors are encoded by a family of three paralogs. The phylogeny and biological function of the unique APL1 gene in An. stephensi have not yet been specifically examined. Methods The APL1 locus was manually annotated to confirm the computationally predicted single APL1 gene in An. stephensi. APL1 evolution within Anopheles was explored by phylogenomic analysis. The single or paralogous APL1 genes were silenced in An. stephensi and An. coluzzii, respectively, followed by mosquito survival analysis, experimental infection with Plasmodium and expression analysis. Results APL1 is present as a single ancestral gene in most Anopheles including An. stephensi but has expanded to three paralogs in an African lineage that includes only the Anopheles gambiae species complex and Anopheles christyi. Silencing of the unique APL1 copy in An. stephensi results in significant mosquito mortality. Elevated mortality of APL1-depleted An. stephensi is rescued by antibiotic treatment, suggesting that pathology due to bacteria is the cause of mortality, and indicating that the unique APL1 gene is essential for host survival. Successful Plasmodium development in An. stephensi depends upon APL1 activity for protection from high host mortality due to bacteria. In contrast, silencing of all three APL1 paralogs in An. coluzzii does not result in elevated mortality, either with or without Plasmodium infection. Expression of the single An. stephensi APL1 gene is regulated by both the Imd and Toll immune pathways, while the two signaling pathways regulate different APL1 paralogs in the expanded APL1 locus. Conclusions APL1 underwent loss and gain of functions concomitant with expansion from a single ancestral gene to three paralogs in one lineage of African Anopheles. We infer that activity of the unique APL1 gene promotes longevity in An. stephensi by conferring protection from or tolerance to an effect of bacterial pathology. The evolution of an expanded APL1 gene family could be a factor contributing to the exceptional levels of malaria transmission mediated by human-feeding members of the An. gambiae species complex in Africa.
Databáze: OpenAIRE
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