Evolutionary novelty in the apoptotic pathway of aphids

Autor: Cissy Huygens, Julien Orlans, Patrick Callaerts, Federica Calevro, Nicolas Parisot, Korneel Hens, Mélanie Ribeiro Lopes, Emmanuelle Jousselin, Karen Gaget, Gabrielle Duport, Pieter Baatsen, Sergio Peignier, Pedro da Silva, Hubert Charles
Přispěvatelé: Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Catholic University of Leuven - Katholieke Universiteit Leuven (KU Leuven), Leuven Center for Cancer Biology (VIB-KU-CCB), Catholic University of Leuven - Katholieke Universiteit Leuven (KU Leuven)-Vlaams Instituut voor Biotechnologie [Ghent, Belgique] (VIB), Centre de Biologie pour la Gestion des Populations (UMR CBGP), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Oxford Brookes University, This work was supported by the Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, INSA (Institut National des Sciences Appliquees), Lyon, the French ANR-16-CE02-0014 (HMicMac) program grant, and KU Leuven grant C14/17/099. INSA-Lyon supported P.C. with an Invited Professorship., ANR-16-CE02-0014,Hmicmac,Co-adaptations hôtes-microbiote: mécanismes et conséquences(2016), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro - Montpellier SupAgro, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)
Jazyk: angličtina
Rok vydání: 2020
Předmět:
Cellular differentiation
Genome
Insect
PROTEIN
Eye
ANNOTATION
Inhibitor of Apoptosis Proteins
ACTIVATION
Animals
Genetically Modified
0302 clinical medicine
insects
SPECIFICITY
Caspase
Phylogeny
Genetics
[SDV.EE]Life Sciences [q-bio]/Ecology
environment
0303 health sciences
Multidisciplinary
biology
Phylogenetic tree
apoptosis
INHIBITOR
food and beverages
IAP
Biological Sciences
Multidisciplinary Sciences
IAPs
Drosophila melanogaster
caspases
Science & Technology - Other Topics
Insect Proteins
EXPRESSION
Programmed cell death
Evolution
Protein domain
PROGRAMMED CELL-DEATH
03 medical and health sciences
Protein Domains
Animals
030304 developmental biology
Science & Technology
fungi
PEA APHID
Acyrthosiphon pisum
biology.organism_classification
GENE
Gene Expression Regulation
Aphids
biology.protein
Heterologous expression
030217 neurology & neurosurgery
[SDV.EE.IEO]Life Sciences [q-bio]/Ecology
environment/Symbiosis
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Proceedings of the National Academy of Sciences of the United States of America, National Academy of Sciences, 2020, 117 (51), pp.32545-32556. ⟨10.1073/pnas.2013847117⟩
Proceedings of the National Academy of Sciences of the United States of America, 2020, 117 (51), pp.32545-32556. ⟨10.1073/pnas.2013847117⟩
ISSN: 0027-8424
1091-6490
DOI: 10.1073/pnas.2013847117⟩
Popis: Significance Apoptotic processes play an important role in the development and physiology of almost all metazoan clades. In the highly diverse group of insects, apoptotic pathways have been characterized in only a few dipteran and lepidopteran species, which may not be representative of all insect species. Here, we report the first complete annotation of the apoptotic pathway in a hemipteran insect, the pea aphid Acyrthosiphon pisum. We showed that its apoptotic pathway is rewired compared to other insects, with a significant increase in the number of inhibitors of apoptosis (IAPs) and evidence for functional diversification and structural modularity of this protein family. These novelties are widespread in the aphid lineage, suggesting a yet not understood novel aphid-specific function of IAPs.
Apoptosis, a conserved form of programmed cell death, shows interspecies differences that may reflect evolutionary diversification and adaptation, a notion that remains largely untested. Among insects, the most speciose animal group, the apoptotic pathway has only been fully characterized in Drosophila melanogaster, and apoptosis-related proteins have been studied in a few other dipteran and lepidopteran species. Here, we studied the apoptotic pathway in the aphid Acyrthosiphon pisum, an insect pest belonging to the Hemiptera, an earlier-diverging and distantly related order. We combined phylogenetic analyses and conserved domain identification to annotate the apoptotic pathway in A. pisum and found low caspase diversity and a large expansion of its inhibitory part, with 28 inhibitors of apoptosis (IAPs). We analyzed the spatiotemporal expression of a selected set of pea aphid IAPs and showed that they are differentially expressed in different life stages and tissues, suggesting functional diversification. Five IAPs are specifically induced in bacteriocytes, the specialized cells housing symbiotic bacteria, during their cell death. We demonstrated the antiapoptotic role of these five IAPs using heterologous expression in a tractable in vivo model, the Drosophila melanogaster developing eye. Interestingly, IAPs with the strongest antiapoptotic potential contain two BIR and two RING domains, a domain association that has not been observed in any other species. We finally analyzed all available aphid genomes and found that they all show large IAP expansion, with new combinations of protein domains, suggestive of evolutionarily novel aphid-specific functions.
Databáze: OpenAIRE
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