1. Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens
- Author
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Sun-Jie Chen, Xin-Yang Liu, Wen-Hua Xue, Nan Xu, Jin-Li Zhang, and Hai-Jun Xu
- Subjects
Cancer Research ,Life Cycles ,Heredity ,Mutant ,Gene Dosage ,Gene Expression ,QH426-470 ,Biochemistry ,Homozygosity ,0302 clinical medicine ,Animal Wings ,Medicine and Health Sciences ,Wings, Animal ,Animal Anatomy ,Genetics (clinical) ,Regulation of gene expression ,Genetics ,Gene Editing ,0303 health sciences ,biology ,Drosophila Melanogaster ,Eukaryota ,Gene Expression Regulation, Developmental ,Animal Models ,Phenotype ,Adaptation, Physiological ,Insects ,Nucleic acids ,Experimental Organism Systems ,Insect Proteins ,Neofunctionalization ,Drosophila ,Brown planthopper ,Drosophila melanogaster ,Anatomy ,Research Article ,Signal Transduction ,Nymph ,endocrine system ,animal structures ,Arthropoda ,Longevity ,DNA replication ,Research and Analysis Methods ,Evolution, Molecular ,Hemiptera ,03 medical and health sciences ,Model Organisms ,health services administration ,Animals ,Gene Regulation ,cardiovascular diseases ,Molecular Biology ,Gene ,Ecology, Evolution, Behavior and Systematics ,030304 developmental biology ,Base Sequence ,fungi ,Organisms ,Biology and Life Sciences ,DNA ,biology.organism_classification ,Invertebrates ,Receptor, Insulin ,Nymphs ,Insulin receptor ,Starvation ,biology.protein ,Animal Studies ,CRISPR-Cas Systems ,Energy Metabolism ,Zoology ,Entomology ,030217 neurology & neurosurgery ,Developmental Biology - Abstract
A single insulin receptor (InR) gene has been identified and extensively studied in model species ranging from nematodes to mice. However, most insects possess additional copies of InR, yet the functional significance, if any, of alternate InRs is unknown. Here, we used the wing-dimorphic brown planthopper (BPH) as a model system to query the role of a second InR copy in insects. NlInR2 resembled the BPH InR homologue (NlInR1) in terms of nymph development and reproduction, but revealed distinct regulatory roles in fuel metabolism, lifespan, and starvation tolerance. Unlike a lethal phenotype derived from NlInR1 null, homozygous NlInR2 null mutants were viable and accelerated DNA replication and cell proliferation in wing cells, thus redirecting short-winged–destined BPHs to develop into long-winged morphs. Additionally, the proper expression of NlInR2 was needed to maintain symmetric vein patterning in wings. Our findings provide the first direct evidence for the regulatory complexity of the two InR paralogues in insects, implying the functionally independent evolution of multiple InRs in invertebrates., Author summary The highly conserved insulin/insulin-like growth factor signaling pathway plays a pivotal role in growth, development, and various physiological processes across a wide phylogeny of organisms. Unlike a single InR in the model species such as the fruit fly Drosophila melanogaster and the nematode Caenorhabditis elegans, most insect lineages have two or even three InR copies. However, the function of the alternative InRs remains elusive. Here, we created a homozygous mutation for a second insulin receptor (InR2) in the wing-dimorphic brown planthopper (BPH), Nilaparvata lugens, using the clustered regularly interspaced palindromic repeats/CRISPR-associated (CRISPR/Cas9) system. Our findings revealed that InR2 possesses functions distinct from the BPH InR homologue (NlInR1), indicating that multiple InR paralogues may have evolved independently and may have functionally diversified in ways more complex than previously expected in invertebrates.
- Published
- 2021