Genome-Wide Analysis of Gene Families of Pattern Recognition Receptors in Fig Wasps (Hymenoptera, Chalcidoidea)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Gene Identification and Feature Prediction
2.2. Phylogenetic Analysis
2.3. Gene Family Expansion and Contraction
2.4. Functional Divergence Analysis
2.5. Genomic Location Analysis
3. Results
3.1. Gram-Negative Bacteria-Binding Proteins (GNBPs)
3.2. C-Type Lectins (CTLs)
3.3. Scavenger Receptor B (SCRBs)
3.4. Fibrinogen-Related Proteins (FREPs)
3.5. Galectins
3.6. Thioester-Containing Proteins (TEPs)
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Lemaitre, B.; Hoffmann, J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25, 697–743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lu, Y.; Su, F.; Li, Q.; Zhang, J.; Li, Y.; Tang, T.; Hu, Q.; Yu, X.Q. Pattern recognition receptors in Drosophila immune responses. Dev. Comp. Immunol. 2020, 102, 103468. [Google Scholar] [CrossRef] [PubMed]
- Beutler, B. Innate immunity: An overview. Mol. Immunol. 2004, 40, 845–859. [Google Scholar] [CrossRef] [PubMed]
- Pal, S.; Wu, L.P. Pattern recognition receptors in the fly: Lessons we can learn from the Drosophila melanogaster immune system. Fly 2009, 3, 121–129. [Google Scholar] [CrossRef] [Green Version]
- Tanaka, H.; Ishibashi, J.; Fujita, K.; Nakajima, Y.; Sagisaka, A.; Tomimoto, K.; Suzuki, N.; Yoshiyama, M.; Kaneko, Y.; Iwasaki, T.; et al. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem. Mol. Biol. 2008, 38, 1087–1110. [Google Scholar] [CrossRef] [PubMed]
- Nei, M.; Rooney, A.P. Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 2005, 39, 121–152. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Christophides, G.K.; Zdobnov, E.; Barillas-Mury, C.; Birney, E.; Blandin, S.; Blass, C.; Brey, P.T.; Collins, F.H.; Danielli, A.; Dimopoulos, G.; et al. Immunity-related genes and gene families in Anopheles gambiae. Science 2002, 298, 159–165. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eirín-López, J.M.; Rebordinos, L.; Rooney, A.P.; Rozas, J. The birth-and-death evolution of multigene families revisited. Genome Dyn. 2012, 7, 170–196. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scott, J.G.; Warren, W.C.; Beukeboom, L.W.; Bopp, D.; Clark, A.G.; Giers, S.D.; Hediger, M.; Jones, A.K.; Kasai, S.; Leichter, C.A.; et al. Genome of the house fly, Musca domestica L., a global vector of diseases with adaptations to a septic environment. Genome Biol. 2014, 15, 466. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McTaggart, S.J.; Conlon, C.; Colbourne, J.K.; Blaxter, M.L.; Little, T.J. The components of the Daphnia pulex immune system as revealed by complete genome sequencing. BMC Genom. 2009, 10, 175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, S.; Zhu, S.; Jia, Q.; Yuan, D.; Ren, C.; Li, K.; Liu, S.; Cui, Y.; Zhao, H.; Cao, Y.; et al. The genomic and functional landscapes of developmental plasticity in the American cockroach. Nat. Commun. 2018, 9, 1008. [Google Scholar] [CrossRef] [PubMed]
- Zhan, S.; Fang, G.; Cai, M.; Kou, Z.; Xu, J.; Cao, Y.; Bai, L.; Zhang, Y.; Jiang, Y.; Luo, X.; et al. Genomic landscape and genetic manipulation of the black soldier fly Hermetia illucens, a natural waste recycler. Cell Res. 2020, 30, 50–60. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H.; Min, J.S.; Kang, J.S.; Kwon, D.H.; Yoon, K.S.; Strycharz, J.; Koh, Y.H.; Pittendrigh, B.R.; Clark, J.M.; Lee, S.H. Comparison of the humoral and cellular immune responses between body and head lice following bacterial challenge. Insect Biochem. Mol. Biol. 2011, 41, 332–339. [Google Scholar] [CrossRef] [PubMed]
- Gerardo, N.M.; Altincicek, B.; Anselme, C.; Atamian, H.; Barribeau, S.M.; de Vos, M.; Duncan, E.J.; Evans, J.D.; Gabaldon, T.; Ghanim, M.; et al. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 2010, 11, R21. [Google Scholar] [CrossRef] [PubMed]
- Allen, H.E.; Charlotte, J.K.; Alberto, M.C. Evolutionary Ecology of Figs and Their Associates: Recent Progress and Outstanding Puzzles. Annu. Rev. Ecol. Evol. Syst. 2008, 39, 439–458. [Google Scholar] [CrossRef] [Green Version]
- Peters, R.S.; Niehuis, O.; Gunkel, S.; Bläser, M.; Mayer, C.; Podsiadlowski, L.; Kozlov, A.; Donath, A.; van Noort, S.; Liu, S.; et al. Transcriptome sequence-based phylogeny of chalcidoid wasps (Hymenoptera: Chalcidoidea) reveals a history of rapid radiations, convergence, and evolutionary success. Mol. Phylogenet. Evol. 2018, 120, 286–296. [Google Scholar] [CrossRef] [PubMed]
- Hou, H.X.; Guo, M.Y.; Geng, J.; Wei, X.Q.; Huang, D.W.; Xiao, J.H. Genome-Wide Analysis of Peptidoglycan Recognition Protein Genes in Fig Wasps (Hymenoptera, Chalcidoidea). Insects 2020, 11, 597. [Google Scholar] [CrossRef] [PubMed]
- Xiao, J.; Wei, X.; Zhou, Y.; Xin, Z.; Miao, Y.; Hou, H.; Li, J.; Zhao, D.; Liu, J.; Chen, R.; et al. Genomes of 12 fig wasps provide insights into the adaptation of pollinators to fig syconia. J. Genet. Genom. 2021, 48, 225–236. [Google Scholar] [CrossRef] [PubMed]
- Katoh, K.; Misawa, K.; Kuma, K.; Miyata, T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002, 30, 3059–3066. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, L.T.; Schmidt, H.A.; von Haeseler, A.; Minh, B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef]
- De Bie, T.; Cristianini, N.; Demuth, J.P.; Hahn, M.W. CAFE: A computational tool for the study of gene family evolution. Bioinformatics 2006, 22, 1269–1271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gu, X.; Velden, K.V. DIVERGE: Phylogeny-based analysis for functional-structural divergence of a protein family. Bioinformatics 2002, 18, 500–501. [Google Scholar] [CrossRef]
- Gu, X.; Zou, Y.; Su, Z.; Huang, W.; Zhou, Z.; Arendsee, Z.; Zeng, Y. An update of DIVERGE software for functional divergence analysis of protein family. Mol. Biol. Evol. 2013, 30, 1713–1719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef] [PubMed]
- Pees, B.; Yang, W.; Zárate-Potes, A.; Schulenburg, H.; Dierking, K. High Innate Immune Specificity through Diversified C-Type Lectin-Like Domain Proteins in Invertebrates. J. Innate Immun. 2016, 8, 129–142. [Google Scholar] [CrossRef]
- Dodd, R.B.; Drickamer, K. Lectin-like proteins in model organisms: Implications for evolution of carbohydrate-binding activity. Glycobiology 2001, 11, 71r–79r. [Google Scholar] [CrossRef] [Green Version]
- Furukawa, A.; Kamishikiryo, J.; Mori, D.; Toyonaga, K.; Okabe, Y.; Toji, A.; Kanda, R.; Miyake, Y.; Ose, T.; Yamasaki, S.; et al. Structural analysis for glycolipid recognition by the C-type lectins Mincle and MCL. Proc. Natl. Acad. Sci. USA 2013, 110, 17438–17443. [Google Scholar] [CrossRef] [Green Version]
- Canton, J.; Neculai, D.; Grinstein, S. Scavenger receptors in homeostasis and immunity. Nat. Rev. Immunol. 2013, 13, 621–634. [Google Scholar] [CrossRef] [PubMed]
- Hanington, P.C.; Zhang, S.M. The primary role of fibrinogen-related proteins in invertebrates is defense, not coagulation. J. Innate Immun. 2011, 3, 17–27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adema, C.M.; Hertel, L.A.; Miller, R.D.; Loker, E.S. A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc. Natl. Acad. Sci. USA 1997, 94, 8691–8696. [Google Scholar] [CrossRef] [Green Version]
- Pace, K.E.; Baum, L.G. Insect galectins: Roles in immunity and development. Glycoconj. J. 2002, 19, 607–614. [Google Scholar] [CrossRef] [PubMed]
- Xia, X.; Yu, L.; Xue, M.; Yu, X.; Vasseur, L.; Gurr, G.M.; Baxter, S.W.; Lin, H.; Lin, J.; You, M. Genome-wide characterization and expression profiling of immune genes in the diamondback moth, Plutella xylostella (L.). Sci. Rep. 2015, 5, 9877. [Google Scholar] [CrossRef] [PubMed]
- Pang, X.; Xiao, X.; Liu, Y.; Zhang, R.; Liu, J.; Liu, Q.; Wang, P.; Cheng, G. Mosquito C-type lectins maintain gut microbiome homeostasis. Nat. Microbiol. 2016, 1, 16023. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, P.; Zhuo, X.R.; Tang, L.; Liu, X.S.; Wang, Y.F.; Wang, G.X.; Yu, X.Q.; Wang, J.L. C-type lectin interacting with β-integrin enhances hemocytic encapsulation in the cotton bollworm, Helicoverpa armigera. Insect Biochem. Mol. Biol. 2017, 86, 29–40. [Google Scholar] [CrossRef] [PubMed]
- Ao, J.; Ling, E.; Yu, X.Q. Drosophila C-type lectins enhance cellular encapsulation. Mol. Immunol. 2007, 44, 2541–2548. [Google Scholar] [CrossRef] [Green Version]
- Zumaya-Estrada, F.A.; Martínez-Barnetche, J.; Lavore, A.; Rivera-Pomar, R.; Rodríguez, M.H. Comparative genomics analysis of triatomines reveals common first line and inducible immunity-related genes and the absence of Imd canonical components among hemimetabolous arthropods. Parasites Vectors 2018, 11, 48. [Google Scholar] [CrossRef]
- Wang, J.; Song, X.; Wang, M. Peptidoglycan recognition proteins in hematophagous arthropods. Dev. Comp. Immunol. 2018, 83, 89–95. [Google Scholar] [CrossRef]
Group | Species | PGRP * | GNBP | CTL | SCRB | FREP | Galectin | TEP |
---|---|---|---|---|---|---|---|---|
Pollinators | Kradibia gibbosae | 4 | 0 | 15 | 10 | 1 | 3 | 2 |
Ceratosolen fusciceps | 6 | 0 | 23 | 10 | 1 | 3 | 3 | |
Ceratosolen solmsi | 6 | 0 | 17 | 10 | 1 | 3 | 3 | |
Dolichoris vasculosae | 5 | 0 | 20 | 11 | 1 | 3 | 3 | |
Eupristina koningsbergeri | 2 | 0 | 25 | 10 | 3 | 3 | 4 | |
Platyscapa corneri | 4 | 0 | 24 | 12 | 1 | 3 | 3 | |
Wiebesia pumilae | 5 | 0 | 19 | 10 | 1 | 3 | 3 | |
Non-pollinators | Apocrypta bakeri | 11 | 2 | 21 | 11 | 1 | 3 | 3 |
Philotrypesis tridentate | 10 | 2 | 27 | 11 | 1 | 3 | 3 | |
Sycophaga agraensis | 6 | 2 | 15 | 11 | 1 | 3 | 3 | |
Sycobia sp.2 | 7 | 2 | 18 | 11 | 2 | 3 | 3 | |
Sycophila sp.2 | 13 | 2 | 26 | 11 | 1 | 3 | 4 | |
Reference species | Pteromalus puparum | 9 | 2 | 26 | 12 | 1 | 3 | 3 |
Nasonia vitripennis | 11 | 3 | 31 | 11 | 1 | 4 | 3 | |
Apis mellifera | 4 | 2 | 12 | 10 | 1 | 3 | 3 | |
Drosophila melanogaster | 13 | 3 | 34 | 13 | 13 | 6 | 6 |
Group | Species | Gene Name | Number | Binding Site | Sugar |
---|---|---|---|---|---|
Pollinators | Ceratosolen fusciceps | Cfus_CTL-5/6/7/11/20/22 | 6 | QPD | galactose |
Cfus_CTL-8/12/17/18/19 | 5 | EPN | mannose | ||
Ceratosolen solmsi | Csol_CTL-5/7/9/16 | 4 | QPD | galactose | |
Csol_CTL-15 | 1 | EPN | mannose | ||
Dolichoris vasculosae | Dvas_CTL-1/4/10/11/14 | 5 | QPD | galactose | |
Dvas_CTL-3 | 1 | EPN | mannose | ||
Eupristina koningsbergeri | Ekon_CTL-1/7/12/14/19/20/23 | 7 | QPD | galactose | |
Ekon_CTL-6/17 | 2 | EPN | mannose | ||
Kradibia gibbosae | Kgib_CTL-2/8/11/12 | 4 | QPD | galactose | |
Kgib_CTL-6 | 1 | EPN | mannose | ||
Platyscapa corneri | Pcor_CTL-2/11/17/19/21 | 5 | QPD | galactose | |
Pcor_CTL-6/7/14/15/18 | 5 | EPN | mannose | ||
Wiebesia pumilae | Wpum_CTL-1/4/7/9/11/17 | 6 | QPD | galactose | |
Wpum_CTL-2/8 | 2 | EPN | mannose | ||
Non-pollinators | Apocrypta bakeri | Abak_CTL-4/5/6/7/8/10/11 | 7 | QPD | galactose |
Abak_CTL-9 | 1 | EPN | mannose | ||
Philotrypesis tridentata | Ptri_CTL-4/15/18(2)/19/22/24/25 | 7 | QPD | galactose | |
Ptri_CTL-7/10 | 2 | EPN | mannose | ||
Sycophaga agraensis | Sagr_CTL-3/6/10/11 | 4 | QPD | galactose | |
Sagr_CTL-8/14/15 | 3 | EPN | mannose | ||
Sycobia sp.2 | Sbsp_CTL-3/13 | 2 | QPD | galactose | |
Sbsp_CTL-7/9/16 | 3 | EPN | mannose | ||
Sycophila sp.2 | Spsp_CTL-1/6/9/11/12/14/15/16 | 8 | QPD | galactose | |
Spsp_CTL-2/10/13/23 | 4 | EPN | mannose |
Clade | MFE θ | MLE θ | MFE Z Score | p-Value |
---|---|---|---|---|
clade 1/ clade 2 | 1.15 ± 0.226 | 1.03 ± 0.130 | −6.266417 | <0.01 |
clade 1/ clade 3 | 1.03 ± 0.212 | 0.9992 ± 0.125 | −6.603005 | <0.01 |
clade 2/ clade 3 | 0.99 ± 0.221 | 0.9992 ± 0.146 | −5.908382 | <0.01 |
Clade | MFE θ | MLE θ | MFE Z Score | p-Value |
---|---|---|---|---|
clade 1/clade 2 | 0.7826 ± 0.0956 | 0.6256 ± 0.0594 | −10.343277 | <0.01 |
clade 1/clade 3 | 0.7619 ± 0.0938 | 0.5832 ± 0.0717 | −10.363998 | <0.01 |
clade 2/clade 3 | 0.6499 ± 0.0966 | 0.596 ± 0.0757 | −8.29982 | <0.01 |
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Hou, H.-X.; Huang, D.-W.; Xin, Z.-Z.; Xiao, J.-H. Genome-Wide Analysis of Gene Families of Pattern Recognition Receptors in Fig Wasps (Hymenoptera, Chalcidoidea). Genes 2021, 12, 1952. https://0-doi-org.brum.beds.ac.uk/10.3390/genes12121952
Hou H-X, Huang D-W, Xin Z-Z, Xiao J-H. Genome-Wide Analysis of Gene Families of Pattern Recognition Receptors in Fig Wasps (Hymenoptera, Chalcidoidea). Genes. 2021; 12(12):1952. https://0-doi-org.brum.beds.ac.uk/10.3390/genes12121952
Chicago/Turabian StyleHou, Hong-Xia, Da-Wei Huang, Zhao-Zhe Xin, and Jin-Hua Xiao. 2021. "Genome-Wide Analysis of Gene Families of Pattern Recognition Receptors in Fig Wasps (Hymenoptera, Chalcidoidea)" Genes 12, no. 12: 1952. https://0-doi-org.brum.beds.ac.uk/10.3390/genes12121952