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Numerous peptidoglycan recognition protein genes expressed in the bacteriome of the green rice leafhopper Nephotettix cincticeps (Hemiptera, Cicadellidae)

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Abstract

Peptidoglycan recognition proteins (PGRPs) contribute to the immune response of vertebrates and higher invertebrates. Animals have a varying number of PGRP genes: 4 in human and mouse, 13 in Drosophila, and 0 in an aphid. Transcriptome analyses revealed that numerous PGRP genes (> 300 in an RNA-Seq analysis) were expressed in the green rice leafhopper Nephotettix cincticeps (Uhler) (Hemiptera, Cicadellidae). PGRP genes were mostly expressed in the bacteriomes, in which two bacterial endosymbionts, Sulcia and Nasuia, are harbored. E. coli inoculation upregulated antimicrobial peptide gene expression in the leafhopper, whereas PGRP gene expression was not affected by the bacterial challenge. High and constant expression of PGRP genes in the bacteriomes and the lack of an immune response against invading bacteria suggest that these PGRPs play a hitherto unknown role in the bacteriomes, implicating a relationship with symbiotic association in N. cincticeps.

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References

  • Anselme C, Vallier A, Balmand S, Fauvarque MO, Heddi A (2006) Host PGRP gene expression and bacterial release in endosymbiosis of the weevil Sitophilus zeamais. Appl Environ Microb 72:6766–6772

    CAS  Google Scholar 

  • Anselme C, Perez-Brocal V, Vallier A, Vincent-Monegat C, Charif D, Latorre A, Moya A, Heddi A (2008) Identification of the weevil immune genes and their expression in the bacteriome tissue. BMC Biol 6:43

    PubMed  PubMed Central  Google Scholar 

  • Bao YY, Qu LY, Zhao D, Chen LB, Jin HY, Xu LM, Cheng JA, Zhang CX (2013) The genome- and transcriptome-wide analysis of innate immunity in the brown planthopper Nilaparvata lugens. BMC Genom 14:160

    CAS  Google Scholar 

  • Bennett GM, Moran NA (2013) Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol Evol 5:1675–1688

    PubMed  PubMed Central  Google Scholar 

  • Bing X, Attardo GM, Vigneron A, Aksoy E, Scolari F, Malacrida A, Weiss BL, Aksoy S (2017) Unravelling the relationship between the tsetse fly and its obligate symbiont Wigglesworthia: transcriptomic and metabolomic landscapes reveal highly integrated physiological networks. Proc Biol Sci 284:20170360

    PubMed  PubMed Central  Google Scholar 

  • Bischoff V, Vignal C, Boneca IG, Michel T, Hoffmann JA, Royet J (2004) Function of the drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nat Immunol 5:1175–1180

    CAS  PubMed  Google Scholar 

  • Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, Royet J (2006) Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog 2:e14 139–e14 147

    Google Scholar 

  • Boneca IG (2009) Mammalian PGRPs in the spotlight. Cell Host Microbe 5:109–111

    CAS  PubMed  Google Scholar 

  • Cheng XD, Zhang X, Pflugrath JW, Studier FW (1994) The Structure of bacteriophage-T7 lysozyme, a zinc amidase and an inhibitor of T7 RNA-polymerase. Proc Natl Acad Sci USA 91:4034–4038

    CAS  PubMed  Google Scholar 

  • Choe KM, Werner T, Stoven S, Hultmark D, Anderson KV (2002) Requirement for a peptidoglycan recognition protein (PGRP) in relish activation and antibacterial immune responses in Drosophila. Science 296:359–362

    CAS  PubMed  Google Scholar 

  • Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, Hetru C, Hoa NT, Hoffmann JA, Kanzok SM, Letunic I, Levashina EA, Loukeris TG, Lycett G, Meister S, Michel K, Moita LF, Muller HM, Osta MA, Paskewitz SM, Reichhart JM, Rzhetsky A, Troxler L, Vernick KD, Vlachou D, Volz J, Von Mering C, Xu JN, Zheng LB, Bork P, Kafatos FC (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298:159–165

    CAS  PubMed  Google Scholar 

  • Dziarski R (2004) Peptidoglycan recognition proteins (PGRPs). Mol Immunol 40:877–886

    CAS  PubMed  Google Scholar 

  • Dziarski R, Gupta D (2006) The peptidoglycan recognition proteins (PGRPs). Genome Biol 7:232

    PubMed  PubMed Central  Google Scholar 

  • Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15:645–656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrandon D, Imler JL, Hetru C, Hoffmann JA (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7:862–874

    CAS  PubMed  Google Scholar 

  • Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, De Vos M, Duncan EJ, Evans JD, Gabaldon T, Ghanim M, Heddi A, Kaloshian I, Latorre A, Moya A, Nakabachi A, Parker BJ, Perez-Brocal V, Pignatelli M, Rahbe Y, Ramsey JS, Spragg CJ, Tamames J, Tamarit D, Tamborindeguy C, Vincent-Monegat C, Vilcinskas A (2010) Immunity and other defenses in pea aphids Acyrthosiphon pisum. Genome Biol 11:R21

    PubMed  PubMed Central  Google Scholar 

  • Gottar M, Gobert V, Michel T, Belvin M, Duyk G, Hoffmann JA, Ferrandon D, Royet J (2002) The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416:640–644

    CAS  PubMed  Google Scholar 

  • Guan RJ, Mariuzza RA (2007) Peptidoglycan recognition proteins of the innate immune system. Trends Microbiol 15:127–134

    CAS  PubMed  Google Scholar 

  • Heddi A, Vallier A, Anselme C, Xin H, Rahbe Y, Wackers F (2005) Molecular and cellular profiles of insect bacteriocytes: mutualism and harm at the initial evolutionary step of symbiogenesis. Cell Microbiol 7:293–305

    CAS  PubMed  Google Scholar 

  • Irving P, Troxler L, Heuer TS, Belvin M, Kopczynski C, Reichhart JM, Hoffmann JA, Hetru C (2001) A genome-wide analysis of immune responses in Drosophila. Proc Natl Acad Sci USA 98:15119–15124

    CAS  PubMed  Google Scholar 

  • Kimura I, Omura T (1988) Leafhopper cell cultures as a means for phytoreovirus research. Adv Dis Vector Res 5:111–135

    Google Scholar 

  • Kim MS, Byun MJ, Oh BH (2003) Crystal structure of peptidoglycan recognition protein LB from Drosophila melanogaster. Nat Immunol 4:787–793

    CAS  PubMed  Google Scholar 

  • Kurata S (2014) Peptidoglycan recognition proteins in Drosophila immunity. Dev Comp Immunol 42:36–41

    CAS  PubMed  Google Scholar 

  • Lee JH, Lee IH, Noda H, Mita K, Taniai K (2007) Verification of elicitor efficacy of lipopolysaccharides and peptidoglycans on antibacterial peptide gene expression in Bombyx mori. Insect Biochem Mol Biol 37:1338–1347

    CAS  Google Scholar 

  • Leulier F, Parquet C, Pili-Floury S, Ryu JH, Caroff M, Lee WJ, Mengin-Lecreulx D, Lemaitre B (2003) The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol 4:478–484

    CAS  PubMed  Google Scholar 

  • Maire J, Vincent-Monegat C, Balmand S, Vallier A, Herve M, Masson F, Parisot N, Vigneron A, Anselme C, Perrin J, Orlans J, Rahioui I, Da Silva P, Fauvarque MO, Mengin-Lecreulx D, Zaidman-Remy A, Heddi A (2019) Weevil pgrp-lb prevents endosymbiont TCT dissemination and chronic host systemic immune activation. Proc Natl Acad Sci USA 116:5623–5632

    CAS  PubMed  Google Scholar 

  • Mao M, Yang X, Bennett GM (2018) Evolution of host support for two ancient bacterial symbionts with differentially degraded genomes in a leafhopper host. Proc Natl Acad Sci USA 115:E11691–E11700

    CAS  PubMed  Google Scholar 

  • Mccutcheon JP (2010) The bacterial essence of tiny symbiont genomes. Curr Opin Microbiol 13:73–78

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mccutcheon JP, Moran NA (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA 104:19392–19397

    CAS  PubMed  Google Scholar 

  • Mccutcheon JP, Moran NA (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol Evol 2:708–718

    PubMed  PubMed Central  Google Scholar 

  • Mccutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10:13–26

    CAS  Google Scholar 

  • Mccutcheon JP, Mcdonald BR, Moran NA (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA 106:15394–15399

    CAS  PubMed  Google Scholar 

  • Mellroth P, Karlsson J, Steiner H (2003) A scavenger function for a Drosophila peptidoglycan recognition protein. J Biol Chem 278:7059–7064

    CAS  PubMed  Google Scholar 

  • Michel T, Reichhart JM, Hoffmann JA, Royet J (2001) Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414:756–759

    CAS  PubMed  Google Scholar 

  • Mitsuhashi J, Kono Y (1975) Intercellular microoganisms in green rice leafhopper, Nephotettix cincticeps Uhler (Hemiptera; Deltocephalidae). Appl Entomol Zool 10:1–9

    Google Scholar 

  • Montaño AM, Tsujino F, Takahata N, Satta Y (2011) Evolutionary origin of peptidoglycan recognition proteins in vertebrate innate immune system. BMC Evol Biol 11:79

    PubMed  PubMed Central  Google Scholar 

  • Nardon P, Grenier AM (1989) Endocytobiosis in coleoptera: Biological, biochemical, and genetic aspects. In: Schwemmler W, Gassner G (eds) Insect endocytobiosis: morphology, physiology, genetics, evolution. CRC Press Inc, Boca Raton, pp 175–216

    Google Scholar 

  • Nasu S (1965) Electron microscopic studies on transovarial passage of rice dwarf virus. Jpn J Appl Entomol Zool 9:225–237

    Google Scholar 

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Noda H, Koizumi Y, Zhang Q, Deng KJ (2001) Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem Mol Biol 31:727–737

    CAS  PubMed  Google Scholar 

  • Noda H, Kawai S, Koizumi Y, Matsui K, Zhang Q, Furukawa S, Shimomura M, Mita K (2008) Annotated ESTs from various tissues of the brown planthopper Nilaparvata lugens: a genomic resource for studying agricultural pests. BMC Genom 9:117

    Google Scholar 

  • Noda H, Watanabe K, Kawai S, Yukuhiro F, Miyoshi T, Tomizawa M, Koizumi Y, Nikoh N, Fukatsu T (2012) Bacteriome-associated endosymbionts of the green rice leafhopper Nephotettix cincticeps (Hemiptera: Cicadellidae). Appl Entomol Zool 47:217–225

    CAS  Google Scholar 

  • Parkinson J, Guiliano DB, Blaxter M (2002) Making sense of EST sequences by CLOBBing them. BMC Bioinform 3:31

    Google Scholar 

  • Persson C, Oldenvi S, Steiner H (2007) Peptidoglycan recognition protein LF: a negative regulator of Drosophila immunity. Insect Biochem Mol Biol 37:1309–1316

    CAS  PubMed  Google Scholar 

  • Rämet M, Manfruelli P, Pearson A, Mathey-Prevot B, RaB E (2002) Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E-coli. Nature 416:644–648

    PubMed  Google Scholar 

  • Royet J, Dziarski R (2007) Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 5:264–277

    CAS  PubMed  Google Scholar 

  • Royet J, Reichhart JM, Hoffmann JA (2005) Sensing and signaling during infection in Drosophila. Curr Opin Immunol 17:11–17

    CAS  PubMed  Google Scholar 

  • Royet J, Gupta D, Dziarski R (2011) Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nat Rev Immunol 11:837–851

    CAS  PubMed  Google Scholar 

  • Steiner H (2004) Peptidoglycan recognition proteins: on and off switches for innate immunity. Immunol Rev 198:83–96

    CAS  PubMed  Google Scholar 

  • Takehana A, Katsuyama T, Yano T, Oshima Y, Takada H, Aigaki T, Kurata S (2002) Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae. Proc Natl Acad Sci USA 99:13705–13710

    CAS  PubMed  Google Scholar 

  • Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K, Suzuki N, Yoshiyama M, Kaneko Y, Iwasaki T, Sunagawa T, Yamaji K, Asaoka A, Mita K, Yamakawa M (2008) A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 38:1087–1110

    CAS  PubMed  Google Scholar 

  • Troll JV, Adin DM, Wier AM, Paquette N, Silverman N, Goldman WE, Stadermann FJ, Stabb EV, Mcfall-Ngai MJ (2009) Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animal-bacterial symbiosis. Cell Microbiol 11:1114–1127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Troll JV, Bent EH, Pacquette N, Wier AM, Goldman WE, Silverman N, Mcfall-Ngai MJ (2010) Taming the symbiont for coexistence: a host PGRP neutralizes a bacterial symbiont toxin. Environ Microbiol 12:2190–2203

    CAS  PubMed  Google Scholar 

  • Vigneron A, Charif D, Vincent-Monegat C, Vallier A, Gavory F, Wincker P, Heddi A (2012) Host gene response to endosymbiont and pathogen in the cereal weevil Sitophilus oryzae. BMC Microbiol 12:S14

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JW, Aksoy S (2012) PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring. Proc Natl Acad Sci USA 109:10552–10557

    CAS  PubMed  Google Scholar 

  • Wang JW, Wu YN, Yang GX, Aksoy S (2009) Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc Natl Acad Sci USA 106:12133–12138

    CAS  PubMed  Google Scholar 

  • Watanabe K, Yukuhiro F, Matsuura Y, Fukatsu T, Noda H (2014) Intra-sperm vertical symbiont transmission. Proc Natl Acad Sci USA 111:7433–7437

    CAS  PubMed  Google Scholar 

  • Woyke T, Tighe D, Mavromatis K, Clum A, Copeland A, Schackwitz W, Lapidus A, Wu DY, Mccutcheon JP, Mcdonald BR, Moran NA, Bristow J, Cheng JF (2010) One bacterial cell, one complete genome. PLoS ONE 5:e10314

    PubMed  PubMed Central  Google Scholar 

  • Yano T, Kurata S (2011) Intracellular recognition of pathogens and autophagy as an innate immune host defence. J Biochem 150:143–149

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yano T, Mita S, Ohmori H, Oshima Y, Fujimoto Y, Ueda R, Takada H, Goldman WE, Fukase K, Silverman N, Yoshimori T, Kurata S (2008) Autophagic control of listeria through intracellular innate immune recognition in drosophila. Nat Immunol 9:908–916

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida H, Kinoshita K, Ashida M (1996) Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J Biol Chem 271:13854–13860

    CAS  PubMed  Google Scholar 

  • Zaidman-Remy A, Herve M, Poidevin M, Pili-Floury S, Kim MS, Blanot D, Oh BH, Ueda R, Mengin-Lecreulx D, Lemaitre B (2006) The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24:463–473

    CAS  PubMed  Google Scholar 

  • Zaidman-Remy A, Poidevin M, Herve M, Welchman DP, Paredes JC, Fahlander C, Steiner H, Mengin-Lecreulx D, Lemaitre B (2011) Drosophila immunity: analysis of PGRP-SB1 expression, enzymatic activity and function. PLoS ONE 6:e17231

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zou Z, Evans JD, Lu ZQ, Zhao PC, Williams M, Sumathipala N, Hetru C, Hultmark D, Jiang HB (2007) Comparative genomic analysis of the Tribolium immune system. Genome Biol 8:R177

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Y. Koizumi, J. Shiba, M. Ebihara, and Y. Matsumoto for EST analysis, M. Hattori for salivary gland sample preparation, K. Yamamoto and M. Shimomura for EST database construction, A. Jouraku for RNA-Seq, F. Yukuhiro for electron microscopy, T. Omura for provision of the leafhopper cell line, and K. Watanabe and H. Tanaka for their valuable suggestions.

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This work was supported by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-Oriented Industry (BRAIN) and by JSPS KAKENHI Grant Number 25292201.

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Correspondence to Hiroaki Noda.

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Yoshitaka Suetsugu: Deceased.

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Tomizawa, M., Nakamura, Y., Suetsugu, Y. et al. Numerous peptidoglycan recognition protein genes expressed in the bacteriome of the green rice leafhopper Nephotettix cincticeps (Hemiptera, Cicadellidae). Appl Entomol Zool 55, 259–269 (2020). https://doi.org/10.1007/s13355-020-00680-z

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