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Heterodera schachtii glutathione peroxidase (HsGPx) is a parasitism protein

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The beet cyst nematode (Heterodera schachtii) is a specialized obligate biotroph that is considered a major threat to sugar beet production. After infection, H. schachtii induce massive physiological and molecular changes to plant cells and create sophisticated syncytial feeding sites. Nematode secretions called effectors govern all of these changes. Here, we identify one of these effectors, H. schachtii glutathione peroxidase (HsGPx), and provide evidence that HsGPx is involved in parasitism. In situ hybridization showed that HsGPx is specifically localized within esophageal glands of pre-parasitic second-stage juveniles (J2). We also showed that HsGPx is upregulated in the post-parasitic stages. Knocking down HsGPx in nematodes by host-induced gene silencing hampers nematode development and leads to smaller nematode size and smaller associated feeding sites in Arabidopsis. Therefore, HsGPx plays an important role in the interaction between the nematode and plant.

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  1. Ali S, Magne M, Chen S et al (2015) Analysis of putative apoplastic effectors from the nematode, Globodera rostochiensis, and identification of an Expansin-like protein that can induce and suppress host defenses. PLoS ONE 10:e0115042. https://doi.org/10.1371/journal.pone.0115042

  2. Bellafiore S, Shen Z, Rosso MN et al (2008) Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog 4:e1000192. https://doi.org/10.1371/journal.ppat.1000192

  3. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313X.1998.00343.x

  4. de Boer JM, Yan Y, Smant G et al (1998) In-situ Hybridization to Messenger RNA in Heterodera glycines. J Nematol 30:309–312

  5. Doyle EA, Lambert KN (2002) Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica. Mol Plant-Microbe Interact 15:549–556. https://doi.org/10.1094/Mpmi.2002.15.6.549

  6. Dubreuil G, Deleury E, Magliano M et al (2011) Peroxiredoxins from the plant parasitic root-knot nematode, Meloidogyne incognita, are required for successful development within the host. Int J Parasitol 41:385–396. https://doi.org/10.1016/j.ijpara.2010.10.008

  7. Foley RC, Gleason CA, Anderson JP et al (2013) Genetic and genomic analysis of Rhizoctonia solani interactions with arabidopsis; evidence of resistance mediated through NADPH oxidases. PLoS ONE 8:e56814. https://doi.org/10.1371/journal.pone.0056814

  8. Gleason C, Polzin F, Habash SS et al (2017) Identification of two Meloidogyne hapla genes and an investigation of their roles in the plant-nematode interaction. Mol Plant-Microbe Interact 30:101–112. https://doi.org/10.1094/MPMI-06-16-0107-R

  9. Habash SS, Radakovic ZS, Vankova R et al (2017a) Heterodera schachtii Tyrosinase-like protein—a novel nematode effector modulating plant hormone homeostasis. Sci Rep 7:6874. https://doi.org/10.1038/s41598-017-07269-7

  10. Habash SS, Sobczak M, Siddique S et al (2017b) Identification and characterization of a putative protein disulfide isomerase (HsPDI) as an alleged effector of Heterodera schachtii. Sci Rep 7:13536. https://doi.org/10.1038/s41598-017-13418-9

  11. Hamamouch N, Li C, Hewezi T et al (2012) The interaction of the novel 30C02 cyst nematode effector protein with a plant β-1,3-endoglucanase may suppress host defence to promote parasitism. J Exp Bot 63:3683–3696. https://doi.org/10.1093/jxb/ers058

  12. Huang K, Czymmek KJ, Caplan JL et al (2011) HYR1-mediated detoxification of reactive oxygen species is required for full virulence in the rice blast fungus. PLoS Pathog 7:e1001335. https://doi.org/10.1371/journal.ppat.1001335

  13. Jones JT, Reavy B, Smant G, Prior AE (2004) Glutathione peroxidases of the potato cyst nematode Globodera Rostochiensis. Gene 324:47–54. https://doi.org/10.1016/j.gene.2003.09.051

  14. Jones JT, Kumar A, Pylypenko LA et al (2009) Identification and functional characterization of effectors in expressed sequence tags from various life cycle stages of the potato cyst nematode Globodera pallida. Mol Plant Pathol 10:815–828. https://doi.org/10.1111/j.1364-3703.2009.00585.x

  15. Karimi M, Inzé D, Depicker A (2002) GATEWAY™ vectors for agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

  16. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. https://doi.org/10.1006/jmbi.2000.4315

  17. Lilley CJ, Maqbool A, Wu D et al (2018) Effector gene birth in plant parasitic nematodes: neofunctionalization of a housekeeping glutathione synthetase gene. PLoS Genet 14:e1007310. https://doi.org/10.1371/journal.pgen.1007310

  18. Lin B, Zhuo K, Chen S et al (2016) A novel nematode effector suppresses plant immunity by activating host reactive oxygen species-scavenging system. New Phytol 209:1159–1173. https://doi.org/10.1111/nph.13701

  19. Lozano-Torres JL, Wilbers RHP, Warmerdam S et al (2014) Apoplastic venom allergen-like proteins of cyst nematodes modulate the activation of basal plant innate immunity by cell surface receptors. PLoS Pathog 10:e1004569. https://doi.org/10.1371/journal.ppat.1004569

  20. Mitchum MG, Hussey RS, Baum TJ et al (2013) Nematode effector proteins: an emerging paradigm of parasitism. New Phytol 199:879–894

  21. Petersen TN, Brunak S, Von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

  22. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT – PCR. Nucleic Acids Res 29:16–21

  23. Robertson L, Robertson WM, Sobczak M et al (2000) Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Mol Biochem Parasitol 111:41–49. https://doi.org/10.1016/S0166-6851(00)00295-4

  24. Siddique S, Matera C, Radakovic ZS et al (2014) Host-pathogen interactions: parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Sci Signal 7:ra33. https://doi.org/10.1126/scisignal.2004777

  25. Siddique S, Radakovic ZS, De La Torre CM et al (2015) A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. Proc Natl Acad Sci 112:12669–12674. https://doi.org/10.1073/pnas.1503657112

  26. Sijmons PC, Grundler FMW, von Mende N et al (1991) Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J 1:245–254. https://doi.org/10.1111/j.1365-313X.1991.00245.x

  27. Steele AE (1965) The host range of the sugar beet nematode, Heterodera schachtii Schmidt. J ASSBT 13:574–603

  28. Waetzig GH, Sobczak M, Grundler FMW (1999) Localization of hydrogen peroxide during the defence response of Arabidopsis thaliana against the plant-parasitic nematode Heterodera glycines. Nematology 1:681–686. https://doi.org/10.1163/156854199508702

  29. Wang X, Meyers D, Yan Y et al (1999) In planta localization of a β-1,4-endoglucanase secreted by Heterodera glycines. Mol Plant-Microbe Interact 64:64–67. https://doi.org/10.1094/MPMI.1999.12.1.64

  30. Wang X, Allen R, Ding X et al (2001) Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol Plant Microbe Interact 14:536–544. https://doi.org/10.1094/MPMI.2001.14.4.536

  31. Williamson VM, Gleason CA (2003) Plant-nematode interactions. Curr Opin Plant Biol 6:327–333

  32. Wyss U, Zunke U (1986) Observations on the behaviour of second stage juveniles of Heterodera schachtii inside host roots. Rev Nematol 9:153–166

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Correspondence to Abdelnaser Elashry.

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This study was done in compliance with the ethical standards. Within this study, there is no experiment that was done on humans and the experiments that included the nematodes were done according to the ethical standards.

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Aharen, I., Habash, S.S., Gleason, C. et al. Heterodera schachtii glutathione peroxidase (HsGPx) is a parasitism protein. J Plant Dis Prot 127, 111–118 (2020). https://doi.org/10.1007/s41348-019-00256-2

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  • Heterodera schachtii
  • Glutathione peroxidase
  • In situ hybridization
  • Effectors
  • Parasitism
  • RNAi