Abstract
Aphelenchoides besseyi, the nematode agent of rice tip white disease, causes huge economic losses in almost all the rice-growing regions of the world. Glutathione peroxidase (GPx), an esophageal glands secretion protein, plays important roles in the parasitism, immune evasion, reproduction and pathogenesis of many plant-parasitic nematodes (PPNs). Therefore, GPx is a promising target for control A. besseyi. Here, the full-length sequence of the GPx gene from A. besseyi (AbGPx1) was cloned using the rapid amplification of cDNA ends method. The full-length 944 bp AbGPx1 sequence, which contains a 678 bp open reading frame, encodes a 225 amino acid protein. The deduced amino acid sequence of the AbGPxl shares highly homologous with other nematode GPxs, and showed the closest evolutionary relationship with DrGPx. In situ hybridization showed that AbGPx1 was constitutively expressed in the esophageal glands of A. besseyi, suggesting its potential roles in parasitism and reproduction. RNA interference (RNAi) was used to assess the functions of the AbGPx1 gene, and quantitative real-time PCR was used to monitor the RNAi effects. After treatment with dsRNA for 12 h, AbGPx1 expression levels and reproduction in the nematodes decreased compared with the same parameters in the control group; thus, the AbGPx1 gene is likely to be associated with the development, reproduction, and infection ability of A. besseyi. These findings may open new avenues towards nematode control.
Acknowledgments
This work was supported by the Special Fund for Forest-Scientific Research in the Public Interest (Grant No. 201304403-4), the Heilongjiang Province Natural Science Foundation of China (Grant NO. ZD201404) and the Fundamental Research Funds for the Central Universities ( Grant NO. 2572015AA09).
References
Andrisic L., Collinson E.J., Tehlivets O., Perak E., Zarkovic T., Dawes I.W., et al. 2015. Transcriptional and antioxidative responses to endogenous polyunsaturated fatty acid accumulation in yeast. Molecular and Cellular Biochemistry, 399, 27–37. 10.1007/s11010-014-2229-6Search in Google Scholar
Baldwin J.G., Nadler S.A., Adams B.J. 2004. Evolution of plant parasitism among nematodes. Annual Review of Phytopathology, 42, 83–105. 10.1146/annurev.phyto.42.012204.130804Search in Google Scholar
Bridge J., Jim L.S.(Eds) 2007. Plant Nematodes of Agricultural Importance-A Colour Handbook. Academic Press10.1201/b15142Search in Google Scholar
Bridge J., Luc M., Plowright R.A.(Eds) 1990. Nematode parasites of rice, Plant parasitic nematodes in subtropical andtropical agriculture. Oxford: CABI PublishingSearch in Google Scholar
Cheng X., Xiang Y., Xie H., Xu C.L., Xie T.F., Zhang C., Li Y. 2013. Molecular Characterization and Functions of Fatty Acid and Retinoid Binding Protein Gene (Ab-far-1) in Aphelenchoides besseyi. PloS One, 8, e66011. 10.1371/journal.pone.0066011Search in Google Scholar
Da Silva G.S. 1992. White tip and national rice production. Informe Agropecuario Belo Horizonte, 16, 57–59Search in Google Scholar
Davis E.L., Hussey R.S., Baum T.J. 2004. Getting to the roots of parasitism by nematodes. Trends in Parasitology, 20, 134–141. 10.1016/j.pt.2004.01.005Search in Google Scholar
De Boer J.M., Yan Y., Smant G., Davis E.L., Baum T.J. 1988. In-situ hybridization to messenger RNA in Heterodera glycines. The Journal of Nematology, 30, 309–312Search in Google Scholar
Dellagi A., Heilbron J., Avrova A.O., Montesano M., Palva E.T., Stewart H.E., et al. 2000. A potato gene encoding a WRKY-like transcription factor is induced in interactions with Erwinia carotovorasubsp. Atroseptica and Phytophthora infestansand is coregulated with class I endochitinase expression. Molecular Plant-Microbe Interactions, 13, 1092–1101. 10.1094/MPMI.2000.13.10.1092Search in Google Scholar
Ding X., Ye J., Wu X., Huang L., Zhu L., Lin S. 2015. Deep sequencing analyses of pine wood nematode Bursaphelenchus xylophilus microRNAs reveal distinct miRNA expression patterns during the pathological process of pine wilt disease. Gene, 555, 346–356. 10.1016/j.gene.2014.11.030Search in Google Scholar
Espada M., Silva A.C., Eves van den Akker S., Cock P.J., Mota M., Jones J.T. 2016. Identification and characterization of parasitism genes from the pinewood nematode Bursaphelenchus xylophilus reveals a multilayered detoxification strategy. Molecular Plant Pathology, 17, 286–295. 10.1111/mpp.12280Search in Google Scholar
Franklin M.T., Siddigi M.R. 1972. Aphelenchoides besseyi. CIH. Descriptions of plant-parasitic nematodes. UK: Common wealth Agricultural Bureaux Press, pp. 21–23Search in Google Scholar
Haegeman A., Elsen A., De Waele D., Gheysen G. 2010. Emerging molecular knowledge on Radopholus similis, an important nematode pest of banana. Molecular Plant Pathology, 11, 315–323. 10.1111/j.1364-3703.2010.00614.xSearch in Google Scholar
Henkle-Dührsen K., Kampkotter A. 2001. Antioxidant enzyme families in parasitic nematodes. Molecular and Biochemical Parasitology, 114, 129–142.10.1016/S0166-6851(01)00252-3Search in Google Scholar
Herbette S., Roeckel-Drevet P., Drevet J.R. 2007. Seleno-independent glutathione peroxidases, more than simple antioxidant scavengers. The FEBS Journal, 274, 2163–2180. 10.1111/j.1742-4658.2007.05774.xSearch in Google Scholar PubMed
Hoshino S., Togashi K. 2000. Effect of Water-Soaking and Air-Drying on Survival of Aphelenchoides besseyi in Oryza sativa Seeds. The Journal of Nematology, 32, 303–308Search in Google Scholar
Hussey R.S. 1989. Disease-inducing secretions of plant-parasitic nematodes. Annual Review of Phytopathology, 27, 123–141. 10.1146/annurev.py.27.090189.001011Search in Google Scholar
Jacob J., Vanholme B., Haegeman A., Gheysen G. 2007. Four transthyretin-like genes of the migratory plantparasitic nematode Radopholus similis members of an extensive nematode-specific family. Gene, 402, 9–19. 10.1016/j.gene.2007.07.015Search in Google Scholar PubMed
Jones J.T., Reavyb B., Smantc G., Prior A.E. 2004. Glutathione peroxidases of the potato cyst nematode Globodera Rostochiensis. Gene, 324, 47–5410.1016/j.gene.2003.09.051Search in Google Scholar PubMed
Lawson J.A., Rokach J., FitzGerald G.A. 1999. Isoprostanes formation, analysis and use as indices of lipid peroxidation in vivo. The Journal of Biological Chemistry, 274, 24441–24444. 10.1074/jbc.274.35.24441Search in Google Scholar PubMed
Li Z., Liu X., Chu Y., Wang Y., Zhang Q., Zhou X. 2011. Cloning and Characterization of a 2-Cys Peroxiredoxin in the Pine Wood Nematode, Bursaphelenchus xylophilus, a Putative Genetic Factor Facilitating the Infestation. International Journal of Biological Sciences, 7, 823–3610.7150/ijbs.7.823Search in Google Scholar PubMed PubMed Central
Lin M.S., Ding X.F., Wang Z.M., Hou F.M., Lin N. 2004. Description of Aphelenchoides besseyi from abnormal rice with ‘small grains and erect panicles’ symptom in China. Rice Science 12, 289–294Search in Google Scholar
Livak K.J., Schmittgen T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402–408. 10.1006/meth.2001.1262Search in Google Scholar PubMed
Maier T.R., Hewezi T., Peng J., Baum T.J. 2012. Isolation of Whole Esophageal Gland Cells from Plant-Parasitic Nematodes for Transcriptome Analyses and Effector Identification. Molecular Plant-Microbe Interactions, 26, 31–35. 10.1094/MPMI-05-12-0121-FISearch in Google Scholar PubMed
Mamiya Y. 1975. The life history of the pine wood nematode, Bursaphelenchus lignicolus. Japanese Journal of Nematology, 5, 16–25Search in Google Scholar
Matamoros M.A., Saiz A., Peñuelas M., Bustos-Sanmamed P., Mulet J.M., Barja M.V., et al. 2015. Function of glutathione peroxidases in legume root nodules. Journal of Experimental Botany, 66, 2979–2990. 10.1093/jxb/erv066Search in Google Scholar PubMed PubMed Central
McGawley E.C., Rush M.C., Hollis J.P. 1984. Occurrence of Aphelenchoides besseyi in Louisiana Rice Seed and Its Interaction with Sclerotium oryzae in Selected Cultivars. The Journal of Nematology, 16, 65–68Search in Google Scholar
Miramón P., Dunker C., Kasper L., Jcobsen I.D., Barz D., Kurzai O., Hube B. 2014. A family of glutathione peroxidases contributes to oxidative stress resistance in Candida albicans. Medical Mycology, 52, 223–239. 10.1093/mmy/myt021Search in Google Scholar PubMed
Mitchum M.G., Hussey R.S., Baum T.J., Wang X., Elling A.A., Wubben M., Davis E.L. 2013. Nematode effector proteins an emerging paradigm of parasitism. New Phytologist, 199, 879–894. 10.1111/nph.12323Search in Google Scholar
Pei Y.Y., Cheng X., Xu C.L., Yang Z.F., Xie H. 2016. Virulence of part populations of Aphelenchoides besseyi on rice in China. Chinese Journal of Rice Science, 26, 218–226Search in Google Scholar
Qiu X.W., Wu X.Q., Huang L., Ye J.R. 2016. Influence of Bxpel1 Gene Silencing by dsRNA Interference on the Development and Pathogenicity of the Pine Wood Nematode, Bursaphelenchus xylophilus. International Journal of Molecular Sciences, 17, 125. 10.3390/ijms17010125Search in Google Scholar
Reymond P., Farmer E.E. 1998. Jasmonate and salicyclate as global signals for defense gene expression. Current Opinion in Plant Biology, 1, 404–411. 10.1016/S1369-5266(98)80264-1Search in Google Scholar
Robertson L., Robertson W.M., Sobczak M., Bakker J., Tetaud E., Ariyanayagam M.R., et al. 2000. Cloning, expression and functional characterisation of a thioredoxin peroxidase from the potato cyst nematode Globodera rostochiensis. Molecular and Biochemical Parasitology, 111, 41–4910.1016/S0166-6851(00)00295-4Search in Google Scholar
Sakamoto T, Maebayashi K, Nakagawa Y, Imai H. 2014. Deletion of the four phospholipid hydroperoxide glutathione peroxidase genes accelerates aging in Caenorhabditis elegans. Genes to Cells, 19, 778–792. 10.1111/gtc.12175Search in Google Scholar
Selkirk M.E., Smith V.P., Thomas G.R., Gounaris K. 1998. Resistance of filarial nematode parasites to oxidative stress. International Journal for Parasitology, 28, 1315–133210.1016/S0020-7519(98)00107-6Search in Google Scholar
Smant G., Goverse A., Stokkermans J.P., DeBoer J.M., Pomp H.R., Zilverentant J.F., et al. 1997. Potato root diffusateinduced secretion of soluble, basic proteins originating from the subventral esophageal glands of potato cyst nematodes. Phytopathology, 87, 839–845. 10.1094/PHYTO.1997.87.8.839Search in Google Scholar PubMed
Sulston J., Hodgkin J. (Eds) 1988. Methods in the nematode Caenorhabditis elegans, New York: Cold Sring Harbor LaboratorySearch in Google Scholar
Sun W., Song X., Yan R. 2012. Cloning and characterization of a selenium-independent glutathione peroxidase (HC29) from adult Haemonchus contortus. Journal of Veterinary Medical Science, 13, 49–5810.4142/jvs.2012.13.1.49Search in Google Scholar PubMed PubMed Central
Urwin P.E., Lilley C.J., Atkinson H.J. 2002. Ingestion of Double-stranded RNA by pre parasitic juvenile cyst nematodes leads to RNA interference. Molecular Plant-Microbe Interactions, 15, 747–752. 10.1094/MPMI.2002.15.8.747Search in Google Scholar PubMed
Viglierchio D.R., Schmitt R.V. 1983. On the methodology of nematode extraction from field samples: baermann funnel modifications. The journal of Nematology, 15, 438–444Search in Google Scholar
Wang F., Li D., Wang Z., Dong A., Liu L., Wang B., Chen Q., Liu X. 2014. Transcriptomic analysis of the rice white tip nematode, Aphelenchoides besseyi (Nematoda: Aphelenchoididae). PLoS One, 9, e91591. 10.1371/journal.pone.0091591Search in Google Scholar PubMed PubMed Central
Xiang Y., Wu X.Q., Zhou A. D. 2015. Bacterial diversity and community structure in the pine wood nematode Bursaphelenchus xylophilus and B. mucronatus with different virulence by high-throughput sequencing of the 16S rDNA. PLoS One, 10, e0137386. 10.1371/journal.pone.0137386Search in Google Scholar PubMed PubMed Central
Zhang C., Xie H., Cheng X., Wang D.W., Li Y., Xu C.L., Huang X. 2015. Molecular identification and functional characterization of the fatty acid and retinoid-binding protein gene Rs-far-1 in the burrowing nematode Radopholus similis (Tylenchida: Pratylenchidae). PloS One, 10, e0118414. 10.1371/journal.pone.0118414Search in Google Scholar PubMed PubMed Central
Zhang C., Xie H., Xu C.L., Cheng X., Li K.M., Li Y. 2010. Differential expression of Rs-eng-1b in two populations of Radopholus similis (Tylenchida: Pratylecnchidae) and its relationship to pathogenicity. European Journal of Plant Pathology, 4, 899–910. 10.1007/s10658-012-0015-4Search in Google Scholar
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