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Special Issue:
线虫合辑Nematology
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| Molecular characterization and functional analysis of two new lysozyme genes from soybean cyst nematode (Heterodera glycines) |
WANG Ning1, PENG Huan1, LIU Shi-ming1, HUANG Wen-kun1, Ricardo Holgado2, Jihong Liu-Clarke2, PENG De-liang1 |
1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
2 NIBIO, Norwegian Institute of Bioeconomy Research, Pb 115, NO-1431 Ås, Norway |
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Abstract Soybean cyst nematode (SCN, Heterodera glycines (I.)) is one of the most important soil-borne pathogens for soybeans. In plant parasitic nematodes, including SCN, lysozyme plays important roles in the innate defense system. In this study, two new lysozyme genes (Hg-lys1 and Hg-lys2) from SCN were cloned and characterized. The in situ hybridization analyses indicated that the transcripts of both Hg-lys1 and Hg-lys2 accumulated in the intestine of SCN. The qRT-PCR analyses showed that both Hg-lys1 and Hg-lys2 were upregulated after SCN second stage juveniles (J2s) were exposed to the Gram-positive bacteria Bacillus thuringiensis, Bacillus subtilis or Staphylococcus aureus. Knockdown of the identified lysozyme genes by in vitro RNA interference caused a significant decrease in the survival rate of SCN. All of the obtained results indicate that lysozyme is very important in the defense system and survival of SCN.
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Received: 25 April 2019
Accepted:
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| Fund: This research was supported the Central Public-Interest Scientific Institution Basal Research Fund, China (Y2019GH03), the Special Fund for Agro-Scientific Research in the Public Interest of China (210503114), and SINOGRAIN II (CHN-17/0019): Technological Innovation to Support Environmentally-Friendly Food Production and Food Safety Under a Changing Climate-Opportunities and Challenges for Norway-China Cooperation. |
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Corresponding Authors:
Correspondence Peng De-liang, E-mail: pengdeliang@caas.cn
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| About author: WANG Ning, E-mail: 954502700@qq.com; |
Cite this article:
WANG Ning, PENG Huan, LIU Shi-ming, HUANG Wen-kun, Ricardo Holgado, Jihong Liu-Clarke, PENG De-liang.
2019.
Molecular characterization and functional analysis of two new lysozyme genes from soybean cyst nematode (Heterodera glycines). Journal of Integrative Agriculture, 18(12): 2806-2813.
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Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.
Bu X J. 2006. Comparison of the innate immune system between nematodes and fruit flies. Bulletin of Biology, 41, 11–12. (in Chinese)
de Boer J M, Yan Y, Smant G, Davis E L, Baum T J. 1998. In-situ hybridization to messenger RNA in Heterodera glycines. Journal of Nematology, 30, 309–312.
Claudia B, Daniel W, Michael H, Kerstin I, Michiels N K, Thomas R, May R C, Schulenburg H. 2011. Protist-type lysozymes of the nematode Caenorhabditis elegans contribute to resistance against pathogenic Bacillus thuringiensis. PLoS ONE, 6, e24619.
Ewbank J J. 2002. Tackling both sides of the host-pathogen equation with Caenorhabditis elegans. Microbes and Infection, 4, 247–256.
Fanelli E, Dileo C, Di Vito M, De Giorgi C. 2008. Inducible antibacterial defense in the plant parasitic nematode Meloidogyne artiellia. International Journal for Parasitology, 38, 609–615.
Gravato-Nobre M J, Vaz F, Filipe S, Chalmers R, Hodgkin J. 2016. The invertebrate lysozyme effector ILYS-3 is systemically activated in response to danger signals and confers antimicrobial protection in C. elegans. PLoS Pathogens, 12, e1005826.
Kawli T, Tan M W. 2008. Neuroendocrine signals modulate the innate immunity of Caenorhabditis elegans through insulin signaling. Nature Immunology, 9, 1415–1424.
Kurz C L, Ewbank J J. 2000. Caenorhabditis elegans for the study of host-pathogen interactions. Trends in Microbiology 8, 142–144.
Liu H, Wang J, Mao Y, Liu M, Niu S F, Qiao Y, Su Y J, Wang C Z, Zheng Z P. 2016. Identification and expression analysis of a new invertebrate lysozyme in Kuruma shrimp (Marsupenaeus japonicus). Fish & Shellfish Immunology, 49, 336–343.
Liu S M, Peng D L. 2016. New progress in the study of soybean nematode resistance in soybeans. Science China (Life Sciences), 46, 535–547. (in Chinese)
Lou S X, Mao D L. 1994. Research progress of lysozyme. Chinese Journal of Clinical Oncology, 21, 709–711.
Mallo G V, Kurz C L, Couillault C, Pujol N, Granjeaud S, Kohara Y, Ewbank J J. 2002. Inducible antibacterial defense system in C. elegans. Current Biology, 12, 1209–1214.
Marsh E K, van den Berg M C W, May R C. 2011. A two-gene balance regulates Salmonella typhimurium tolerance in the nematode Caenorhabditis elegans. PLoS ONE, 6, e16839.
Minagawa S, Hikima J I, Hirono I, Aoki T, Mori H. 2001. Expression of Japanese flounder c-type lysozyme cDNA in insect cells. Developmental & Comparative Immunology, 25, 439–445.
Nandakumar M, Tan M W. 2008. Gamma-linolenic and stearidonic acids are required for basal immunity in Caenorhabditis elegans through their effects on p38 MAP kinase activity. PLoS Genetics, 4, e1000273.
Nicholas H R, Hodgkin J. 2004. Responses to infection and possible recognition strategies in the innate immune system of Caenorhabditis elegans. Molecular Immunology, 41, 479–493.
Niu Q H, Huang X W, Tian B Y, Yang J K, Liu J, Zhang L, Zhang K Q. 2005. Bacillus sp. B16 kills nematodes with a serine protease identified as a pathogenic factor. Applied Microbiology and Biotechnology, 69, 722–730.
O’Rourke D, Baban D, Demidova M, Mott R, Hodgkin J. 2006. Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of
C. elegans with M. nematophilum. Genome Research, 16, 1005–1016.
Peng H, Peng D L, Huang W K. 2009. Cloning and sequence analysis of full-length cDNA of β-1,4-endoglucanase gene (Dd-eng-1b) from C. elegans. Journal of Agricultural Biotechnology, 17, 1035–1041. (in Chinese)
Petersen T N, Brunak S, Von H G, Nielsen H. 2011. SIGNALP 4.0: Discriminating signal peptides from transmembrane regions. Nature Methods, 8, 785–786.
Schulenburg H, Boehnisch C. 2008. Diversification and adaptive sequence evolution of Caenorhabditis lysozymes (Nematoda: Rhabditidae). BMC Evolutionary Biology, 8, 114.
Simonsen K T, Moller-Jensen J, Kristensen A R, Andersen J S, Riddle D L. 2011. Quantitative proteomics identifies ferritin in the innate immune response of C. elegans. Virulence, 2, 120–130.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
Tarr D E K. 2012. Distribution and characteristics of ABFs, cecropins, nemapores, and lysozymes in nematodes. Developmental & Comparative Immunology, 36, 502–520.
Urwin P E, Lilley C J, Atkinson H J. 2002. Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Molecular Plant-Microbe Interactions, 15, 747–752.
Wang G F, Peng D L, Gao B L, Huang W K, Kong L, Long H B, Jane H. 2014. Differentially expressed genes at different ages of soybean cyst nematode No.3 and No.4 physiological races. In: Proceeding of 2014 Academic Annual Meeting published by Chinese Society of Plant Pathology. China Agricultural Science and Technology Press, Beijing. p. 438. (in Chinese)
Wohlkönig A, Huet J, Looze Y, Wintjens R. 2010. Structural relationships in the lysozyme superfamily: Significant evidence for glycoside hydrolase signature motifs. PLoS ONE, 5, e15388.
Xia Y, Spence H J, Moore J, Heaney N, McDermott L, Cooper A, Kennedy M W. 2000. The ABA-1 allergen of Ascaris lumbricoides: Sequence polymorphism, stage and tissue-specific expression, lipid binding function, and protein biophysical properties. Parasitology, 120, 211–224.
Ye X, Gao F Y, Zheng Q M, Bai J J, Wang H, Lao H H, Jian Q. 2009. Cloning and characterization of the tiger shrimp lysozyme. Molecular Biology Reports, 36, 1239–1246.
Yu Y, Yu L, Zhao M, Zhang K, Wang S. 2012. Advances in the innate immune mechanism of C. elegans. Journal of Huainan Teachers College, 14, 27–29. (in Chinese)
Yue X, Liu B, Xue Q. 2011. An i-type lysozyme from the Asiatic hard clam Meretrix meretrix potentially functioning in host immunity. Fish & Shellfish Immunology, 30, 550–558.
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