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Journal of Integrative Agriculture  2022, Vol. 21 Issue (10): 2973-2983    DOI: 10.1016/j.jia.2022.07.048
Special Issue: 线虫合辑Nematology
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
A fragment of a 70-kDa Heterodera glycines heat shock protein (HgHSP70) interacts with soybean cyst nematode-resistant protein GmSHMT08
LIU Zhi1, 2, ZHANG Liu-ping1, ZHAO Jie1, JIAN Jin-zhuo1, PENG Huan1, HUANG Wen-kun1KONG Ling-an1PENG De-liang1, LIU Shi-ming1

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 MARA–CABI joint laboratory for bio-safety, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China

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大豆孢囊线虫(SCN, Heterodera glycines)严重制约大豆生产。大豆抗线虫数量性状遗传位点Rhg4上的丝氨酸羟甲基转移酶编码基因(GmSHMT08)对大豆孢囊线虫有显著的抗性,但该基因如何介导了对大豆孢囊线虫的抗性机制仍不明晰,GmSHMT08能否与大豆孢囊线虫产生的蛋白发生互作仍不明确。本研究以GmSHMT08作为诱饵,通过酵母双杂交体系在线虫中筛选出了与GmSHMT08互作的一个热休克蛋白70片段(HgHSP70p)。通过GST pull-down和荧光双分子互补,进一步验证了HgHSP70p与GmSHMT08之间存在互作关系。本研究发现的HgHSP70基因可以作为关键候选基因,用于进一步探究GmSHMT08介导的对大豆孢囊线虫的抗性机制。


Soybean cyst nematode (SCN) Heterodera glycines is considered as the major constraint to soybean production.  GmSHMT08 at Rhg4 locus on chromosome 08, encoding a serine hydroxylmethyltransferase, is a major gene underlying resistance against Hglycines in Peking-type soybeans.  However, the molecular mechanism underpinning this resistance is less well characterized, and whether GmSHMT08 could interact with proteins in Hglycines remains unclear.  In this study, yeast two-hybrid screening was conducted using GmSHMT08 as a bait protein, and a fragment of a 70-kDa heat shock protein (HgHSP70) was screened from Hglycines that exhibited interaction with GmSHMT08.  This interaction was verified by both GST pull-down and bimolecular fluorescence complementation assays.  Our finding reveals HgHSP70 could be applied as a potential candidate gene for further exploring the mechanism on GmSHMT08-mediated resistance against SCN Hglycines.

Keywords:  soybean cyst nematode       Heterodera glycines       GmSHMT08       HgHSP70       interaction       resistance  
Received: 31 August 2021   Accepted: 09 March 2022

This study is supported by the National Natural Science Foundation of China (31972248) and the Agricultural Science and Technology Innovation Project of Chinese Academy of Agricultural Sciences, China (ASTIP-02-IPP-04). 

About author:  LIU Zhi, E-mail:; Correspondence LIU Shi-ming, E-mail:; PENG De-liang, E-mail:

Cite this article: 

LIU Zhi, ZHANG Liu-ping, ZHAO Jie, JIAN Jin-zhuo, PENG Huan, HUANG Wen-kun, KONG Ling-an, PENG De-liang, LIU Shi-ming. 2022. A fragment of a 70-kDa Heterodera glycines heat shock protein (HgHSP70) interacts with soybean cyst nematode-resistant protein GmSHMT08. Journal of Integrative Agriculture, 21(10): 2973-2983.

Allen T W, Bradley C A, Sisson A J, Byamukama E, Chilvers M I, Coker C M, Collins A A, Damicone J P, Dorrance A E, Dufault N S, Esker P D, Faske T R, Giesler L J, Grybauskas A P, Hershman D E, Hollier C A, Isakeit T, Jardine D J, Kelly H M, Kemerait R C, et al. 2017. Soybean yield loss estimates due to diseases in the United States and Ontario, Canada, from 2010 to 2014. Plant Health Progress, 18, 19–27.
Almagro Armenteros J J, Tsirigos K D, Sønderby C K, Petersen T N, Winther O, Brunak S, von Heijne G, Nielsen H. 2019. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nature Biotechnology, 37, 420–423.
Alvim F C, Carolino S M, Cascardo J C, Nunes C C, Martinez C A, Otoni W C, Fontes E P. 2001. Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiology, 126, 1042–1054.
Bauwe H, Kolukisaoglu U. 2003. Genetic manipulation of glycine decarboxylation. Journal of Experimental Botany, 54, 1523–1535.
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.
de Boer J M, Yan Y, Wang X, Smant G, Hussey R S, Davis E L, Baum T J. 1999. Developmental expression of secretory beta-1,4-endoglucanases in the subventral esophageal glands of Heterodera glycines. Molecular Plant–Microbe Interactions, 12, 663–669.
Daugaard M, Rohde M, Jäättelä M. 2007. The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Letters, 581, 3702–3710.
Duan Y, Chen L, Liu G, Li H, Wang X, Wang Y. 2011. The economic importance of plant pathogenic nematodes. In: Duan Y, ed., Plant Pathogenic Nematodes. Science Press, Beijing. pp. 1–2.
Endo B Y. 1964. Penetration and development of Heterodera glycines in soybean roots and related anatomical changes. Phytopathology, 54, 79–88.
Fei J, Wang Y S, Zhou Q, Gu J D. 2015. Cloning and expression analysis of HSP70 gene from mangrove plant Kandelia obovata under cold stress. Ecotoxicology, 24, 1677–1685.
Fernández-Fernández M R, Gragera M, Ochoa-Ibarrola L, Quintana-Gallardo L, Valpuesta J M. 2017. Hsp70 - A master regulator in protein degradation. FEBS Letters, 591, 2648–2660.
Gao B, Allen R, Maier T, Davis E L, Baum T J, Hussey R S. 2003. The parasitome of the phytonematode Heterodera glycines. Molecular Plant–Microbe Interaction, 16, 720–726.
Ge F Y, Zheng N, Zhang L P, Huang W K, Peng D L, Liu S M. 2018. Chemical mutagenesis and soybean mutants potential for identification of novel genes conferring resistance to soybean cyst nematode. Journal of Integrative Agriculture, 17, 2734–2744. 
Gillan V, Maitland K, McCormack G, Him N A, Devaney E. 2009. Functional genomics of hsp-90 in parasitic and free-living nematodes. International Journal for Parasitology, 39, 1071–1081.
Gorovits R, Moshe A, Ghanim M, Czosnek H. 2013. Recruitment of the host plant heat shock protein 70 by Tomato yellow leaf curl virus coat protein is required for virus infection. PLoS ONE, 8, e70280.
Guo M, Zhai Y F, Lu J P, Chai L, Chai W G, Gong Z H, Lu M H. 2014. Characterization of CaHsp70-1, a pepper heat-shock protein gene in response to heat stress and some regulation exogenous substances in Capsicum annuum L. International Journal of Molecular Sciences, 15, 19741–19759.
Hartl F U, Hayer-Hartl M. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science, 295, 1852–1858.
Hewezi T. 2015. Cellular signaling pathways and posttranslational modifications mediated by nematode effector proteins. Plant Physiology, 169, 1018–1026.
Hussey R S. 1989. Disease-inducing secretions of plant-parasitic nematodes. Annual Review of Phytopathology, 27, 123–141.
Jungkunz I, Link K, Vogel F, Voll L M, Sonnewald S, Sonnewald U. 2011. AtHsp70-15-deficient Arabidopsis plants are characterized by reduced growth, a constitutive cytosolic protein response and enhanced resistance to TuMV. The Plant Journal, 66, 983–995.
Juvale P S, Baum T J. 2018. “Cyst-ained” research into Heterodera parasitism. PLoS Pathogens, 14, e1006791. 
Kabani M, Martineau C N. 2008. Multiple hsp70 isoforms in the eukaryotic cytosol: Mere redundancy or functional specificity? Current Genomics, 9, 338–348. 
Koenning S R, Wrather J A. 2010. Suppression of soybean yield potential in the continental United States from plant diseases estimated from 2006 to 2009. Plant Health Progress, 11, doi: 10.1094/PHP-2010-1122-01-RS.
Koizumi S, Ohama N, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2014. Functional analysis of the Hikeshi-like protein and its interaction with HSP70 in Arabidopsis. Biochemical and Biophysical Research Communications, 450, 396–400.
Kyte J, Doolittle R F. 1982. A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology, 157, 105–132.
Lee S, Lee D W, Lee Y, Mayer U, Stierhof Y D, Lee S, Jürgens G, Hwang I. 2009. Heat shock protein cognate 70–4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. The Plant Cell, 21, 3984–4001.
Lindquist S. 1986. The heat-shock response. Annual Review of Biochemistry, 55, 1151–1191.
Lindquist S, Craig E A. 1988. The heat-shock proteins. Annual Review of Genetics, 22, 631–677.
Liu S, Kandoth P K, Warren S D, Yeckel G, Heinz R, Alden J, Yang C, Jamai A, El-Mellouki T, Juvale P S, Hill J, Baum T J, Cianzio S, Whitham S A, Korkin D, Mitchum M G, Meksem K. 2012. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature, 492, 256–260. 
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. 
Lourenço-Tessutti I T, Souza Junior J D, Martins-de-Sa D, Viana A A, Carneiro R M, Togawa R C, de Almeida-Engler J, Batista J A, Silva M C, Fragoso R R, Grossi-de-Sa M F. 2015. Knock-down of heat-shock protein 90 and isocitrate lyase gene expression reduced root-knot nematode reproduction. Phytopathology, 105, 628–637. 
de Luca F, Di Vito M, Fanelli E, Reyes A, Greco N, de Giorgi C. 2009. Characterization of the heat shock protein 90 gene in the plant parasitic nematode Meloidogyne artiellia and its expression as related to different developmental stages and temperature. Gene, 440, 16–22. 
Masonbrink R, Maier T R, Muppirala U, Seetharam A S, Lord E, Juvale P S, Schmutz J, Johnson N T, Korkin D, Mitchum M G, Mimee B, den Akker S E, Hudson M, Severin A J, Baum T J. 2019. The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes. BMC Genomics, 20, 119.
Matthews R G, Drummond J T. 1990. Providing one-carbon units for biological methylations: mechanistic studies on serine hydroxymethyltransferase, methylenetetrahydrofolate reductase, and methyltetrahydrofolate-homocysteine methyltransferase. Chemical Reviews, 90, 1275–1290. 
Mayer M P. 2005. Recruitment of Hsp70 chaperones: A crucial part of viral survival strategies. Reviews of Physiology, Biochemistry and Pharmacology, 153, 1–46.
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. The New Phytologist, 199, 879–894.
Nagy P D, Wang R Y, Pogany J, Hafren A, Makinen K. 2011. Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology, 411, 374–382.
Nakamoto H, Vígh L. 2007. The small heat shock proteins and their clients. Cellular and Molecular Life Sciences, 64, 294–306. 
Noon J B, Hewezi T, Maier T R, Simmons C, Wei J Z, Wu G, Llaca V, Deschamps S, Davis E L, Mitchum M G, Hussey R S, Baum T J. 2015. Eighteen new candidate effectors of the phytonematode Heterodera glycines produced specifically in the secretory esophageal gland cells during parasitism. Phytopathology, 105, 1362–1372.
Ohtsu M, Sato Y, Kurihara D, Suzaki T, Kawaguchi M, Maruyama D, Higashiyama T. 2017. Spatiotemporal deep imaging of syncytium induced by the soybean cyst nematode Heterodera glycines. Protoplasma, 254, 2107–2115.
Peng D, Jiang R, Peng H, Liu S. 2021. Soybean cyst nematodes: A destructive threat to soybean production in China. Phytopathology Research, 3, 19.
Rincker K, Cary T, Diers B W. 2017. Impact of soybean cyst nematode resistance on soybean yield. Crop Science, 57, 1373–1382.
Ristic Z, Gifford D J, Cass D D. 1991. Heat shock proteins in two lines of Zea mays L. that differ in drought and heat resistance. Plant Physiology, 97, 1430–1434.
Sarkar N K, Kundnani P, Grover A. 2013. Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones, 18, 427–437.
Schirch L. 1982. Serine hydroxymethyltransferase. Advances in Enzymology and Related Areas of Molecular Biology, 53, 83–112.
Schirch V, Szebenyi D M. 2005. Serine hydroxymethyltransferase revisited. Current Opinion in Chemical Biology, 9, 482–487.
Skantar A M, Carta L K. 2004. Molecular characterization and phylogenetic evaluation of the Hsp90 gene from selected nematodes. Journal of Nematology, 36, 466–480.
Tomanek L, Sanford E. 2003. Heat-shock protein 70 (Hsp70) as a biochemical stress indicator: an experimental field test in two congeneric intertidal gastropods (genus: Tegula). The Biological Bulletin, 205, 276–284.
Tompa P, Kovacs D. 2010. Intrinsically disordered chaperones in plants and animals. Biochemistry and Cell Biology, 88, 167–174.
Usman M G, Rafii M Y, Ismail M R, Malek M A, Latif M A. 2015. Expression of target gene Hsp70 and membrane stability determine heat tolerance in chili pepper. Journal of the American Society for Horticultural Science, 140, 144–150. 
Usman M G, Rafii M Y, Martini M Y, Yusuff O A, Ismail M R, Miah G. 2017. Molecular analysis of Hsp70 mechanisms in plants and their function in response to stress. Biotechnology and Genetic Engineering Review, 33, 26–39. 
Wang N, Peng H, Liu S M, Huang W K, Holgado R Liu-Clarke J H, Peng D L. 2019. Molecular characterization and functional analysis of two new lysozyme genes from soybean cyst nematode (Heterodera glycines). Journal of Integrative Agriculture, 18, 2806–2813.
Wang Y, Lin S, Song Q, Li K, Tao H, Huang J, Chen X, Que S, He H. 2014. Genome-wide identification of heat shock proteins (Hsps) and Hsp interactors in rice: Hsp70s as a case study. BMC Genomics, 5, 344. 
Werner I, Hinton D E. 2000. Spatial profiles of hsp70 proteins in Asian clam (Potamocorbula amurensis) in northern San Francisco Bay may be linked to natural rather than anthropogenic stressors. Marine Environmental Research, 50, 379–384.
Zhao J, Li L, Liu Q, Liu P, Li S, Yang D, Chen Y, Pagnotta S, Favery B, Abad P, Jian H. 2019. A MIF-like effector suppresses plant immunity and facilitates nematode parasitism by interacting with plant annexins. Journal of Experimental Botany, 70, 5943–5958.

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