Research Advances on the Functional Study of Host Resistance Genes to Heterodera glycines

doi:10.13560/j.cnki.biotech.bull.1985.2021-0627

Abstract

Abstract:

Soybean plays an essential role in China’s economy. China is currently the largest soybean consumer and importer in the world,and the number of imported soybeans is increasing year by year. Soybean cyst nematode disease is a significant disease threatening major soybean producing areas globally,causing more than one billion US dollars in economic losses worldwide every year. The control of this pathogen is challenging. The use of resistant varieties is the most economical and effective measures to control soybean cyst nematode disease. At present,with the excessive use of a single resistant variety,the races of soybean cyst nematode continue to evolve,leading to reduced resistance and threatening the safety of the soybean industry. With the development of modern biotechnology,many researchers have elucidated the resistances to soybean cyst nematode by means of genetics,transcriptomics,and protein function studies. This review,summarizes the resistance mechanism of known major resistant sites Rhg1and Rhg4 in soybean,as well as the relationship between vlicular transport,phytohormone pathway and the resistance to soybean cyst nematode,discusses the significance of related functional proteins for soybean resistance and possible issues in the future research direction,and prospects the further reaches in this field. This is conducive to fully exploring the potential resistance genes of soybeans,laying a theoretical foundation for the creation of new soybean germplasms resistant to soybean cyst nematode,and serving the safe development of China’s soybean industry.

Key words: soybean cyst nematode, resistance mechanism, phytohormones, Rhg1, Rhg4, interaction between plant parasitic nematode and host

HAN Shao-jie, ZHENG Jing-wu. Research Advances on the Functional Study of Host Resistance Genes to Heterodera glycines[J]. Biotechnology Bulletin, 2021, 37(7): 14-24.

Figures/Tables 1

References 70

[1]	Niblack TL, Lambert KN, Tylka GL. A model plant pathogen from the kingdom Animalia:Heterodera glycines, the soybean cyst nematode[J]. Annu Rev Phytopathol, 2006, 44(1):283-303. doi: 10.1146/annurev.phyto.43.040204.140218 URL
[2]	许艳丽, 王丽芳, 战丽莉. 大豆胞囊线虫病研究进展(续一)[J]. 大豆科技, 2010(1):21-24.
	Xu YL, Wang LF, Zhan LL. The research advances on soybean cyst nematodes(SCN)[J]. Soybean Sci Technol, 2010(1):21-24.
[3]	Bandara AY, Weerasooriya DK, Bradley CA, et al. Dissecting the economic impact of soybean diseases in the United States over two decades[J]. PLoS One, 2020, 15(4):e0231141. doi: 10.1371/journal.pone.0231141 URL
[4]	Wang D, Duan YX, Wang YY, et al. First report of soybean cyst nematode, Heterodera glycines, on soybean from Guangxi, Guizhou, and Jiangxi provinces, China[J]. Plant Dis, 2015, 99(6):893.
[5]	宋美静, 朱晓峰, 王东, 等. 我国大豆主产区大豆胞囊线虫群体分布及致病性分化研究[J]. 大豆科学, 2016, 35(4):630-636.
	Song MJ, Zhu XF, Wang D, et al. Population distribution and pathogenicity differentiation of soybean cyst nematode in main soybean production areas of China[J]. Soybean Sci, 2016, 35(4):630-636.
[6]	Li YH, Qi XT, Chang RZ, et al. Evaluation and utilization of soybean germplasm for resistance to cyst nematode in China[M]// Sudarić A. Soybean-Molecular aspects of breeding. Croatia:Poljoprivreda, 2011.
[7]	Jung C, Wyss U. New approaches to control plant parasitic nematodes[J]. Appl Microbiol Biotechnol, 1999, 51(4):439-446. doi: 10.1007/s002530051414 URL
[8]	孔祥超, 李红梅, 耿甜, 等. 大豆种质资源对大豆孢囊线虫3号和4号生理小种的抗性鉴定[J]. 植物保护, 2012, 38(1):146-150.
	Kong XC, Li HM, Geng T, et al. Resistance evaluation of soybean varieties and germplasms to the races No. 3 and No. 4 of soybean cyst nematode Heterodera glycines[J]. Plant Prot, 2012, 38(1):146-150.
[9]	刘世名, 彭德良. 大豆的孢囊线虫抗性研究新进展[J]. 中国科学:生命科学, 2016, 46(5):535-547.
	Liu SM, Peng DL. Recent progresses on soybean resistance to soybean cyst nematode[J]. Sci Sin:Vitae, 2016, 46(5):535-547. doi: 10.1360/N052016-00162 URL
[10]	石红利. 大豆孢囊线虫的生物学特性及诱导抗性研究[D]. 杭州:浙江大学, 2013.
	Shi HL. Biological characteristics and induced resistance to Heterodera glycines[D]. Hangzhou:Zhejiang University, 2013.
[11]	Hua C, Li CJ, Hu YF, et al. Identification of HG types of soybean cyst nematode Heterodera glycines and resistance screening on soybean genotypes in northeast China[J]. J Nematol, 2018, 50(1):41-50.
[12]	Chen JS, Zhou YY, Wang YY, et al. Characterization of virulence phenotypes of Heterodera glycines in Heilongjiang, northeast China[J]. Plant Dis, 2021. https://doi.org/10.1094/PDIS-04-20-0820-SR. doi: https://doi.org/10.1094/PDIS-04-20-0820-SR
[13]	Chowdhury IA, Yan GP, Plaisance A, et al. Characterization of virulence phenotypes of soybean cyst nematode(Heterodera glycines)populations in north Dakota[J]. Phytopathology, 2021. DOI: 10.1094/phyto-01-21-0031-r. doi: 10.1094/phyto-01-21-0031-r
[14]	Meinhardt C, Howland A, Ellersieck M, et al. Resistance gene pyramiding and rotation to combat widespread soybean cyst nematode virulence[J]. Plant Dis, 2021. https://doi.org/10.1094/PDIS-12-20-2556-RE. doi: https://doi.org/10.1094/PDIS-12-20-2556-RE
[15]	Melito S, Heuberger AL, Cook D, et al. A nematode demographics assay in transgenic roots reveals no significant impacts of the Rhg1 locus LRR-Kinase on soybean cyst nematode resistance[J]. BMC Plant Biol, 2010, 10:104. doi: 10.1186/1471-2229-10-104 pmid: 20529370
[16]	Liu X, Liu S, Jamai A, et al. Soybean cyst nematode resistance in soybean is independent of the Rhg4 locus LRR-RLK gene[J]. Funct Integr Genomics, 2011, 11(4):539-549. doi: 10.1007/s10142-011-0225-4 URL
[17]	Ithal N, Recknor J, Nettleton D, et al. Developmental transcript profiling of cyst nematode feeding cells in soybean roots[J]. Mol Plant Microbe Interactions®, 2007, 20(5):510-525.
[18]	Klink VP, Overall CC, Alkharouf NW, et al. A time-course comparative microarray analysis of an incompatible and compatible response by Glycine max(soybean)to Heterodera glycines(soybean cyst nematode)infection[J]. Planta, 2007, 226(6):1423-1447. doi: 10.1007/s00425-007-0581-4 URL
[19]	Klink VP, Overall CC, Alkharouf NW, et al. Laser capture microdissection(LCM)and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean(Glycine max)roots infected by the soybean cyst nematode(Heterodera glycines)[J]. Planta, 2007, 226(6):1389-1409. doi: 10.1007/s00425-007-0578-z URL
[20]	Kandoth PK, Ithal N, Recknor J, et al. The Soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates the expression of a large number of stress- and defense-related genes in degenerating feeding cells[J]. Plant Physiol, 2011, 155(4):1960-1975. doi: 10.1104/pp.110.167536 URL
[21]	Matsye PD, Kumar R, Hosseini P, et al. Mapping cell fate decisions that occur during soybean defense responses[J]. Plant Mol Biol, 2011, 77(4/5):513-528. doi: 10.1007/s11103-011-9828-3 URL
[22]	Tian B, Wang S, Todd TC, et al. Genome-wide identification of soybean microRNA responsive to soybean cyst nematodes infection by deep sequencing[J]. BMC Genomics, 2017, 18(1):572. doi: 10.1186/s12864-017-3963-4 pmid: 28768484
[23]	Jiang HP, Tian LZ, Bu FS, et al. RNA-seq-based identification of potential resistance genes against the soybean cyst nematode(Heterodera glycines)HG Type 1. 2. 3. 5. 7 in ‘Dongnong L-10’[J]. Physiol Mol Plant Pathol, 2021, 114:101627. doi: 10.1016/j.pmpp.2021.101627 URL
[24]	Ge FY, Zheng N, Zhang LP, et al. Chemical mutagenesis and soybean mutants potential for identification of novel genes conferring resistance to soybean cyst nematode[J]. J Integr Agric, 2018, 17(12):2734-2744. doi: 10.1016/S2095-3119(18)62105-7 URL
[25]	Liu S, Ge F, Huang W, et al. Effective identification of soybean candidate genes involved in resistance to soybean cyst nematode via direct whole genome re-sequencing of two segregating mutants[J]. Theor Appl Genet, 2019, 132(9):2677-2687. doi: 10.1007/s00122-019-03381-6 URL
[26]	Tylka G, Mullaney M. Soybean cyst nematode-resistant soybeans for Iowa. extension publication pm 1649[M]. Iowa state university extension, Ames, 2017.
[27]	Cook DE, Lee TG, Guo X, et al. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean[J]. Science, 2012, 338(6111):1206-1209. doi: 10.1126/science.1228746 URL
[28]	Cook DE, Bayless AM, Wang K, et al. Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode[J]. Plant Physiol, 2014, 165(2):630-647. doi: 10.1104/pp.114.235952 URL
[29]	Liu Y, Du H, Li P, et al. Pan-genome of wild and cultivated soybeans[J]. Cell, 2020, 182(1):162-176. e13.
[30]	Butler KJ, Chen SY, Smith JM, et al. Soybean resistance locus Rhg1 confers resistance to multiple cyst nematodes in diverse plant species[J]. Phytopathology, 2019, 109(12):2107-2115. doi: 10.1094/PHYTO-07-19-0225-R URL
[31]	Bayless AM, Smith JM, Song JQ, et al. Disease resistance through impairment of α-SNAP-NSF interaction and vesicular trafficking by soybean Rhg1[J]. PNAS, 2016, 113(47):E7375-E7382. doi: 10.1073/pnas.1610150113 URL
[32]	Liu SM, Kandoth PK, Lakhssassi N, et al. The soybean GmSNAP18 gene underlies two types of resistance to soybean cyst nematode[J]. Nat Commun, 2017, 8:14822. doi: 10.1038/ncomms14822 URL
[33]	Bayless AM, Zapotocny RW, Grunwald DJ, et al. An atypical N-ethylmaleimide sensitive factor enables the viability of nematode-resistant Rhg1 soybeans[J]. PNAS, 2018, 115(19):E4512-E4521. doi: 10.1073/pnas.1717070115 URL
[34]	Bayless AM, Zapotocny RW, Han S, et al. The rhg1-a(Rhg1 low-copy)nematode resistance source harbors a copia-family retrotransposon within the Rhg1-encoded α-SNAP gene[J]. Plant Direct, 2019, 3(8):e00164.
[35]	Lee TG, Kumar I, Diers BW, et al. Evolution and selection of Rhg1, a copy-number variant nematode-resistance locus[J]. Mol Ecol, 2015, 24(8):1774-1791. doi: 10.1111/mec.2015.24.issue-8 URL
[36]	Li YH, Shi XH, Li HH, et al. Dissecting the genetic basis of resistance to soybean cyst nematode combining linkage and association mapping[J]. Plant Genome, 2016, 9(2). DOI: 10. 3835/plantgenome2015. 04. 0020. doi: 10. 3835/plantgenome2015. 04. 0020
[37]	Lakhssassi N, Liu S, Bekal S, et al. Characterization of the Soluble NSF Attachment Protein gene family identifies two members involved in additive resistance to a plant pathogen[J]. Sci Rep, 2017, 7:45226. doi: 10.1038/srep45226 pmid: 28338077
[38]	Guo W, Zhang F, Bao AL, et al. The soybean Rhg1 amino acid transporter gene alters glutamate homeostasis and jasmonic acid-induced resistance to soybean cyst nematode[J]. Mol Plant Pathol, 2019, 20(2):270-286. doi: 10.1111/mpp.2019.20.issue-2 URL
[39]	Han SJ, Smith JM, Du YL, et al. The soybean Rhg1 amino acid transporter protein becomes abundant along the SCN penetration path and impacts ROS generation[J]. bioRxiv, 2020, DOI: 10. 1101/2020. 09. 01. 277814. doi: 10. 1101/2020. 09. 01. 277814
[40]	Chen X, Li S, Zhao XB, et al. Modulation of(Homo)glutathione metabolism and H₂O₂ accumulation during soybean cyst nematode infections in susceptible and resistant soybean cultivars[J]. Int J Mol Sci, 2020, 21(2):388. doi: 10.3390/ijms21020388 URL
[41]	Matson A L, Williams L F. Evidence of a fourt gene for resistance to the soybean cyst nematodde 1[J]. Crop Science, 1965, 5(5):477. doi: 10.2135/cropsci1965.0011183X000500050032x URL
[42]	Webb DM, Baltazar BM, Rao-Arelli AP, et al. Genetic mapping of soybean cyst nematode race-3 resistance loci in the soybean PI 437. 654[J]. Theor Appl Genet, 1995, 91(4):574-581. doi: 10.1007/BF00223282 pmid: 24169883
[43]	Yu N, Lee TG, Rosa DP, et al. Impact of Rhg1 copy number, type, and interaction with Rhg4 on resistance to Heterodera glycines in soybean[J]. TAG Theor Appl Genet Theor Und Angewandte Genet, 2016, 129(12):2403-2412.
[44]	Liu S, Kandoth PK, Warren SD, et al. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens[J]. Nature, 2012, 492(7428):256-260. doi: 10.1038/nature11651 URL
[45]	Kandoth PK, Liu S, Prenger E, et al. Systematic mutagenesis of serine hydroxymethyltransferase reveals an essential role in nematode resistance[J]. Plant Physiol, 2017, 175(3):1370-1380. doi: 10.1104/pp.17.00553 pmid: 28912378
[46]	Patil GB, Lakhssassi N, Wan J, et al. Whole-genome re-sequencing reveals the impact of the interaction of copy number variants of the rhg1 and Rhg4 genes on broad-based resistance to soybean cyst nematode[J]. Plant Biotechnol J, 2019, 17(8):1595-1611. doi: 10.1111/pbi.2019.17.issue-8 URL
[47]	Lakhssassi N, Piya S, Knizia D, et al. Mutations at the serine hydroxymethyltransferase impact its interaction with a soluble NSF attachment protein and a pathogenesis-related protein in soybean[J]. Vaccines, 2020, 8(3):349. doi: 10.3390/vaccines8030349 URL
[48]	Lakhssassi N, Piya S, Bekal S, et al. A pathogenesis-related protein GmPR08-Bet VI promotes a molecular interaction between the GmSHMT08 and GmSNAP18 in resistance to Heterodera glycines[J]. Plant Biotechnol J, 2020, 18(8):1810-1829. doi: 10.1111/pbi.13343 pmid: 31960590
[49]	Meksem K, Pantazopoulos P, Njiti VN, et al. ’Forrest’ resistance to the soybean cyst nematode is bigenic:saturation mapping of the Rhg1and Rhg4 loci[J]. Theor Appl Genet, 2001, 103(5):710-717. doi: 10.1007/s001220100597 URL
[50]	Hawes CR, Brandizzi F, Andreeva AV. Endomembranes and vesicle trafficking[J]. Curr Opin Plant Biol, 1999, 2(6):454-461. pmid: 10607657
[51]	Gu Y, Zavaliev R, Dong X. Membrane trafficking in plant immunity[J]. Mol Plant, 2017, 10(8):1026-1034. doi: 10.1016/j.molp.2017.07.001 URL
[52]	McNeece BT, Sharma K, Lawrence GW, et al. The mitogen activated protein kinase(MAPK)gene family functions as a cohort during the Glycine max defense response to Heterodera glycines[J]. Plant Physiol Biochem, 2019, 137:25-41. doi: 10.1016/j.plaphy.2019.01.018 URL
[53]	Klink VP, Sharma K, Pant SR, et al. Components of the SNARE-containing regulon are co-regulated in root cells undergoing defense[J]. Plant Signal Behav, 2017, 12(2):e1274481. doi: 10.1080/15592324.2016.1274481 URL
[54]	Sharma K, Niraula PM, Troell HA, et al. Exocyst components promote an incompatible interaction between Glycine max(soybean)and Heterodera glycines(the soybean cyst nematode)[J]. Sci Rep, 2020, 10(1):15003. doi: 10.1038/s41598-020-72126-z URL
[55]	Jahn R, Scheller RH. SNAREs——engines for membrane fusion[J]. Nat Rev Mol Cell Biol, 2006, 7(9):631-643. doi: 10.1038/nrm2002 URL
[56]	Pant SR, Matsye PD, McNeece BT, et al. Syntaxin 31 functions in Glycine max resistance to the plant parasitic nematode Heterodera glycines[J]. Plant Mol Biol, 2014, 85(1/2):107-121. doi: 10.1007/s11103-014-0172-2 URL
[57]	Sharma K, Pant SR, McNeece BT, et al. Co-regulation of the Glycine max soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor(SNARE)-containing regulon occurs during defense to a root pathogen[J]. J Plant Interact, 2016, 11(1):74-93. doi: 10.1080/17429145.2016.1195891 URL
[58]	Dong J, Zielinski RE, Hudson ME. T-SNAREs bind the Rhg1 α-SNAP and mediate soybean cyst nematode resistance[J]. Plant J, 2020, 104(2):318-331. doi: 10.1111/tpj.v104.2 URL
[59]	Lawaju BR, Niraula P, Lawrence GW, et al. The Glycine max conserved oligomeric Golgi(COG)complex functions during a defense response to Heterodera glycines[J]. Front Plant Sci, 2020, 11:564495. doi: 10.3389/fpls.2020.564495 URL
[60]	Hu YF, You J, Li CJ, et al. Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines[J]. Sci Rep, 2017, 7:41282. doi: 10.1038/srep41282 URL
[61]	Tucker ML, Xue P, Yang R. 1-Aminocyclopropane-1-carboxylic acid(ACC)concentration and ACC synthase expression in soybean roots, root tips, and soybean cyst nematode(Heterodera glycines)-infected roots[J]. J Exp Bot, 2010, 61(2):463-472. doi: 10.1093/jxb/erp317 pmid: 19861652
[62]	Mazarei M, Puthoff DP, Hart JK, et al. Identification and characterization of a soybean ethylene-responsive element-binding protein gene whose mRNA expression changes during soybean cyst nematode infection[J]. Mol Plant Microbe Interactions®, 2002, 15(6):577-586.
[63]	Mazarei M, Elling AA, Maier TR, et al. GmEREBP₁ is a transcription factor activating defense genes in soybean and Arabidopsis[J]. Mol Plant Microbe Interact, 2007, 20(2):107-119. doi: 10.1094/MPMI-20-2-0107 URL
[64]	Hermsmeier D, Mazarei M, Baum TJ. Differential display analysis of the early compatible interaction between soybean and the soybean cyst nematode[J]. Mol Plant Microbe Interactions, 1998, 11(12):1258-1263. doi: 10.1094/MPMI.1998.11.12.1258 URL
[65]	Lin JY, Mazarei M, Zhao N, et al. Overexpression of a soybean salicylic acid methyltransferase gene confers resistance to soybean cyst nematode[J]. Plant Biotechnol J, 2013, 11(9):1135-1145. doi: 10.1111/pbi.12108 URL
[66]	Guo XL, Chronis D, de la Torre CM, et al. Enhanced resistance to soybean cyst nematodeHeterodera glycinesin transgenic soybean by silencing putative CLE receptors[J]. Plant Biotechnol J, 2015, 13(6):801-810. doi: 10.1111/pbi.2015.13.issue-6 URL
[67]	Wang J, Dhroso A, Liu X, et al. Phytonematode peptide effectors exploit a host post-translational trafficking mechanism to the ER using a novel translocation signal[J]. New Phytol, 2021, 229(1):563-574. doi: 10.1111/nph.v229.1 URL
[68]	Lee MW, Huffaker A, Crippen D, et al. Plant elicitor peptides promote plant defences against nematodes in soybean[J]. Mol Plant Pathol, 2018, 19(4):858-869. doi: 10.1111/mpp.2018.19.issue-4 URL
[69]	Niraula PM, Zhang XF, Jeremic D, et al. Xyloglucan endotransglycosylase/hydrolase increases tightly-bound xyloglucan and chain number but decreases chain length contributing to the defense response that Glycine max has to Heterodera glycines[J]. PLoS One, 2021, 16(1):e0244305.
[70]	Ngaki MN, Sahoo DK, Wang B, et al. Overexpression of a plasma membrane protein generated broad-spectrum immunity in soybean[J]. Plant Biotechnol J, 2021, 19(3):502-516. doi: 10.1111/pbi.v19.3 URL