1932

Abstract

Resistance to the soybean cyst nematode (SCN) is a topic incorporating multiple mechanisms and multiple types of science. It is also a topic of substantial agricultural importance, as SCN is estimated to cause more yield damage than any other pathogen of soybean, one of the world's main food crops. Both soybean and SCN have experienced jumps in experimental tractability in the past decade, and significant advances have been made. The locus, deployed on millions of farm acres, has been durable and will remain important, but local SCN populations are gradually evolving to overcome . Multiple other SCN resistance quantitative trait loci (QTL) of proven value are now in play with soybean breeders. QTL causal gene discovery and mechanistic insights into SCN resistance are contributing to both basic and applied disciplines. Additional understanding of SCN and other cyst nematodes will also grow in importance and lead to novel disease control strategies.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-020620-120823
2022-08-26
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/phyto/60/1/annurev-phyto-020620-120823.html?itemId=/content/journals/10.1146/annurev-phyto-020620-120823&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Acharya K, Yan G, Plaisance A 2021. Effects of cover crops on population reduction of soybean cyst nematode (Heterodera glycines). Plant Dis 105:764–69
    [Google Scholar]
  2. 2.
    Ali MA, Azeem F, Abbas A, Joyia FA, Li H, Dababat AA. 2017. Transgenic strategies for enhancement of nematode resistance in plants. Front. Plant Sci. 8:750
    [Google Scholar]
  3. 3.
    Allen TW. 2017. Soybean yield loss estimates due to diseases in the United States and Ontario, Canada, from 2010 to 2014. Plant Health Prog 18:19–27
    [Google Scholar]
  4. 4.
    An QL, Ehlers K, Kogel KH, van Bel AJE, Huckelhoven R. 2006. Multivesicular compartments proliferate in susceptible and resistant MLA12 barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytol 172:563–76
    [Google Scholar]
  5. 5.
    Atkinson HJ, Lilley CJ, Urwin PE. 2012. Strategies for transgenic nematode control in developed and developing world crops. Curr. Opin. Biotechnol. 23:251–56
    [Google Scholar]
  6. 6.
    Bandara AY, Weerasooriya DK, Bradley CA, Allen TW, Esker PD 2020. Dissecting the economic impact of soybean diseases in the United States over two decades. PLOS ONE 15:e0231141
    [Google Scholar]
  7. 7.
    Basnet P, Meinhardt CG, Usovsky M, Gillman JD, Joshi T et al. 2022. Epistatic interaction between Rhg1-a and Rhg2 in PI 90763 confers resistance to virulent soybean cyst nematode populations. Theor. Appl. Genet. https://doi.org/10.1007/s00122-022-04091-2
    [Crossref] [Google Scholar]
  8. 8.
    Bayless AM, Smith JM, Song J, McMinn PH, Teillet A et al. 2016. Disease resistance through impairment of alpha-SNAP-NSF interaction and vesicular trafficking by soybean Rhg1. PNAS 113:E7375–E82
    [Google Scholar]
  9. 9.
    Bayless AM, Zapotocny RW, Grunwald DJ, Amundson KK, Diers BW, Bent AF. 2018. An atypical N-ethylmaleimide sensitive factor enables the viability of nematode-resistant Rhg1 soybeans. PNAS 115:E4512–E21
    [Google Scholar]
  10. 10.
    Bayless AM, Zapotocny RW, Han S, Grunwald DJ, Amundson KK, Bent AF. 2019. The rhg1-a (Rhg1 low-copy) nematode resistance source harbors a copia-family retrotransposon within the Rhg1-encoded α-SNAP gene. Plant Direct 3:e00164
    [Google Scholar]
  11. 11.
    Bekal S, Domier LL, Gonfa B, Lakhssassi N, Meksem K, Lambert KN. 2015. A SNARE-like protein and biotin are implicated in soybean cyst nematode virulence. PLOS ONE 10:e0145601
    [Google Scholar]
  12. 12.
    Bird G, Markell S, Bissonnette K, Bradley C, Johnston J et al. 2021. The SCN coalition: a public private partnership. J. Nematol. 53:4
    [Google Scholar]
  13. 13.
    Bissonnette KM, Marett CC, Mullaney MP, Gebhart GD, Kyveryga PM et al. 2020. Effects of ILeVO seed treatment on Heterodera glycines reproduction and soybean yield in small-plot and strip-trial experiments in Iowa. Plant Dis 104:2914–20
    [Google Scholar]
  14. 14.
    Boutrot F, Zipfel C. 2017. Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu. Rev. Phytopathol. 55:257–86
    [Google Scholar]
  15. 15.
    Brucker E, Carlson S, Wright E, Niblack T, Diers B. 2005. Rhg1 alleles from soybean PI 437654 and PI 88788 respond differentially to isolates of Heterodera glycines in the greenhouse. Theor. Appl. Genet. 111:44–49
    [Google Scholar]
  16. 16.
    Brzostowski LF, Diers BW. 2017. Pyramiding of alleles from multiple sources increases the resistance of soybean to highly virulent soybean cyst nematode isolates. Crop Sci. 57:2932–41
    [Google Scholar]
  17. 17.
    Butler KJ, Chen SY, Smith JM, Wang XH, Bent AF. 2019. Soybean resistance locus Rhg1 confers resistance to multiple cyst nematodes in diverse plant species. Phytopathology 109:2107–15
    [Google Scholar]
  18. 18.
    Butler KJ, Fliege C, Zapotocny R, Diers B, Hudson M, Bent AF. 2021. Soybean cyst nematode resistance quantitative trait locus cqSCN-006 alters the expression of a γ-SNAP protein. Mol. Plant-Microbe Interact. 34:121433–45
    [Google Scholar]
  19. 19.
    Caldwell BE, Brim C, Ross J 1960. Inheritance of resistance of soybeans to the cyst nematode, Heterodera glycines. Agron. J. 52:635–36
    [Google Scholar]
  20. 20.
    Chen GQ, Zhu LN, Yang JM, Zhang S, Li YH et al. 2021. Synthesis of novel 3/5(3,5)-(di)nitropaeonol hydrazone derivatives as nematicidal agents. J. Asian Nat. Prod. Res. 24:166–75
    [Google Scholar]
  21. 21.
    Chen J, Zhou Y, Wang Y, Fan H, Liu X et al. 2021. Characterization of virulence phenotypes of Heterodera glycines in Heilongjiang, Northeast China. Plant Dis. 105:2056–60
    [Google Scholar]
  22. 22.
    Chen SY. 2020. Dynamics of population density and virulence phenotype of the soybean cyst nematode as influenced by resistance source sequence and tillage. Plant Dis 104:2111–22
    [Google Scholar]
  23. 23.
    Chen X, Li S, Zhao X, Zhu X, Wang Y et al. 2020. Modulation of (homo)glutathione metabolism and H2O2 accumulation during soybean cyst nematode infections in susceptible and resistant soybean cultivars. Int. J. Mol. Sci. 21:2388
    [Google Scholar]
  24. 24.
    Chopra D, Hasan MS, Matera C, Chitambo O, Mendy B et al. 2021. Plant parasitic cyst nematodes redirect host indole metabolism via NADPH oxidase-mediated ROS to promote infection. New Phytol. 232:1318–31
    [Google Scholar]
  25. 25.
    Chowdhury IA, Yan G, Plaisance A, Markell S. 2021. Characterization of virulence phenotypes of soybean cyst nematode (Heterodera glycines) populations in North Dakota. Phytopathology 111:2100–9
    [Google Scholar]
  26. 26.
    Concibido VC, Diers BW, Arelli PR. 2004. A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci 44:1121–31
    [Google Scholar]
  27. 27.
    Cook DE, Bayless AM, Wang K, Guo X, Song Q et al. 2014. Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiol 165:630–47
    [Google Scholar]
  28. 28.
    Cook DE, Lee TG, Guo X, Melito S, Wang K et al. 2012. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–9
    [Google Scholar]
  29. 29.
    da Silveira DLM, Montecelli TD, da Silva GJ, Schuster I. 2019. SNP haplotypes for soybean resistance to SCN race 1 and 3. Euphytica 215:143
    [Google Scholar]
  30. 30.
    Davis EL, Hussey RS, Baum TJ. 2004. Getting to the roots of parasitism by nematodes. Trends Parasitol 20:134–41
    [Google Scholar]
  31. 31.
    Derevnina L, Contreras MP, Adachi H, Upson J, Vergara Cruces A et al. 2021. Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network. PLOS Biol 19:e3001136
    [Google Scholar]
  32. 32.
    Dick K, Samanfar B, Barnes B, Cober ER, Mimee B et al. 2020. PIPE4: fast PPI predictor for comprehensive inter- and cross-species interactomes. Sci. Rep. 10:1390
    [Google Scholar]
  33. 33.
    Dong J, Hudson ME. 2021. WI12Rhg1 interacts with DELLAs and mediates soybean cyst nematode resistance through hormone pathways. Plant Biotechnol. J. 20:2283–96
    [Google Scholar]
  34. 34.
    Dong J, Zielinski RE, Hudson ME. 2020. t-SNAREs bind the Rhg1 α-SNAP and mediate soybean cyst nematode resistance. Plant J 104:318–31
    [Google Scholar]
  35. 35.
    Endo BY. 1975. Pathogenesis of nematode-infected plants. Annu. Rev. Phytopathol. 13:213–38
    [Google Scholar]
  36. 36.
    Eves-van den Akker S. 2021. Plant-nematode interactions. Curr. Opin. Plant Biol. 62:102035
    [Google Scholar]
  37. 37.
    Eves-van den Akker S, Laetsch DR, Thorpe P, Lilley CJ, Danchin EGJ et al. 2016. The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence. Genome Biol 17:124
    [Google Scholar]
  38. 38.
    Eves-van den Akker S, Lilley CJ, Jones JT, Urwin PE. 2015. Plant-parasitic nematode feeding tubes and plugs: new perspectives on function. Nematology 17:1–9
    [Google Scholar]
  39. 39.
    Eves-van den Akker S, Stojilkovic B, Gheysen G. 2021. Recent applications of biotechnological approaches to elucidate the biology of plant-nematode interactions. Curr. Opin. Biotechnol. 70:122–30
    [Google Scholar]
  40. 40.
    Fan YL, Zhang XH, Zhong LJ, Wang XY, Jin LS, Lyu SH 2020. One-step generation of composite soybean plants with transgenic roots by Agrobacterium rhizogenes-mediated transformation. BMC Plant Biol 20:208
    [Google Scholar]
  41. 41.
    Fosu-Nyarko J, Jones MGK. 2015. Application of biotechnology for nematode control in crop plants. Adv. Bot. Res. 73:339–76
    [Google Scholar]
  42. 42.
    Gardner M, Dhroso A, Johnson N, Davis EL, Baum TJ et al. 2018. Novel global effector mining from the transcriptome of early life stages of the soybean cyst nematode Heterodera glycines. Sci. Rep. 8:2505
    [Google Scholar]
  43. 43.
    Gardner M, Heinz R, Wang J, Mitchum MG. 2017. Genetics and adaptation of soybean cyst nematode to broad spectrum soybean resistance. G3 7:835–41
    [Google Scholar]
  44. 44.
    Grunwald DJ, Zapotocny RW, Ozer S, Diers BW, Bent AF. 2022. Detection of rare nematode resistance Rhg1 haplotypes in Glycine soja and a novel Rhg1 α-SNAP. Plant Genome15:e20152
    [Google Scholar]
  45. 45.
    Guo W, Chen JS, Zhang F, Li ZY, Chen HF et al. 2020. Characterization of Pingliang xiaoheidou (ZDD 11047), a soybean variety with resistance to soybean cyst nematode Heterodera glycines. Plant Mol. Biol. 103:253–67
    [Google Scholar]
  46. 46.
    Guo W, Zhang F, Bao AL, You QB, Li ZY et al. 2019. The soybean Rhg1 amino acid transporter gene alters glutamate homeostasis and jasmonic acid-induced resistance to soybean cyst nematode. Mol. Plant Pathol. 20:270–86
    [Google Scholar]
  47. 47.
    Haarith D, Bushley KE, Chen SY. 2020. Fungal communities associated with Heterodera glycines and their potential in biological control: a current update. J. Nematol. 52:e2020–22
    [Google Scholar]
  48. 48.
    Hammond-Kosack KE, Jones JDG 2015. Responses to plant pathogens. Biochemistry and Molecular Biology of Plants RL Jones, BB Buchanan, W Gruissem 984–1050 Chichester, UK: Wiley. , 2nd ed..
    [Google Scholar]
  49. 49.
    Han S, Smith JM, Du Y, Bent AF. 2020. The soybean Rhg1 amino acid transporter protein becomes abundant along the SCN penetration path and impacts ROS generation. bioRxiv 277814. https://doi.org/10.1101/2020.09.01.277814
    [Crossref]
  50. 50.
    Harbach CJ, Wlezien E, Tylka GL. 2021. A mechanistic approach to assessing the potential for cover crops to serve as trap crops for the soybean cyst nematode. Plant Dis 105:1136–42
    [Google Scholar]
  51. 51.
    Hawamda AIM, Zahoor A, Abbas A, Ali MA, Bohlmann H. 2020. The Arabidopsis RboHB encoded by At1g09090 is important for resistance against nematodes. Int. J. Mol. Sci. 21:155556
    [Google Scholar]
  52. 52.
    Hewezi T. 2020. Epigenetic mechanisms in nematode-plant interactions. Annu. Rev. Phytopathol. 58:119–38
    [Google Scholar]
  53. 53.
    Hewezi T, Baum TJ. 2013. Manipulation of plant cells by cyst and root-knot nematode effectors. Mol. Plant-Microbe Interact. 26:9–16
    [Google Scholar]
  54. 54.
    Hewezi T, Lane T, Piya S, Rambani A, Rice JH, Staton M. 2017. Cyst nematode parasitism induces dynamic changes in the root epigenome. Plant Physiol 174:405–20
    [Google Scholar]
  55. 55.
    Holbein J, Franke RB, Marhavy P, Fujita S, Gorecka M et al. 2019. Root endodermal barrier system contributes to defence against plant-parasitic cyst and root-knot nematodes. Plant J 100:221–36
    [Google Scholar]
  56. 56.
    Hu YF, You J, Li CJ, Williamson VM, Wang CL. 2017. Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines. Sci. Rep. 7:41282
    [Google Scholar]
  57. 57.
    Huang CC, Yang JI, Chou KL, Lin CH, Chang HX. 2021. Copy number quantification for the soybean cyst nematode resistance locus rhg1 in the soybean varieties of Taiwan. Agronomy 11:71346
    [Google Scholar]
  58. 58.
    Huang M, Qin R, Li C, Liu C, Jiang Y et al. 2021. Transgressive resistance to Heterodera glycines in chromosome segment substitution lines derived from susceptible soybean parents. Plant Genome 14:e20091
    [Google Scholar]
  59. 59.
    Ithal N, Recknor J, Nettleton D, Hearne L, Maier T et al. 2007. Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol. Plant-Microbe Interact. 20:293–305
    [Google Scholar]
  60. 60.
    Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG. 2007. Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol. Plant-Microbe Interact. 20:510–25
    [Google Scholar]
  61. 61.
    Jain S, Kumar A. 2015. The pathogenesis related class 10 proteins in plant defense against biotic and abiotic stresses. Adv. Plants Agric. Res. 2:305–14
    [Google Scholar]
  62. 62.
    Jain S, Poromarto S, Osorno JM, McClean PE, Nelson BD. 2019. Genome wide association study discovers genomic regions involved in resistance to soybean cyst nematode (Heterodera glycines) in common bean. PLOS ONE 14:2e0212140
    [Google Scholar]
  63. 63.
    Kabelka EA, Carlson SR, Diers BW. 2006. Glycine soja PI 468916 SCN resistance loci's associated effects on soybean seed yield and other agronomic traits. Crop Sci. 46:622–29
    [Google Scholar]
  64. 64.
    Kadam S, Vuong TD, Qiu D, Meinhardt CG, Song L et al. 2016. Genomic-assisted phylogenetic analysis and marker development for next generation soybean cyst nematode resistance breeding. Plant Sci 242:342–50
    [Google Scholar]
  65. 65.
    Kahn TW, Duck NB, McCarville MT, Schouten LC, Schweri K et al. 2021. A Bacillus thuringiensis Cry protein controls soybean cyst nematode in transgenic soybean plants. Nat. Commun. 12:3380
    [Google Scholar]
  66. 66.
    Kambakam S, Ngaki MN, Sahu BB, Kandel DR, Singh P et al. 2021. Arabidopsis non-host resistance PSS30 gene enhances broad-spectrum disease resistance in the soybean cultivar Williams 82. Plant J 107:1432–46
    [Google Scholar]
  67. 67.
    Kammerhofer N, Radakovic Z, Regis JMA, Dobrev P, Vankova R et al. 2015. Role of stress-related hormones in plant defence during early infection of the cyst nematode Heterodera schachtii in Arabidopsis. New Phytol 207:778–89
    [Google Scholar]
  68. 68.
    Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D et al. 2011. 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. Plant Physiol 155:1960–75
    [Google Scholar]
  69. 69.
    Kandoth PK, Liu S, Prenger E, Ludwig A, Lakhssassi N et al. 2017. Systematic mutagenesis of serine hydroxymethyltransferase reveals an essential role in nematode resistance. Plant Physiol 175:1370–80
    [Google Scholar]
  70. 70.
    Kim KS, Vuong TD, Qiu D, Robbins RT, Shannon JG et al. 2016. Advancements in breeding, genetics, and genomics for resistance to three nematode species in soybean. Theor. Appl. Genet. 129:2295–311
    [Google Scholar]
  71. 71.
    Klepadlo M, Meinhardt CG, Vuong TD, Patil G, Bachleda N et al. 2018. Evaluation of soybean germplasm for resistance to multiple nematode species: Heterodera glycines, Meloidogyne incognita, and Rotylenchulus reniformis. Crop Sci. 58:2511–22
    [Google Scholar]
  72. 72.
    Klessig DF, Manohar M, Baby S, Koch A, Danquah WB et al. 2019. Nematode ascaroside enhances resistance in a broad spectrum of plant-pathogen systems. J. Phytopathol. 167:265–72
    [Google Scholar]
  73. 73.
    Klink VP, Darwish O, Alkharouf NW, Lawaju BR, Khatri R, Lawrence KS. 2021. Conserved oligomeric golgi (COG) complex genes functioning in defense are expressed in root cells undergoing a defense response to a pathogenic infection and exhibit regulation my MAPKs. PLOS ONE 16:e0256472
    [Google Scholar]
  74. 74.
    Klink VP, Hosseini P, Matsye P, Alkharouf NW, Matthews BF. 2009. A gene expression analysis of syncytia laser microdissected from the roots of the Glycine max (soybean) genotype PI 548402 (Peking) undergoing a resistant reaction after infection by Heterodera glycines (soybean cyst nematode). Plant Mol. Biol. 71:525–67
    [Google Scholar]
  75. 75.
    Klink VP, Hosseini P, Matsye PD, Alkharouf NW, Matthews BF. 2010. Syncytium gene expression in Glycine max[PI 88788] roots undergoing a resistant reaction to the parasitic nematode Heterodera glycines. Plant Physiol. Biochem 48:176–93
    [Google Scholar]
  76. 76.
    Klink VP, Hosseini P, Matsye PD, Alkharouf NW, Matthews BF. 2011. Differences in gene expression amplitude overlie a conserved transcriptomic program occurring between the rapid and potent localized resistant reaction at the syncytium of the Glycine max genotype Peking (PI 548402) as compared to the prolonged and potent resistant reaction of PI 88788. Plant Mol. Biol. 75:141–65
    [Google Scholar]
  77. 77.
    Klink VP, Kim KH, Martins V, Macdonald MH, Beard HS et al. 2009. A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of development of female Heterodera glycines cyst formation during infection of Glycine max. Planta 230:53–71
    [Google Scholar]
  78. 78.
    Klink VP, Matsye PD, Lawrence KS, Lawrence GW. 2013. Engineered soybean cyst nematode resistance. Soybean HA El-Shemy London: IntechOpen
    [Google Scholar]
  79. 79.
    Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF. 2007. 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). Planta 226:1389–409
    [Google Scholar]
  80. 80.
    Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF. 2007. A time-course comparative microarray analysis of an incompatible and compatible response by Glycine max (soybean) to Heterodera glycines (soybean cyst nematode) infection. Planta 226:1423–47
    [Google Scholar]
  81. 81.
    Klink VP, Sharma K, Pant SR, McNeece B, Niraula P, Lawrence GW. 2017. Components of the SNARE-containing regulon are co-regulated in root cells undergoing defense. Plant Signal. Behav. 12:e1274481
    [Google Scholar]
  82. 82.
    Koch A, Wassenegger M. 2021. Host-induced gene silencing: mechanisms and applications. New Phytol 231:54–59
    [Google Scholar]
  83. 83.
    Kofsky J, Zhang H, Song BH. 2021. Novel resistance strategies to soybean cyst nematode (SCN) in wild soybean. Sci. Rep. 11:7967
    [Google Scholar]
  84. 84.
    Kopisch-Obuch FJ, Diers BW 2006. Segregation at the SCN resistance locus rhg1 in soybean is distorted by an association between the resistance allele and reduced field emergence. Theor. Appl. Genet. 112:199–207
    [Google Scholar]
  85. 85.
    Kranse O, Beasley H, Adams S, Pires-daSilva A, Bell C et al. 2021. Toward genetic modification of plant-parasitic nematodes: delivery of macromolecules to adults and expression of exogenous mRNA in second stage juveniles. G3 11:2jkaa058
    [Google Scholar]
  86. 86.
    Lakhssassi N, Liu S, Bekal S, Zhou Z, Colantonio V et al. 2017. Characterization of the soluble NSF attachment protein gene family identifies two members involved in additive resistance to a plant pathogen. Sci. Rep. 7:45226
    [Google Scholar]
  87. 87.
    Lakhssassi N, Patil G, Piya S, Zhou Z, Baharlouei A et al. 2019. Genome reorganization of the GmSHMT gene family in soybean showed a lack of functional redundancy in resistance to soybean cyst nematode. Sci. Rep. 9:1506
    [Google Scholar]
  88. 88.
    Lakhssassi N, Piya S, Bekal S, Liu S, Zhou Z et al. 2020. A pathogenesis-related protein GmPR08-Bet VI promotes a molecular interaction between the GmSHMT08 and GmSNAP18 in resistance to Heterodera glycines. Plant Biotechnol. J. 18:1810–29
    [Google Scholar]
  89. 89.
    Lakhssassi N, Piya S, Knizia D, El Baze A, Cullen MA et al. 2020. Mutations at the serine hydroxymethyltransferase impact its interaction with a soluble NSF attachment protein and a pathogenesis-related protein in soybean. Vaccines 8:3349
    [Google Scholar]
  90. 90.
    Lawaju BR, Niraula P, Lawrence GW, Lawrence KS, Klink VP. 2020. The Glycine max conserved oligomeric golgi (COG) complex functions during a defense response to Heterodera glycines. Front. Plant Sci. 11:564495
    [Google Scholar]
  91. 91.
    Lee MW, Huffaker A, Crippen D, Robbins RT, Goggin FL. 2018. Plant elicitor peptides promote plant defences against nematodes in soybean. Mol. Plant Pathol. 19:858–69
    [Google Scholar]
  92. 92.
    Lee TG, Diers BW, Hudson ME. 2016. An efficient method for measuring copy number variation applied to improvement of nematode resistance in soybean. Plant J 88:143–53
    [Google Scholar]
  93. 93.
    Lee TG, Kumar I, Diers BW, Hudson ME. 2015. Evolution and selection of Rhg1, a copy-number variant nematode-resistance locus. Mol. Ecol. 24:1774–91
    [Google Scholar]
  94. 94.
    Lei P, Qi NW, Zhou Y, Wang YY, Zhu XF et al. 2021. Soybean miR159-GmMYB33 regulatory network involved in gibberellin-modulated resistance to Heterodera glycines. Int. J. Mol. Sci. 22:2313172
    [Google Scholar]
  95. 95.
    Li J, Todd TC, Oakley TR, Lee J, Trick HN. 2010. Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232:775–85
    [Google Scholar]
  96. 96.
    Lian Y, Wei H, Wang JS, Lei CF, Li HC et al. 2019. Chromosome-level reference genome of X12, a highly virulent race of the soybean cyst nematode Heterodera glycines. Mol. Ecol. Resour. 19:1637–46
    [Google Scholar]
  97. 97.
    Liu S, Ge F, Huang W, Lightfoot DA, Peng D. 2019. Effective identification of soybean candidate genes involved in resistance to soybean cyst nematode via direct whole genome re-sequencing of two segregating mutants. Theor. Appl. Genet. 132:2677–87
    [Google Scholar]
  98. 98.
    Liu S, Kandoth PK, Lakhssassi N, Kang J, Colantonio V et al. 2017. The soybean GmSNAP18 gene underlies two types of resistance to soybean cyst nematode. Nat. Commun. 8:14822
    [Google Scholar]
  99. 99.
    Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R et al. 2012. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256–60
    [Google Scholar]
  100. 100.
    Liu Y, Du H, Li P, Shen Y, Peng H et al. 2020. Pan-genome of wild and cultivated soybeans. Cell 182:162–76.e13
    [Google Scholar]
  101. 101.
    Maier TR, Masonbrink RE, Vijayapalani P, Gardner M, Howland AD et al. 2021. Esophageal gland RNA-Seq resource of a virulent and avirulent population of the soybean cyst nematode Heterodera glycines. Mol. Plant-Microbe Interact. 34:1084–87
    [Google Scholar]
  102. 102.
    Manohar M, Tenjo-Castano F, Chen S, Zhang YK, Kumari A et al. 2020. Plant metabolism of nematode pheromones mediates plant-nematode interactions. Nat. Commun. 11:208
    [Google Scholar]
  103. 103.
    Manosalva P, Manohar M, von Reuss SH, Chen S, Koch A et al. 2015. Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nat. Commun. 6:7795
    [Google Scholar]
  104. 104.
    Marhavy P, Kurenda A, Siddique S, Tendon VD, Zhou F et al. 2019. Single-cell damage elicits regional, nematode-restricting ethylene responses in roots. EMBO J 38:10e100972
    [Google Scholar]
  105. 105.
    Masonbrink R, Maier TR, Muppirala U, Seetharam AS, Lord E et al. 2019. The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes. BMC Genom. 20:119
    [Google Scholar]
  106. 106.
    Masonbrink R, Maier TR, Seetharam AS, Juvale PS, Baber L et al. 2019. SCNBase: a genomics portal for the soybean cyst nematode (Heterodera glycines). Database 2019:1baz111
    [Google Scholar]
  107. 107.
    Masonbrink RE, Maier TR, Hudson M, Severin A, Baum T. 2021. A chromosomal assembly of the soybean cyst nematode genome. Mol. Ecol. Resour. 21:2407–22
    [Google Scholar]
  108. 108.
    Matsye PD, Lawrence GW, Youssef RM, Kim KH, Lawrence KS et al. 2012. The expression of a naturally occurring, truncated allele of an α-SNAP gene suppresses plant parasitic nematode infection. Plant Mol. Biol. 80:131–55
    [Google Scholar]
  109. 109.
    Matthews BF, Beard H, MacDonald MH, Kabir S, Youssef RM et al. 2013. Engineered resistance and hypersusceptibility through functional metabolic studies of 100 genes in soybean to its major pathogen, the soybean cyst nematode. Planta 237:1337–57
    [Google Scholar]
  110. 110.
    McCarville MT, Marett CC, Mullaney MP, Gebhart GD, Tylka GL. 2017. Increase in soybean cyst nematode virulence and reproduction on resistant soybean varieties in Iowa from 2001 to 2015 and the effects on soybean yields. Plant Health Prog 18:146–55
    [Google Scholar]
  111. 111.
    McNeece BT, Sharma K, Lawrence GW, Lawrence KS, Klink VP. 2019. The mitogen activated protein kinase (MAPK) gene family functions as a cohort during the Glycine max defense response to Heterodera glycines. Plant Physiol. Biochem. 137:25–41
    [Google Scholar]
  112. 112.
    Meinhardt C, Howland A, Ellersieck M, Scaboo A, Diers B, Mitchum MG. 2021. Resistance gene pyramiding and rotation to combat widespread soybean cyst nematode virulence. Plant Dis 105:3238–43
    [Google Scholar]
  113. 113.
    Mejias J, Truong NM, Abad P, Favery B, Quentin M. 2019. Plant proteins and processes targeted by parasitic nematode effectors. Front. Plant Sci. 10:970
    [Google Scholar]
  114. 114.
    Mendy B, Wang'ombe MW, Radakovic ZS, Holbein J, Ilyas M et al. 2017. Arabidopsis leucine-rich repeat receptor-like kinase NILR1 is required for induction of innate immunity to parasitic nematodes. PLOS Pathog 13:4e1006284
    [Google Scholar]
  115. 115.
    Miraeiz E, Chaiprom U, Afsharifar A, Karegar A, Drnevich JM, Hudson ME. 2020. Early transcriptional responses to soybean cyst nematode HG Type 0 show genetic differences among resistant and susceptible soybeans. Theor. Appl. Genet. 133:87–102
    [Google Scholar]
  116. 116.
    Mitchum MG. 2016. Soybean resistance to the soybean cyst nematode Heterodera glycines: an update. Phytopathology 106:1444–50
    [Google Scholar]
  117. 117.
    Ngaki MN, Sahoo DK, Wang B, Bhattacharyya MK 2021. Overexpression of a plasma membrane protein generated broad-spectrum immunity in soybean. Plant Biotechnol. J. 19:502–16
    [Google Scholar]
  118. 118.
    Ngou BPM, Jones JDG, Ding P. 2021. Plant immune networks. Trends Plant Sci. 27:3255–73
    [Google Scholar]
  119. 119.
    Niblack T, Colgrove A, Colgrove K, Bond J. 2008. Shift in virulence of soybean cyst nematode is associated with use of resistance from PI 88788. Plant Health Prog. https://doi.org/10.1094/PHP-2008-0118-01-RS
    [Crossref]
  120. 120.
    Niblack TL, Lambert KN, Tylka GL. 2006. A model plant pathogen from the kingdom Animalia: Heterodera glycines, the soybean cyst nematode. Annu. Rev. Phytopathol. 44:283–303
    [Google Scholar]
  121. 121.
    Niraula PM, Sharma K, McNeece BT, Troell HA, Darwish O et al. 2020. Mitogen activated protein kinase (MAPK)-regulated genes with predicted signal peptides function in the Glycine max defense response to the root pathogenic nematode Heterodera glycines. PLOS ONE 15:e0241678
    [Google Scholar]
  122. 122.
    Niraula PM, Zhang X, Jeremic D, Lawrence KS, Klink VP. 2021. 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. PLOS ONE 16:e0244305
    [Google Scholar]
  123. 123.
    Ohtsu M, Sato Y, Kurihara D, Suzaki T, Kawaguchi M et al. 2017. Spatiotemporal deep imaging of syncytium induced by the soybean cyst nematode Heterodera glycines. Protoplasma 254:2107–15
    [Google Scholar]
  124. 124.
    Opperman CH, Bird DM. 1998. The soybean cyst nematode, Heterodera glycines: a genetic model system for the study of plant-parasitic nematodes. Curr. Opin. Plant Biol. 1:342–46
    [Google Scholar]
  125. 125.
    Pant SR, Krishnavajhala A, McNeece BT, Lawrence GW, Klink VP. 2015. The syntaxin 31-induced gene, LESION SIMULATING DISEASE1 (LSD1), functions in Glycine max defense to the root parasite Heterodera glycines. Plant Signal. Behav. 10:e977737
    [Google Scholar]
  126. 126.
    Pant SR, Matsye PD, McNeece BT, Sharma K, Krishnavajhala A et al. 2014. Syntaxin 31 functions in Glycine max resistance to the plant parasitic nematode Heterodera glycines. Plant Mol. Biol. 85:107–21
    [Google Scholar]
  127. 127.
    Parisi C, Tillie P, Rodriguez-Cerezo E. 2016. The global pipeline of GM crops out to 2020. Nat. Biotechnol. 34:31–36
    [Google Scholar]
  128. 128.
    Patil GB, Lakhssassi N, Wan J, Song L, Zhou Z et al. 2019. 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. Plant Biotechnol. J. 17:1595–611
    [Google Scholar]
  129. 129.
    Pawlowski ML, Hartman GL. 2020. Impact of arbuscular mycorrhizal species on Heterodera glycines. Plant Dis 104:2406–10
    [Google Scholar]
  130. 130.
    Peng DL, Jiang R, Peng H, Liu SM. 2021. Soybean cyst nematodes: a destructive threat to soybean production in China. Phytopathol. Res. 3:19
    [Google Scholar]
  131. 131.
    Piya S, Binder BM, Hewezi T. 2019. Canonical and noncanonical ethylene signaling pathways that regulate Arabidopsis susceptibility to the cyst nematode Heterodera schachtii. New Phytol 221:946–59
    [Google Scholar]
  132. 132.
    Piya S, Hawk T, Patel B, Baldwin L, Rice JH et al. 2021. Kinase-dead mutation: a novel strategy for improving soybean resistance to soybean cyst nematode Heterodera glycines. Mol. Plant Pathol. 23:3417–30
    [Google Scholar]
  133. 133.
    Pogorelko G, Wang J, Juvale PS, Mitchum MG, Baum TJ. 2020. Screening soybean cyst nematode effectors for their ability to suppress plant immunity. Mol. Plant Pathol. 21:1240–47
    [Google Scholar]
  134. 134.
    Pogorelko GV, Juvale PS, Rutter WB, Hutten M, Maier TR et al. 2019. Re-targeting of a plant defense protease by a cyst nematode effector. Plant J 98:1000–14
    [Google Scholar]
  135. 135.
    Radhakrishnan GV, Cook NM, Bueno-Sancho V, Lewis CM, Persoons A et al. 2019. MARPLE, a point-of-care, strain-level disease diagnostics and surveillance tool for complex fungal pathogens. BMC Biol 17:165
    [Google Scholar]
  136. 136.
    Rambani A, Hu YF, Piya S, Long M, Rice JH et al. 2020. Identification of differentially methylated miRNA genes during compatible and incompatible interactions between soybean and soybean cyst nematode. Mol. Plant-Microbe Interact. 33:1340–52
    [Google Scholar]
  137. 137.
    Rambani A, Pantalone V, Yang SN, Rice JH, Song QJ et al. 2020. Identification of introduced and stably inherited DNA methylation variants in soybean associated with soybean cyst nematode parasitism. New Phytol 227:168–84
    [Google Scholar]
  138. 138.
    Rambani A, Rice JH, Liu JY, Lane T, Ranjan P et al. 2015. The methylome of soybean roots during the compatible interaction with the soybean cyst nematode. Plant Physiol 168:1364–77
    [Google Scholar]
  139. 139.
    Ravelombola WS, Qin J, Shi A, Nice L, Bao Y et al. 2019. Genome-wide association study and genomic selection for soybean chlorophyll content associated with soybean cyst nematode tolerance. BMC Genom 20:904
    [Google Scholar]
  140. 140.
    Ravelombola WS, Qin J, Shi A, Nice L, Bao Y et al. 2020. Genome-wide association study and genomic selection for tolerance of soybean biomass to soybean cyst nematode infestation. PLOS ONE 15:e0235089
    [Google Scholar]
  141. 141.
    Rincker K, Cary T, Diers BW. 2017. Impact of soybean cyst nematode resistance on soybean yield. Crop Sci. 57:1373–82
    [Google Scholar]
  142. 142.
    Rocha LF, Pimentel MF, Bailey J, Wyciskalla T, Davidson D et al. 2021. Impact of wheat on soybean cyst nematode population density in double-cropping soybean production. Front. Plant Sci. 12:640714
    [Google Scholar]
  143. 143.
    Roth MG, Jacobs JL, Napieralski S, Byrne AM, Stouffer-Hopkins A et al. 2020. Fluopyram suppresses population densities of Heterodera glycines in field and greenhouse studies in Michigan. Plant Dis 104:1305–11
    [Google Scholar]
  144. 144.
    Sato K, Kadota Y, Shirasu K. 2019. Plant immune responses to parasitic nematodes. Front. Plant Sci. 10:1165
    [Google Scholar]
  145. 145.
    Saur IML, Panstruga R, Schulze-Lefert P. 2021. NOD-like receptor-mediated plant immunity: from structure to cell death. Nat. Rev. Immunol. 21:305–18
    [Google Scholar]
  146. 146.
    Schroeder NE, MacGuidwin AE. 2010. Behavioural quiescence reduces the penetration and toxicity of exogenous compounds in second-stage juveniles of Heterodera glycines. Nematology 12:277–87
    [Google Scholar]
  147. 147.
    Sebastian SA, Streit LG, Stephens PA, Thompson JA, Hedges BR et al. 2010. Context-specific marker-assisted selection for improved grain yield in elite soybean populations. Crop Sci. 50:1196–206
    [Google Scholar]
  148. 148.
    Sharma K, Niraula PM, Troell HA, Adhikari M, Alshehri HA et al. 2020. Exocyst components promote an incompatible interaction between Glycine max (soybean) and Heterodera glycines (the soybean cyst nematode). Sci. Rep. 10:15003
    [Google Scholar]
  149. 149.
    Shi A, Gepts P, Song Q, Xiong H, Michaels TE, Chen S 2021. Genome-wide association study and genomic prediction for soybean cyst nematode resistance in USDA common bean (Phaseolus vulgaris) core collection. Front. Plant Sci. 12:624156
    [Google Scholar]
  150. 150.
    Shi X, Chen Q, Liu S, Wang J, Peng D, Kong L. 2021. Combining targeted metabolite analyses and transcriptomics to reveal the specific chemical composition and associated genes in the incompatible soybean variety PI437654 infected with soybean cyst nematode HG1.2.3.5.7. BMC Plant Biol 21:217
    [Google Scholar]
  151. 151.
    Shi Z, Liu S, Noe J, Arelli P, Meksem K, Li Z. 2015. SNP identification and marker assay development for high-throughput selection of soybean cyst nematode resistance. BMC Genom 16:314
    [Google Scholar]
  152. 152.
    Siddique S, Matera C, Radakovic ZS, Hasan MS, Gutbrod P et al. 2014. Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Sci. Signal. 7:ra33
    [Google Scholar]
  153. 153.
    Siddique S, Coomer A, Baum T, Williamson VM. 2022. Recognition and response in plant–nematode interactions. Annu. Rev. Phytopathol. 60:143–62
    [Google Scholar]
  154. 154.
    Sindhu AS, Maier TR, Mitchum MG, Hussey RS, Davis EL, Baum TJ 2009. Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J. Exp. Bot. 60:315–24
    [Google Scholar]
  155. 155.
    Soares PLM, dos Santos JM, Dias WP. 2016. The soybean cyst nematode control in Brazil. J. Nematol. 48:370–71 (Meet. Abstr.)
    [Google Scholar]
  156. 156.
    Sobczak M, Golinowski W 2011. Cyst nematodes and syncytia. Genomics and Molecular Genetics of Plant-Nematode Interactions J Jones, G Gheysen, C Fenoll 61–82
    [Google Scholar]
  157. 157.
    Song J, Toth K, Montes-Luz B, Stacey G. 2021. Soybean hairy root transformation: a rapid and highly efficient method. Curr. Protoc. 1:e195
    [Google Scholar]
  158. 158.
    Song Q, Yan L, Quigley C, Fickus E, Wei H et al. 2020. Soybean BARCSoySNP6K: an assay for soybean genetics and breeding research. Plant J 104:800–11
    [Google Scholar]
  159. 159.
    St-Amour VTB, Mimee B, Torkamaneh D, Jean M, Belzile F, O'Donoughue LS. 2020. Characterizing resistance to soybean cyst nematode in PI 494182, an early maturing soybean accession. Crop Sci. 60:2053–69
    [Google Scholar]
  160. 160.
    Ste-Croix DT, St-Marseille AFG, Lord E, Belanger RR, Brodeur J, Mimee B. 2021. Genomic profiling of virulence in the soybean cyst nematode using single-nematode sequencing. Phytopathology 111:137–48
    [Google Scholar]
  161. 161.
    Steeves RM, Todd TC, Essig JS, Trick HN. 2006. Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction. Funct. Plant Biol. 33:991–99
    [Google Scholar]
  162. 162.
    Suzuki C, Taguchi-Shiobara F, Ikeda C, Iwahashi M, Matsui T et al. 2020. Mapping soybean rhg2 locus, which confers resistance to soybean cyst nematode race 1 in combination with rhg1 and Rhg4 derived from PI 84751. Breed. Sci. 70:474–80
    [Google Scholar]
  163. 163.
    Tabashnik BE, Carrière Y. 2017. Surge in insect resistance to transgenic crops and prospects for sustainability. Nat. Biotechnol. 35:926–35
    [Google Scholar]
  164. 164.
    Tian Y, Liu B, Shi XH, Reif JC, Guan RX et al. 2019. Deep genotyping of the gene GmSNAP facilitates pyramiding resistance to cyst nematode in soybean. Crop J. 7:677–84
    [Google Scholar]
  165. 165.
    Topalovic O, Bredenbruch S, Schleker ASS, Heuer H. 2020. Microbes attaching to endoparasitic phytonematodes in soil trigger plant defense upon root penetration by the nematode. Front. Plant Sci. 11:138
    [Google Scholar]
  166. 166.
    Torkamaneh D, Laroche J, Valliyodan B, O'Donoughue L, Cober E et al. 2021. Soybean (Glycine max) haplotype map (GmHapMap): a universal resource for soybean translational and functional genomics. Plant Biotechnol. J. 19:324–34
    [Google Scholar]
  167. 167.
    Torkamaneh D, Lemay MA, Belzile F. 2021. The pan-genome of the cultivated soybean (PanSoy) reveals an extraordinarily conserved gene content. Plant Biotechnol. J. 19:1852–62
    [Google Scholar]
  168. 168.
    Toruno TY, Stergiopoulos I, Coaker G. 2016. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54:419–41
    [Google Scholar]
  169. 169.
    Tran DT, Steketee CJ, Boehm JD Jr., Noe J, Li Z. 2019. Genome-wide association analysis pinpoints additional major genomic regions conferring resistance to soybean cyst nematode (Heterodera glycines Ichinohe). Front. Plant Sci. 10:401
    [Google Scholar]
  170. 170.
    Tylka G, Gebhart GD, Marett CC, Mullaney MP. 2021. Evaluation of soybean varieties resistant to soybean cyst nematode in Iowa—2021 Rep. IPM 2 Iowa State Univ. Ext. Outreach Ames, IA: https://store.extension.iastate.edu/product/2429
  171. 171.
    Tylka GL. 2021. The soybean cyst nematode: pervasive and destructive to soybean production in the mid-western United States. Integrated Nematode Management: State-of-the-Art and Visions for the Future RA Sikora, J Desaeger, LPG Molendijk 117–24 Wallingford, UK: CABI
    [Google Scholar]
  172. 172.
    Tylka GL, Marett CC. 2021. Known distribution of the soybean cyst nematode, Heterodera glycines, in the United States and Canada in 2020. Plant Health Prog 22:72–74
    [Google Scholar]
  173. 173.
    Urwin PE, Lilley CJ, Atkinson HJ. 2002. Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant-Microbe Interact. 15:747–52
    [Google Scholar]
  174. 174.
    Usovsky M, Lakhssassi N, Patil GB, Vuong TD, Piya S et al. 2021. Dissecting nematode resistance regions in soybean revealed pleiotropic effect of soybean cyst and reniform nematode resistance genes. Plant Genome 14:e20083
    [Google Scholar]
  175. 175.
    Usovsky M, Robbins R, Fultz Wilkes J, Crippen D, Shankar V et al. 2022. Classification methods and identification of reniform nematode resistance in known soybean cyst nematode resistant soybean genotypes. Plant Dis 106:2382–89
    [Google Scholar]
  176. 176.
    Usovsky M, Ye H, Vuong TD, Patil GB, Wan J et al. 2021. Fine-mapping and characterization of qSCN18, a novel QTL controlling soybean cyst nematode resistance in PI 567516C. Theor. Appl. Genet. 134:621–31
    [Google Scholar]
  177. 177.
    van Esse HP, Reuber TL, van der Does D. 2020. Genetic modification to improve disease resistance in crops. New Phytol 225:70–86
    [Google Scholar]
  178. 178.
    Velloso JA, Campos VP, Terra WC, Barros AF, Pedroso MP et al. 2021. Slight induction and strong inhibition of Heterodera glycines hatching by short-chain molecules released by different plant species. J. Nematol. 53:e2021–71
    [Google Scholar]
  179. 179.
    Vieira CC, Chen PY, Usovsky M, Vuong T, Howland AD et al. 2021. A major quantitative trait locus resistant to southern root-knot nematode sustains soybean yield under nematode pressure. Crop Sci. 61:31773–82
    [Google Scholar]
  180. 180.
    Vieira P, Gleason C. 2019. Plant-parasitic nematode effectors: insights into their diversity and new tools for their identification. Curr. Opin. Plant Biol. 50:37–43
    [Google Scholar]
  181. 181.
    Vleeshouwers VGAA, Oliver RP. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol. Plant-Microbe Interact. 27:196–206
    [Google Scholar]
  182. 182.
    Vuong TD, Sleper DA, Shannon JG, Nguyen HT. 2010. Novel quantitative trait loci for broad-based resistance to soybean cyst nematode (Heterodera glycines Ichinohe) in soybean PI 567516C. Theor. Appl. Genet. 121:1253–66
    [Google Scholar]
  183. 183.
    Vuong TD, Sonah H, Meinhardt CG, Deshmukh R, Kadam S et al. 2015. Genetic architecture of cyst nematode resistance revealed by genome-wide association study in soybean. BMC Genom 16:593
    [Google Scholar]
  184. 184.
    Vuong TD, Sonah H, Patil G, Meinhardt C, Usovsky M et al. 2021. Identification of genomic loci conferring broad-spectrum resistance to multiple nematode species in exotic soybean accession PI 567305. Theor. Appl. Genet. 134:3379–95
    [Google Scholar]
  185. 185.
    Wang D, Arelli PR, Shoemaker RC, Diers BW. 2001. Loci underlying resistance to race 3 of soybean cyst nematode in Glycine soja plant introduction 468916. Theor. Appl. Genet. 103:561–66
    [Google Scholar]
  186. 186.
    Wang J, Niblack TL, Tremain JA, Wiebold WJ, Tylka GL et al. 2003. Soybean cyst nematode reduces soybean yield without causing obvious aboveground symptoms. Plant Dis. 87:623–28
    [Google Scholar]
  187. 187.
    Wang R, Deng MM, Yang C, Yu QQ, Zhang L et al. 2021. A Qa-SNARE complex contributes to soybean cyst nematode resistance via regulation of mitochondria-mediated cell death. J. Exp. Bot. 72:7145–62
    [Google Scholar]
  188. 188.
    Warnock ND, Wilson L, Patten C, Fleming CC, Maule AG, Dalzell JJ. 2017. Nematode neuropeptides as transgenic nematicides. PLOS Pathog 13:2e1006237
    [Google Scholar]
  189. 189.
    Webb DM, Baltazar BM, Rao-Arelli AP, Schupp J, Clayton K et al. 1995. Genetic mapping of soybean cyst nematode race-3 resistance loci in the soybean PI 437.654. Theor. Appl. Genet. 91:574–81
    [Google Scholar]
  190. 190.
    Wen LW, Chang HX, Brown PJ, Domier LL, Hartman GL. 2019. Genome-wide association and genomic prediction identifies soybean cyst nematode resistance in common bean including a syntenic region to soybean Rhg1 locus. Hortic. Res. 6:9
    [Google Scholar]
  191. 191.
    Whitham SA, Qi M, Innes RW, Ma W, Lopes-Caitar V, Hewezi T. 2016. Molecular soybean-pathogen interactions. Annu. Rev. Phytopathol. 54:443–68
    [Google Scholar]
  192. 192.
    Wubben MJE, Su H, Rodermel SR, Baum TJ. 2001. Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 14:1206–12
    [Google Scholar]
  193. 193.
    Wyss U, Zunke U, Hard T, Lechner K, Poloczek E. 1985. Heterodera schachtii (Nematoda). Video E2904. Encycl. Cinematogr. IWF Göttingen Göttingen: https://av.tib.eu/media/15489
  194. 194.
    Xing ZF, Wu XJ, Zhao J, Zhao XB, Zhu XF et al. 2020. Isolation and identification of induced systemic resistance determinants from Bacillus simplex Sneb545 against Heterodera glycines. Sci. Rep. 10:11586
    [Google Scholar]
  195. 195.
    Yang L, Tian Y, Liu YL, Reif JC, Li YH, Qiu LJ. 2021. QTL mapping of qSCN3–1 for resistance to soybean cyst nematode in soybean line Zhongpin 03–5373. Crop J. 9:351–59
    [Google Scholar]
  196. 196.
    Yu N, Diers BW. 2017. Fine mapping of the SCN resistance QTL cqSCN-006 and cqSCN-007 from Glycine soja PI 468916. Euphytica 213:54
    [Google Scholar]
  197. 197.
    Yu N, Lee TG, Rosa DP, Hudson M, Diers BW. 2016. Impact of Rhg1 copy number, type, and interaction with Rhg4 on resistance to Heterodera glycines in soybean. Theor. Appl. Genet. 129:2403–12
    [Google Scholar]
  198. 198.
    Yun HS, Kwon C. 2017. Vesicle trafficking in plant immunity. Curr. Opin. Plant Biol. 40:34–42
    [Google Scholar]
  199. 199.
    Zhang H, Li C, Davis EL, Wang J, Griffin JD et al. 2016. Genome-wide association study of resistance to soybean cyst nematode (Heterodera glycines) HG type 2.5.7 in wild soybean (Glycine soja). Front. Plant Sci. 7:1214
    [Google Scholar]
  200. 200.
    Zhang M, Liu S, Wang Z, Yuan Y, Zhang Z et al. 2022. Progress in soybean functional genomics over the past decade. Plant Biotechnol. J. 20:2256–82
    [Google Scholar]
  201. 201.
    Zhao M, Wu S, Zhou Q, Vivona S, Cipriano DJ et al. 2015. Mechanistic insights into the recycling machine of the SNARE complex. Nature 518:61–67
    [Google Scholar]
  202. 202.
    Zheng Q, Putker V, Goverse A. 2021. Molecular and cellular mechanisms involved in host-specific resistance to cyst nematodes in crops. Front. Plant Sci. 12:641582
    [Google Scholar]
  203. 203.
    Zhou L, Song L, Lian Y, Ye H, Usovsky M et al. 2021. Genetic characterization of qSCN10 from an exotic soybean accession PI 567516C reveals a novel source conferring broad-spectrum resistance to soybean cyst nematode. Theor. Appl. Genet. 134:859–74
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-020620-120823
Loading
/content/journals/10.1146/annurev-phyto-020620-120823
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error