1932

Abstract

Soybean hosts a wide variety of pathogens that cause significant yield losses. The importance of soybean as a major oilseed crop has led to research focused on its interactions with pathogens, such as , , , , and . Pioneering work on soybean's interactions with these organisms, which represent the five major pathogen groups (viruses, bacteria, oomycetes, fungi, and nematodes), has contributed to our understanding of the molecular mechanisms underlying virulence and immunity. These mechanisms involve conserved and unique features that validate the need for research in both soybean and homologous model systems. In this review, we discuss identification of effectors and their functions as well as resistance gene–mediated recognition and signaling. We also point out areas in which model systems and recent advances in resources and tools have provided opportunities to gain deeper insights into soybean-pathogen interactions.

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2016-08-04
2024-04-24
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Literature Cited

  1. Abberton M, Batley J, Bentley A, Bryant J, Cai H. 1.  et al. 2015. Global agricultural intensification during climate change: a role for genomics. Plant Biotechnol. J. 14:1095–98 [Google Scholar]
  2. Alves MS, Soares ZG, Vidigal PMP, Barros EG, Poddanosqui AMP. 2.  et al. 2015. Differential expression of four soybean bZIP genes during Phakopsora pachyrhizi infection. Funct. Integr. Genom. 15:685–96 [Google Scholar]
  3. Alves Pereira Morales AM, Borém A, Graham MA, Abdelnoor RV. 3.  2012. Advances on molecular studies of the interaction soybean: Asian rust. Crop Breed. Appl. Biotechnol. 12:1–7 [Google Scholar]
  4. Anderson RG, Casady MS, Fee RA, Vaughan MM, Deb D. 4.  et al. 2012. Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojae suppress immunity in distantly related plants. Plant J. 72:882–93 [Google Scholar]
  5. Ashfield T, Egan AN, Pfeil BE, Chen NW, Podicheti R. 5.  et al. 2012. Evolution of a complex disease resistance gene cluster in diploid Phaseolus and tetraploid Glycine. Plant Physiol. 159:336–54 [Google Scholar]
  6. Ashfield T, Keen NT, Buzzell RI, Innes RW. 6.  1995. Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus. Genetics 141:1597–604 [Google Scholar]
  7. Ashfield T, Ong LE, Nobuta K, Schneider CM, Innes RW. 7.  2004. Convergent evolution of disease resistance gene specificity in two flowering plant families. Plant Cell 16:309–18 [Google Scholar]
  8. Ashfield T, Redditt T, Russell A, Kessens R, Rodibaugh N. 8.  et al. 2014. Evolutionary relationship of disease resistance genes in soybean and Arabidopsis specific for the Pseudomonas syringae effectors AvrB and AvrRpm1. Plant Physiol. 166:235–51Revealed that NLR genes with similar specificities evolved independently in Arabidopsis and soybean. [Google Scholar]
  9. Bencke-Malato M, Cabreira C, Wiebke-Strohm B, Bücker-Neto L, Mancini E. 9.  et al. 2014. Genome-wide annotation of the soybean WRKY family and functional characterization of genes involved in response to Phakopsora pachyrhizi infection. BMC Plant Biol. 14:236 [Google Scholar]
  10. Bisgrove SR, Simonich MT, Smith NM, Sattler A, Innes RW. 10.  1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6:927–33 [Google Scholar]
  11. Brucker E, Carlson S, Wright E, Niblack T, Diers B. 11.  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]
  12. Brucker E, Niblack T, Kopisch-Obuch FJ, Diers BW. 12.  2005. The effect of rhg1 on reproduction of Heterodera glycines in the field and greenhouse and associated effects on agronomic traits. Crop Sci. 45:1721–27 [Google Scholar]
  13. Campe R, Langenbach C, Leissing F, Popescu GV, Popescu SC. 13.  et al. 2015. ABC transporter PEN3/PDR8/ABCG36 interacts with calmodulin that, like PEN3, is required for Arabidopsis nonhost resistance. New Phytol. 209:294–306 [Google Scholar]
  14. Chakraborty N, Curley J, Frederick RD, Hyten DL, Nelson RL. 14.  et al. 2009. Mapping and confirmation of a new allele at Rpp1 from soybean PI 594538A conferring RB lesion-type resistance to soybean rust. Crop Sci. 49:783–90 [Google Scholar]
  15. Chen H, Zhang L, Yu K, Wang A. 15.  2015. Pathogenesis of Soybean mosaic virus in soybean carrying Rsv1 gene is associated with miRNA and siRNA pathways, and breakdown of AGO1 homeostasis. Virology 476:395–404 [Google Scholar]
  16. Chen H, Zhao S, Yang Z, Sha A, Wan Q. 16.  et al. 2015. Genetic analysis and molecular mapping of resistance gene to Phakopsora pachyrhizi in soybean germplasm SX6907. Theor. Appl. Genet. 128:733–43 [Google Scholar]
  17. Chen NW, Sevignac M, Thareau V, Magdelenat G, David P. 17.  et al. 2010. Specific resistances against Pseudomonas syringae effectors AvrB and AvrRpm1 have evolved differently in common bean (Phaseolus vulgaris), soybean (Glycine max), and Arabidopsis thaliana. New Phytol. 187:941–56 [Google Scholar]
  18. Choi JJ, Alkharouf NW, Schneider KT, Matthews BF, Frederick RD. 18.  2008. Expression patterns in soybean resistant to Phakopsora pachyrhizi reveal the importance of peroxidases and lipoxygenases. Funct. Integr. Genom. 8:341–59 [Google Scholar]
  19. Chowda-Reddy RV, Sun H, Chen H, Poysa V, Ling H. 19.  et al. 2011. Mutations in the P3 protein of Soybean mosaic virus G2 isolates determine virulence on Rsv4-genotype soybean. Mol. Plant-Microbe Interact. 24:37–43 [Google Scholar]
  20. Chowda-Reddy RV, Sun H, Hill JH, Poysa V, Wang A. 20.  2011. Simultaneous mutations in multi-viral proteins are required for Soybean mosaic virus to gain virulence on soybean genotypes carrying different R genes. PLOS ONE 6:e28342 [Google Scholar]
  21. Chung BY, Miller WA, Atkins JF, Firth AE. 21.  2008. An overlapping essential gene in the Potyviridae. PNAS 105:5897–902 [Google Scholar]
  22. Chung EH, El-Kasmi F, He Y, Loehr A, Dangl JL. 22.  2014. A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16:484–94 [Google Scholar]
  23. Coaker G, Falick A, Staskawicz B. 23.  2005. Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308:548–50 [Google Scholar]
  24. Concibido VC, Diers BW, Arelli PR. 24.  2004. A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci. 44:1121–31 [Google Scholar]
  25. Cook DE, Bayless AM, Wang K, Guo XL, Song QJ. 25.  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]
  26. Cook DE, Lee TG, Guo XL, Melito S, Wang K. 26.  et al. 2012. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–9First example of disease resistance conferred by copy number variation of a tandem repeat. [Google Scholar]
  27. Cooper B, Campbell KB, Feng J, Garrett WM, Frederick R. 27.  2011. Nuclear proteomic changes linked to soybean rust resistance. Mol. Biosyst. 7:773–83 [Google Scholar]
  28. Cooper B, Campbell KB, McMahon MB, Luster DG. 28.  2013. Disruption of Rpp1-mediated soybean rust immunity by virus-induced gene silencing. Plant Signal. Behav. 8:e27543 [Google Scholar]
  29. Curtin SJ, Michno JM, Campbell BW, Gil-Humanes J, Mathioni SM. 29.  et al. 2015. microRNA maturation and microRNA target gene expression regulation are severely disrupted in soybean dicer-like1 double mutants. G3 (Bethesda) 6:423–33 [Google Scholar]
  30. Curtin SJ, Zhang F, Sander JD, Haun WJ, Starker C. 30.  et al. 2011. Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol. 156:466–73 [Google Scholar]
  31. Day B, Dahlbeck D, Staskawicz BJ. 31.  2006. NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18:2782–91 [Google Scholar]
  32. DeYoung BJ, Innes RW. 32.  2006. Plant NBS-LRR proteins in pathogen sensing and host defense. Nat. Immunol. 7:1243–49 [Google Scholar]
  33. Diers B, Skorupska H, Rao-Arelli A, Cianzio S. 33.  1997. Genetic relationships among soybean plant introductions with resistance to soybean cyst nematodes. Crop Sci. 37:1966–72 [Google Scholar]
  34. Dong S, Kong G, Qutob D, Yu X, Tang J. 34.  et al. 2012. The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity. Mol. Plant-Microbe Interact. 25:896–909 [Google Scholar]
  35. Dong S, Yin W, Kong G, Yang X, Qutob D. 35.  et al. 2011. Phytophthora sojae avirulence effector Avr3b is a secreted NADH and ADP-ribose pyrophosphorylase that modulates plant immunity. PLOS Pathog. 7:e1002353 [Google Scholar]
  36. Dorrance AE, Mills D, Robertson AE, Draper MA, Giesler L, Tenuta A. 36.  2007. Phytophthora root and stem rot of soybean. Plant Health Instr. doi: 10.1094/PHI-I-2007-0830-07
  37. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM. 37.  et al. 2012. Widespread dynamic DNA methylation in response to biotic stress. PNAS 109:E2183–91 [Google Scholar]
  38. Eggenberger AL, Hajimorad MR, Hill JH. 38.  2008. Gain of virulence on Rsv1-genotype soybean by an avirulent Soybean mosaic virus requires concurrent mutations in both P3 and HC-Pro. Mol. Plant-Microbe Interact. 21:931–36 [Google Scholar]
  39. Fang Y, Tyler BM. 39.  2016. Efficient disruption and replacement of an effector gene in the oomycete Phytophthora sojae using CRISPR/Cas9. Mol. Plant Pathol. 17:127–39 [Google Scholar]
  40. Gao B, Allen R, Davis EL, Baum TJ, Hussey RS. 40.  2004. Molecular characterisation and developmental expression of a cellulose-binding protein gene in the soybean cyst nematode Heterodera glycines. Int. J. Parasitol. 34:1377–83 [Google Scholar]
  41. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS. 41.  2001. Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant-Microbe Interact. 14:1247–54 [Google Scholar]
  42. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS. 42.  2003. The parasitome of the phytonematode Heterodera glycines. Mol. Plant-Microbe Interact. 16:720–26 [Google Scholar]
  43. Gao H, Bhattacharyya MK. 43.  2008. The soybean-Phytophthora resistance locus Rps1-k encompasses coiled coil-nucleotide binding-leucine rich repeat-like genes and repetitive sequences. BMC Plant Biol. 8:29 [Google Scholar]
  44. Garcia A, Calvo ES, de Souza Kiihl RA, Harada A, Hiromoto DM, Vieira LGE. 44.  2008. Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor. Appl. Genet. 117:545–53 [Google Scholar]
  45. Gijzen M, Ishmael C, Shrestha SD. 45.  2014. Epigenetic control of effectors in plant pathogens. Front. Plant Sci. 5:638 [Google Scholar]
  46. Gijzen M, Nurnberger T. 46.  2006. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67:1800–7 [Google Scholar]
  47. Godoy CV. 47.  2012. Risk and management of fungicide resistance in the Asian soybean rust fungus Phakopsora pachyrhizi. Fungicide Resistance in Crop Protection: Risk and Management TS Thind 87–95 Wallingford, UK: CABI [Google Scholar]
  48. Gopalan S, Bauer DW, Alfano JR, Loniello AO, He SY, Collmer A. 48.  1996. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8:1095–105 [Google Scholar]
  49. Grant MR, Godiard L, Straube E, Ashfield T, Lewald J. 49.  et al. 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–46 [Google Scholar]
  50. Hajimorad MR, Eggenberger AL, Hill JH. 50.  2005. Loss and gain of elicitor function of Soybean mosaic virus G7 provoking Rsv1-mediated lethal systemic hypersensitive response maps to P3. J. Virol. 79:1215–22 [Google Scholar]
  51. Hajimorad MR, Eggenberger AL, Hill JH. 51.  2006. Strain-specific P3 of Soybean mosaic virus elicits Rsv1-mediated extreme resistance, but absence of P3 elicitor function alone is insufficient for virulence on Rsv1-genotype soybean. Virology 345:156–66 [Google Scholar]
  52. Hajimorad MR, Eggenberger AL, Hill JH. 52.  2008. Adaptation of Soybean mosaic virus avirulent chimeras containing P3 sequences from virulent strains to Rsv1-genotype soybeans is mediated by mutations in HC-Pro. Mol. Plant-Microbe Interact. 21:937–46 [Google Scholar]
  53. Hajimorad MR, Hill JH. 53.  2001. Rsv1-mediated resistance against Soybean mosaic virus-N is hypersensitive response–independent at inoculation site, but has the potential to initiate a hypersensitive response–like mechanism. Mol. Plant-Microbe Interact. 14:587–98 [Google Scholar]
  54. Haldar K, Kamoun S, Hiller NL, Bhattacharje S, van Ooij C. 54.  2006. Common infection strategies of pathogenic eukaryotes. Nat. Rev. Microbiol. 4:922–31 [Google Scholar]
  55. Hamamouch N, Li C, Hewezi T, Baum TJ, Mitchum MG. 55.  et al. 2012. The interaction of the novel 30C02 cyst nematode effector protein with a plant β-1,3-endoglucanase may suppress host defence to promote parasitism. J. Exp. Bot. 63:3683–95 [Google Scholar]
  56. Hayes AJ, Jeong SC, Gore MA, Yu YG, Buss GR. 56.  et al. 2004. Recombination within a nucleotide-binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to Soybean mosaic virus in soybeans. Genetics 166:493–503 [Google Scholar]
  57. Hewezi T. 57.  2015. Cellular signaling pathways and posttranslational modifications mediated by nematode effector proteins. Plant Physiol. 169:1018–26 [Google Scholar]
  58. Hewezi T, Howe P, Maier TR, Baum TJ. 58.  2008. Arabidopsis small RNAs and their targets during cyst nematode parasitism. Mol. Plant-Microbe Interact. 21:1622–34 [Google Scholar]
  59. Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG. 59.  et al. 2008. Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–93 [Google Scholar]
  60. Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG. 60.  et al. 2010. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol. 152:968–84 [Google Scholar]
  61. Hewezi T, Juvale PS, Piya S, Maier TR, Rambani A. 61.  et al. 2015. The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis. Plant Cell 27:891–907 [Google Scholar]
  62. Hill JH, Whitham SA. 62.  2014. Control of virus diseases in soybeans. Adv. Virus Res. 90:355–90 [Google Scholar]
  63. Hwang IY, Lim SM. 63.  1992. Effects of individual and multiple infections with 3 bacterial pathogens on disease severity and yield of soybeans. Plant Dis. 76:195–98 [Google Scholar]
  64. Hyten DL, Hartman GL, Nelson RL, Frederick RD, Concibido VC. 64.  et al. 2007. Map location of the Rpp1 locus that confers resistance to soybean rust in soybean. Crop Sci. 47:835–38 [Google Scholar]
  65. Hyten DL, Smith JR, Frederick RD, Tucker ML, Song Q, Cregan PB. 65.  2009. Bulked segregant analysis using the GoldenGate assay to locate the locus that confers resistance to soybean rust in soybean. Crop Sci. 49:265 [Google Scholar]
  66. Igarashi A, Yamagata K, Sugai T, Takahashi Y, Sugawara E. 66.  et al. 2009. Apple latent spherical virus vectors for reliable and effective virus-induced gene silencing among a broad range of plants including tobacco, tomato, Arabidopsis thaliana, cucurbits, and legumes. Virology 386:407–16 [Google Scholar]
  67. Ilut DC, Lipka AE, Jeong N, Bae DN, Kim DH. 67.  et al. 2015. Identification of haplotypes at the Rsv4 genomic region in soybean associated with durable resistance to Soybean mosaic virus. Theor. Appl Genet. 129:453–68 [Google Scholar]
  68. Innes RW, Ameline-Torregrosa C, Ashfield T, Cannon E, Cannon SB. 68.  et al. 2008. Differential accumulation of retroelements and diversification of NB-LRR disease resistance genes in duplicated regions following polyploidy in the ancestor of soybean. Plant Physiol. 148:1740–59 [Google Scholar]
  69. Innes RW, Bisgrove SR, Smith NM, Bent AF, Staskawicz BJ, Liu YC. 69.  1993. Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. Plant J. 4:813–20 [Google Scholar]
  70. Jiang RH, Tripathy S, Govers F, Tyler BM. 70.  2008. RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. PNAS 105:4874–79 [Google Scholar]
  71. Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D. 71.  et al. 2011. The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates expression of a large number of stress- and defense-related genes in degenerating feeding cells. Plant Physiol. 155:1960–75 [Google Scholar]
  72. Kawashima CG, Guimarães GA, Nogueira SR, MacLean D, Cook DR. 72.  et al. 2016. A pigeonpea gene confers resistance to Asian soybean rust in soybean. Nat. Biotechnol. 34661–65
  73. Kelly HY, Dufault NS, Walker DR, Isard SA, Schneider RW. 73.  et al. 2015. From select agent to an established pathogen: the response to Phakopsora pachyrhizi (soybean rust) in North America. Phytopathology 105:905–16 [Google Scholar]
  74. Kendrick MD, Harris DK, Ha BK, Hyten DL, Cregan PB. 74.  et al. 2011. Identification of a second Asian soybean rust resistance gene in Hyuuga soybean. Phytopathology 101:535–43 [Google Scholar]
  75. Kennedy BW, Tachibana H. 75.  1973. Bacterial disease. Soybeans: Improvement, Production and Uses BE Caldwell 491–504 Madison, WI: Am. Soc. Agron. [Google Scholar]
  76. Kessens R, Ashfield T, Kim SH, Innes RW. 76.  2014. Determining the GmRIN4 requirements of the soybean disease resistance proteins Rpg1b and Rpg1r using a Nicotiana glutinosa–based agroinfiltration system. PLOS ONE 9:e108159 [Google Scholar]
  77. Khatabi B, Fajolu OL, Wen RH, Hajimorad MR. 77.  2012. Evaluation of North American isolates of Soybean mosaic virus for gain of virulence on Rsv-genotype soybeans with special emphasis on resistance-breaking determinants on Rsv4. Mol. Plant Pathol. 13:1077–88 [Google Scholar]
  78. Kim KS, Unfried JR, Hyten DL, Frederick RD, Hartman GL. 78.  et al. 2012. Molecular mapping of soybean rust resistance in soybean accession PI 561356 and SNP haplotype analysis of the Rpp1 region in diverse germplasm. Theor. Appl. Genet. 125:1339–52 [Google Scholar]
  79. Kim M, Hyten DL, Bent AF, Diers BW. 79.  2010. Fine mapping of the SCN resistance locus rhg1-b from PI 88788. Plant Genome 3:81–89 [Google Scholar]
  80. Kim M, Hyten DL, Niblack TL, Diers BW. 80.  2011. Stacking resistance alleles from wild and domestic soybean sources improves soybean cyst nematode resistance. Crop Sci. 51:934–43 [Google Scholar]
  81. King ZR, Harris DK, Pedley KF, Song Q, Wang D. 81.  et al. 2016. A novel Phakopsora pachyrhizi resistance allele (Rpp) contributed by PI 567068A. Theor. Appl. Genet. 129:517–34 [Google Scholar]
  82. Kole C, Muthamilarasan M, Henry R, Edwards D, Sharma R. 82.  et al. 2015. Application of genomics-assisted breeding for generation of climate resilient crops: progress and prospects. Front. Plant Sci. 6:563 [Google Scholar]
  83. Kong G, Zhao Y, Jing M, Huang J, Yang J. 83.  et al. 2015. The activation of Phytophthora effector Avr3b by plant cyclophilin is required for the nudix hydrolase activity of Avr3b. PLOS Pathog. 11:e1005139 [Google Scholar]
  84. Kyndt T, Vieira P, Gheysen G, de Almeida-Engler J. 84.  2013. Nematode feeding sites: unique organs in plant roots. Planta 238:807–18 [Google Scholar]
  85. Langenbach C, Campe R, Schaffrath U, Goellner K, Conrath U. 85.  2013. UDP-glucosyltransferase UGT84A2/BRT1 is required for Arabidopsis nonhost resistance to the Asian soybean rust pathogen Phakopsora pachyrhizi. New Phytol. 198:536–45 [Google Scholar]
  86. Langenbach C, Schultheiss H, Rosendahl M, Tresch N, Conrath U, Goellner K. 86.  2016. Interspecies gene transfer provides soybean resistance to a fungal pathogen. Plant Biotechnol. J. 14:699–708 [Google Scholar]
  87. Lee C, Chronis D, Kenning C, Peret B, Hewezi T. 87.  et al. 2011. The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiol. 155:866–80 [Google Scholar]
  88. Lee D, Bourdais G, Yu G, Robatzek S, Coaker G. 88.  2015. Phosphorylation of the plant immune regulator RPM1-INTERACTING PROTEIN4 enhances plant plasma membrane H+-ATPase activity and inhibits flagellin-triggered immune responses in Arabidopsis. Plant Cell 27:2042–56 [Google Scholar]
  89. Levesque CA, Brouwer H, Cano L, Hamilton JP, Holt C. 89.  et al. 2010. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol. 11:R73 [Google Scholar]
  90. Lewis JD, Lee A, Ma W, Zhou H, Guttman DS, Desveaux D. 90.  2011. The YopJ superfamily in plant-associated bacteria. Mol. Plant Pathol. 12:928–37 [Google Scholar]
  91. Li M, Ma X, Chiang YH, Yadeta KA, Ding P. 91.  et al. 2014. Proline isomerization of the immune receptor-interacting protein RIN4 by a cyclophilin inhibits effector-triggered immunity in Arabidopsis. Cell Host Microbe 16:473–83 [Google Scholar]
  92. Li S, Smith JR, Ray JD, Frederick RD. 92.  2012. Identification of a new soybean rust resistance gene in PI 567102B. Theor. Appl. Genet. 125:133–42 [Google Scholar]
  93. Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W. 93.  2012. Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PLOS ONE 7:e39650 [Google Scholar]
  94. Lin F, Zhao M, Baumann DD, Ping J, Sun L. 94.  et al. 2014. Molecular response to the pathogen Phytophthora sojae among ten soybean near isogenic lines revealed by comparative transcriptomics. BMC Genom. 15:18 [Google Scholar]
  95. Link TI, Lang P, Scheffler BE, Duke MV, Graham MA. 95.  et al. 2014. The haustorial transcriptomes of Uromyces appendiculatus and Phakopsora pachyrhizi and their candidate effector families. Mol. Plant Pathol. 15:379–93 [Google Scholar]
  96. Liu J, Elmore JM, Lin ZJ, Coaker G. 96.  2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:137–46 [Google Scholar]
  97. Liu JZ, Graham MA, Pedley KF, Whitham SA. 97.  2015. Gaining insight into soybean defense responses using functional genomics approaches. Brief. Funct. Genom. 14:283–90 [Google Scholar]
  98. Liu JZ, Horstman HD, Braun E, Graham MA, Zhang C. 98.  et al. 2011. Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiol. 157:1363–78 [Google Scholar]
  99. Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R. 99.  et al. 2012. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256–60Revealed a novel type of resistance gene encoding a serine hydroxymethyltransferase. [Google Scholar]
  100. Loehrer M, Langenbach C, Goellner K, Conrath U, Schaffrath U. 100.  2008. Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol. Plant-Microbe Interact. 21:1421–30 [Google Scholar]
  101. Ma W, Dong FF, Stavrinides J, Guttman DS. 101.  2006. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLOS Genet. 2:e209 [Google Scholar]
  102. Ma W, Guttman DS. 102.  2008. Evolution of prokaryotic and eukaryotic virulence effectors. Curr. Opin. Plant Biol. 11:412–19 [Google Scholar]
  103. Mackey D, Holt BF 3rd, Wiig A, Dangl JL. 103.  2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–54 [Google Scholar]
  104. Meksem K, Zobrist K, Ruben E, Hyten D, Quanzhou T. 104.  et al. 2000. Two large-insert soybean genomic libraries constructed in a binary vector: applications in chromosome walking and genome wide physical mapping. Theor. Appl. Genet. 101:747–55 [Google Scholar]
  105. Meyer JD, Silva DC, Yang C, Pedley KF, Zhang C. 105.  et al. 2009. Identification and analyses of candidate genes for Rpp4-mediated resistance to Asian soybean rust in soybean. Plant Physiol. 150:295–307 [Google Scholar]
  106. Mitchum MG, Wang X, Wang J, Davis EL. 106.  2012. Role of nematode peptides and other small molecules in plant parasitism. Annu. Rev. Phytopathol. 50:175–95 [Google Scholar]
  107. Morales AMAP, O’Rourke JA, van de Mortel M, Scheider KT, Bancroft TJ. 107.  et al. 2013. Transcriptome analyses and virus induced gene silencing identify genes in the Rpp4-mediated Asian soybean rust resistance pathway. Funct. Plant Biol. 40:1029–47 [Google Scholar]
  108. Napoli C, Staskawicz B. 108.  1987. Molecular characterization and nucleic acid sequence of an avirulence gene from race 6 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:572–78 [Google Scholar]
  109. Noon JB, Hewezi TAF, Maier TR, Simmons C, Wei J-Z. 109.  et al. 2015. Eighteen new candidate effectors of the phytonematode Heterodera glycines produced specifically in the secretory esophageal gland cells during parasitism. Phytopathology 105:1362–72 [Google Scholar]
  110. Nunes CC, Dean RA. 110.  2012. Host-induced gene silencing: a tool for understanding fungal host interaction and for developing novel disease control strategies. Mol. Plant Pathol. 13:519–29 [Google Scholar]
  111. Olspert A, Chung BY, Atkins JF, Carr JP, Firth AE. 111.  2015. Transcriptional slippage in the positive-sense RNA virus family Potyviridae. EMBO Rep. 16:995–1004 [Google Scholar]
  112. Pandey AK, Yang C, Zhang C, Graham MA, Horstman HD. 112.  et al. 2011. Functional analysis of the Asian soybean rust resistance pathway mediated by Rpp2. Mol. Plant-Microbe Interact. 24:194–206Demonstrated the feasibility of large-scale gene function studies in soybean using VIGS. [Google Scholar]
  113. Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS. 113.  et al. 2010. A nematode effector protein similar to annexins in host plants. J. Exp. Bot. 61:235–48 [Google Scholar]
  114. Petre B, Kamoun S. 114.  2014. How do filamentous pathogens deliver effector proteins into plant cells?. PLOS Biol. 12:e1001801 [Google Scholar]
  115. Qiao Y, Liu L, Xiong Q, Flores C, Wong J. 115.  et al. 2013. Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45:330–33First report on effectors with RNA silencing suppression activity in eukaryotic pathogens. [Google Scholar]
  116. Qiao Y, Shi J, Zhai Y, Hou Y, Ma W. 116.  2015. Phytophthora effector targets a novel component of small RNA pathway in plants to promote infection. PNAS 112:5850–55 [Google Scholar]
  117. Qutob D, Chapman BP, Gijzen M. 117.  2013. Transgenerational gene silencing causes gain of virulence in a plant pathogen. Nat. Commun. 4:1349Revealed that eukaryotic plant pathogens use epigenetic changes to regulate expression of avirulence genes. [Google Scholar]
  118. Qutob D, Kamoun S, Gijzen M. 118.  2002. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J. 32:361–73 [Google Scholar]
  119. Qutob D, Tedman-Jones J, Dong S, Kuflu K, Pham H. 119.  et al. 2009. Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a. PLOS ONE 4:e5066 [Google Scholar]
  120. Rajput NA, Zhang M, Ru Y, Liu T, Xu J. 120.  et al. 2014. Phytophthora sojae effector PsCRN70 suppresses plant defenses in Nicotiana benthamiana. PLOS ONE 9:e98114 [Google Scholar]
  121. Rambani A, Rice JH, Liu J, Lane T, Ranjan P. 121.  et al. 2015. The methylome of soybean roots during the compatible interaction with the soybean cyst nematode. Plant Physiol. 168:1364–77First report on soybean genome-wide DNA methylation patterns in response to SCN infection. [Google Scholar]
  122. Replogle A, Wang J, Bleckmann A, Hussey RS, Baum TJ. 122.  et al. 2011. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant J. 65:430–40 [Google Scholar]
  123. Replogle A, Wang J, Paolillo V, Smeda J, Kinoshita A. 123.  et al. 2013. Synergistic interaction of CLAVATA1, CLAVATA2, and RECEPTOR-LIKE PROTEIN KINASE2 in cyst nematode parasitism of Arabidopsis. Mol. Plant-Microbe Interact. 26:87–96 [Google Scholar]
  124. Rose JKC, Ham K-S, Darvill AG, Albersheim P. 124.  2002. Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens. Plant Cell 14:1329–45 [Google Scholar]
  125. Schmitz RJ, He Y, Valdés-López O, Khan SM, Joshi T. 125.  et al. 2013. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. 23:1663–74 [Google Scholar]
  126. Schneider KT, van de Mortel M, Bancroft TJ, Braun E, Nettleton D. 126.  et al. 2011. Biphasic gene expression changes elicited by Phakopsora pachyrhizi in soybean correlate with fungal penetration and haustoria formation. Plant Physiol. 157:355–71 [Google Scholar]
  127. Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M. 127.  et al. 2010. Ancient class of translocated oomycete effectors targets the host nucleus. PNAS 107:17421–26 [Google Scholar]
  128. Selote D, Kachroo A. 128.  2010. RPG1-B-derived resistance to AvrB-expressing Pseudomonas syringae requires RIN4-like proteins in soybean. Plant Physiol. 153:1199–211 [Google Scholar]
  129. Selote D, Robin GP, Kachroo A. 129.  2013. GmRIN4 protein family members function nonredundantly in soybean race-specific resistance against Pseudomonas syringae. New Phytol. 197:1225–35 [Google Scholar]
  130. Selote D, Shine MB, Robin GP, Kachroo A. 130.  2014. Soybean NDR1-like proteins bind pathogen effectors and regulate resistance signaling. New Phytol. 202:485–98 [Google Scholar]
  131. Seo JK, Lee SH, Kim KH. 131.  2009. Strain-specific cylindrical inclusion protein of Soybean mosaic virus elicits extreme resistance and a lethal systemic hypersensitive response in two resistant soybean cultivars. Mol. Plant-Microbe Interact. 22:1151–59 [Google Scholar]
  132. Shen D, Liu T, Ye W, Liu L, Liu P. 132.  et al. 2013. Gene duplication and fragment recombination drive functional diversification of a superfamily of cytoplasmic effectors in Phytophthora sojae. PLOS ONE 8:e70036 [Google Scholar]
  133. Silva DC, Yamanaka N, Brogin RL, Arias CA, Nepomuceno AL. 133.  et al. 2008. Molecular mapping of two loci that confer resistance to Asian rust in soybean. Theor. Appl. Genet. 117:57–63 [Google Scholar]
  134. Sohn KH, Lei R, Nemri A, Jones JDG. 134.  2007. The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19:4077–90 [Google Scholar]
  135. Song J, Win J, Tian M, Schornack S, Kaschani F. 135.  et al. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. PNAS 106:1654–59 [Google Scholar]
  136. Specht JE, Diers BW, Nelson RL, Francisco J, de Toledo F. 136.  et al. 2014. Soybean. Yield Gains in Major U.S. Field Crops S Smith, B Diers, J Specht, B Carver 311–51 Madison, WI: Am. Soc. Agron. [Google Scholar]
  137. Stam R, Jupe J, Howden AJ, Morris JA, Boevink PC. 137.  et al. 2013. Identification and characterisation CRN effectors in Phytophthora capsici shows modularity and functional diversity. PLOS ONE 8:e59517 [Google Scholar]
  138. Staskawicz B, Dahlbeck D, Keen N, Napoli C. 138.  1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789–94 [Google Scholar]
  139. Staskawicz BJ, Dahlbeck D, Keen NT. 139.  1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. PNAS 81:6024–28 [Google Scholar]
  140. Stassen JH, Van den Ackerveken G. 140.  2011. How do oomycete effectors interfere with plant life?. Curr. Opin. Plant Biol. 14:407–14 [Google Scholar]
  141. Suh SJ, Bowman BC, Jeong N, Yang K, Kastl C. 141.  et al. 2011. The Rsv3 locus conferring resistance to Soybean mosaic virus is associated with a cluster of coiled-coil nucleotide-binding leucine-rich repeat genes. Plant Genome 4:55–64 [Google Scholar]
  142. Sumit R, Sahu BB, Xu M, Sandhu D, Bhattacharyya MK. 142.  2012. Arabidopsis nonhost resistance gene PSS1 confers immunity against an oomycete and a fungal pathogen but not a bacterial pathogen that cause diseases in soybean. BMC Plant Biol. 12:87 [Google Scholar]
  143. Tyler BM. 143.  2007. Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol. Plant Pathol. 8:1–8 [Google Scholar]
  144. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY. 144.  et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–66 [Google Scholar]
  145. van de Mortel M, Recknor JC, Graham MA, Nettleton D, Dittman JD. 145.  et al. 2007. Distinct biphasic mRNA changes in response to Asian soybean rust infection. Mol. Plant-Microbe Interact. 20:887–99 [Google Scholar]
  146. Vanholme B, Van Thuyne W, Vanhouteghem K, De Meutter J, Cannoot B, Gheysen G. 146.  2007. Molecular characterization and functional importance of pectate lyase secreted by the cyst nematode Heterodera schachtii. Mol. Plant Pathol. 8:267–78 [Google Scholar]
  147. Vijayapalani P, Maeshima M, Nagasaki-Takekuchi N, Miller WA. 147.  2012. Interaction of the trans-frame potyvirus protein P3N-PIPO with host protein PCaP1 facilitates potyvirus movement. PLOS Pathog. 8:e1002639 [Google Scholar]
  148. Wang J, Lee C, Replogle A, Joshi S, Korkin D. 148.  et al. 2010. Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol. 187:1003–17 [Google Scholar]
  149. Wang J, Shine MB, Gao QM, Navarre D, Jiang W. 149.  et al. 2014. Enhanced Disease Susceptibility1 mediates pathogen resistance and virulence function of a bacterial effector in soybean. Plant Physiol. 165:1269–84 [Google Scholar]
  150. Wang L, Eggenberger AL, Hill J, Bogdanove AJ. 150.  2006. Pseudomonas syringae effector avrB confers soybean cultivar-specific avirulence on Soybean mosaic virus adapted for transgene expression but effector avrPto does not. Mol. Plant-Microbe Interact. 19:304–12 [Google Scholar]
  151. Wang Q, Han C, Ferreira AO, Yu X, Ye W. 151.  et al. 2011. Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 23:2064–86A systematic analysis on RxLR effector expression and function in P. sojae. [Google Scholar]
  152. Wang X, Allen R, Ding X, Goellner M, Maier T. 152.  et al. 2001. Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant-Microbe Interact. 14:536–44 [Google Scholar]
  153. Wang X, Meyers D, Yan Y, Baum T, Smant G. 153.  et al. 1999. In planta localization of a β-1,4-endoglucanase secreted by Heterodera glycines. Mol. Plant-Microbe Interact. 12:64–67 [Google Scholar]
  154. Wang X, Mitchum MG, Gao B, Li C, Diab H. 154.  et al. 2005. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol. Plant Pathol. 6:187–91 [Google Scholar]
  155. Wei T, Zhang C, Hong J, Xiong R, Kasschau KD. 155.  et al. 2010. Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLOS Pathog. 6:e1000962 [Google Scholar]
  156. Wen RH, Hajimorad MR. 156.  2010. Mutational analysis of the putative pipo of Soybean mosaic virus suggests disruption of PIPO protein impedes movement. Virology 400:1–7 [Google Scholar]
  157. Wen RH, Khatabi B, Ashfield T, Saghai Maroof MA, Hajimorad MR. 157.  2013. The HC-Pro and P3 cistrons of an avirulent Soybean mosaic virus are recognized by different resistance genes at the complex Rsv1 locus. Mol. Plant-Microbe Interact. 26:203–15Demonstrated that different genes at the Rsv1 locus recognize the SMV HC-Pro and P3 avirulence determinants. [Google Scholar]
  158. Wen RH, Saghai Maroof MA, Hajimorad MR. 158.  2011. Amino acid changes in P3, and not the overlapping pipo-encoded protein, determine virulence of Soybean mosaic virus on functionally immune Rsv1-genotype soybean. Mol. Plant Pathol. 12:799–807 [Google Scholar]
  159. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG. 159.  et al. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115–18 [Google Scholar]
  160. Whitham SA, Eggenberger AL, Zhang C, Chowda-Reddy RV, Martin KM, Hill JH. 160.  2015. Recent advances in in planta transient expression and silencing systems for soybean using viral vectors. Recent Advancements in Gene Expression and Enabling Technologies in Crop Plants K Azhakanandam, A Silverstone, H Daniell, MR Davey 423–51 New York: Springer [Google Scholar]
  161. Win J, Krasileva KV, Kamoun S, Shirasu K, Staskawicz BJ, Banfield MJ. 161.  2012. Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic oomycete species. PLOS Pathog. 8:e1002400 [Google Scholar]
  162. Wong J, Gao L, Yang Y, Zhai J, Arikit S. 162.  et al. 2014. Roles of small RNAs in soybean defense against Phytophthora sojae infection. Plant J. 79:928–40 [Google Scholar]
  163. Wrather JA, Koenning SR. 163.  2009. Effects of diseases on soybean yields in the United States 1996 to 2007. Plant Health Prog. doi: 10.1094/PHP-2009-0401-01-RS
  164. Xiong Q, Ye W, Choi D, Wong J, Qiao Y. 164.  et al. 2014. Phytophthora suppressor of RNA silencing 2 is a conserved RxLR effector that promotes infection in soybean and Arabidopsis thaliana. Mol. Plant-Microbe Interact. 27:1379–89 [Google Scholar]
  165. Yamagishi N, Yoshikawa N. 165.  2009. Virus-induced gene silencing in soybean seeds and the emergence stage of soybean plants with Apple latent spherical virus vectors. Plant Mol. Biol. 71:15–24 [Google Scholar]
  166. Yang Y, Zheng G, Han L, Dagang W, Yang X. 166.  et al. 2013. Genetic analysis and mapping of genes for resistance to multiple strains of Soybean mosaic virus in a single resistant soybean accession PI 96983. Theor. Appl. Genet. 126:1783–91 [Google Scholar]
  167. Ye W, Wang Y, Wang Y. 167.  2015. Bioinformatics analysis reveals abundant short alpha-helices as a common structural feature of oomycete RxLR effector proteins. PLOS ONE 10:e0135240 [Google Scholar]
  168. Yu A, Lepere G, Jay F, Wang J, Bapaume L. 168.  et al. 2013. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. PNAS 110:2389–94 [Google Scholar]
  169. Yu N, Kim M, King ZR, Harris DK, Buck JW. 169.  et al. 2015. Fine mapping of the Asian soybean rust resistance gene Rpp2 from soybean PI 230970. Theor. Appl. Genet. 128:387–96 [Google Scholar]
  170. Zhang C, Bradshaw JD, Whitham SA, Hill JH. 170.  2010. The development of an efficient multipurpose Bean pod mottle virus viral vector set for foreign gene expression and RNA silencing. Plant Physiol. 153:52–65 [Google Scholar]
  171. Zhang C, Grosic S, Whitham SA, Hill JH. 171.  2012. The requirement of multiple defense genes in soybean Rsv1-mediated extreme resistance to Soybean mosaic virus. Mol. Plant-Microbe Interact. 25:1307–13 [Google Scholar]
  172. Zhang C, Hajimorad MR, Eggenberger AL, Tsang S, Whitham SA, Hill JH. 172.  2009. Cytoplasmic inclusion cistron of Soybean mosaic virus serves as a virulence determinant on Rsv3-genotype soybean and a symptom determinant. Virology 391:240–48 [Google Scholar]
  173. Zhang M, Li Q, Liu T, Liu L, Shen D. 173.  et al. 2015. Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases. Plant Physiol. 167:164–75 [Google Scholar]
  174. Zhou H, Lin J, Johnson A, Morgan RL, Zhong W, Ma W. 174.  2011. Pseudomonas syringae type III effector HopZ1 targets a host enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell Host Microbe 9:177–86Revealed that a P. syringae effector protein suppresses resistance by inhibiting phytoalexin production. [Google Scholar]
  175. Zhou H, Morgan RL, Guttman DS, Ma W. 175.  2009. Allelic variants of the Pseudomonas syringae type III effector HopZ1 are differentially recognized by plant resistance systems. Mol. Plant-Microbe Interact. 22:176–89 [Google Scholar]
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