**Author details**

Vincent P. Klink1\*, Prachi D. Matsye1 , Katheryn S. Lawrence2 and Gary W. Lawrence3

\*Address all correspondence to: vklink@biology.msstate.edu

1 Department of Biological Sciences, Mississippi State University, Mississippi State, MS, U.S.A.

2 Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Missis‐ sippi State University, Mississippi State, MS,, U.S.A.

3 Department of Entomology and Plant Pathology, Auburn University, Auburn, AL, U.S.A.

## **References**


[4] Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y. 2006. Endoge‐ nous and synthetic microRNAs stimulate simultaneous, efficient, and localized regu‐ lation of multiple targets in diverse species. Plant Cell 18: 1134-1151

[16] Bird D McK, Wilson MA. 1994. DNA sequence and expression analysis of root-knot

Engineered Soybean Cyst Nematode Resistance

http://dx.doi.org/10.5772/54514

161

[17] Bradley EB, Duffy M. 1982. The value of plant resistance to soybean cyst nematode: a case study of Forrest soybeans. National Resource Economics Staff Report No.

[18] Brucker E, Carlson S, Wright E, Niblack T, Diers B. 2005. Rhg1 alleles from soybean PI 437654 and PI 88788 respond differently to isolates of Heterodera glycines in the

[19] C. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. ele‐

[20] Caldwell BE, Brim CA, Ross JP. 1960. Inheritance of resistance of soybeans to the soy‐

[21] Caudy AA, Ketting RF, *Hammond* SM, Denli AM, Bathoorn AM, Tops BB, Silva JM, Myers MM, Hannon GJ, Plasterk RH. 2003. A micrococcal nuclease homologue in

[22] Chapin III FS, Shaver GR. 1985. Individualistic growth response of tundra plant spe‐

[23] Chen W, Chao G, Singh KB. 1996. The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites.

[24] Chen SY, Dickson DW. 1996. Pathogenicity of fungi to eggs of *Heterodera glycines*.

[25] Chen X, MacDonald MH. Khan F, Garrett WM, Matthews BF, Natarajan SS. 2011. Two-dimentional proteome reference maps for the soybean cyst nematode Hetero‐

[26] Chitwood DG, Lusby WR: Metabolism of plant sterols by nematodes. *Lipids* 1990, 26:

[27] Clary DO, Griff IC, Rothman JE. 1990. SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell 61: 709–721

[28] Colgrove AL, Niblack TL. 2008. Correlation of female indices from virulence assays on inbred lines and field populations of Heterodera glycines. J Nematol 40: 39–45

[29] Collier R, Fuchs B, Walter N, Kevin Lutke W, Taylor CG. 2005. Ex vitro composite

[30] Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Hückel‐ hoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P. 2003. SNARE-

protein mediated disease resistance at the plant cell wall. Nature 425: 973–977

plants: an inexpensive, rapid method for root biology. Plant J 43: 449-457

cies to environmental manipulations in the field. Ecology 66: 564–576

AGES820929, USDA. Washington DC: U.S. Government Printing Office

gans: a platform for investigating biology. Science 282: 2012-2018

bean cyst nematode, *Heterodera glycines*. Agron J 52: 635-636

nematode-elicited giant cell transcripts. MPMI 7:419-424

greenhouse. Theor Appl Genet 111: 44-49

*RNAi* effector complexes. Nature 425: 411-414

Plant J 10: 955-966

619-627

Journal of Nematology 28: 148-158

dera glycines. Proteomics 11: 4742-4746


[16] Bird D McK, Wilson MA. 1994. DNA sequence and expression analysis of root-knot nematode-elicited giant cell transcripts. MPMI 7:419-424

[4] Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y. 2006. Endoge‐ nous and synthetic microRNAs stimulate simultaneous, efficient, and localized regu‐

[5] An Q, Ehlers K, Kogel KH, van Bel AJ, Hückelhoven R. 2006a. Multivesicular com‐ partments proliferate in susceptible and resistant MLA12-barley leaves in response to

[6] An Q, Hückelhoven R, Kogel KH, van Bel AJ. 2006b. Multivesicular bodies partici‐ pate in a cell wall-associated defence response in barley leaves attacked by the patho‐

[7] Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H. 2004. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for

[8] Atkinson HJ, Harris PD. 1989. Changes in nematode antigens recognized by mono‐ clonal antibodies during early infections of soya bean with cyst nematode Hetero‐

[9] Bakhetia M, Urwin PE, Atkinson HJ. 2007. QPCR analysis and RNAi define pharyng‐ eal gland cell-expressed genes of Heterodera glycines required for initial interactions

[10] Bakhetia M, Urwin PE, Atkinson HJ. 2008. Characterisation by RNAi of pioneer genes expressed in the dorsal pharyngeal gland cell of Heterodera glycines and the

[11] Barker KR, Koenning SR, Huber SC, Huang JS. 1993. Physiological and structural re‐ sponses of plants to nematode parasitism with Glycine max-Heterodera glycines as a model system. Pp. 761-771 in DR Buxon R Shibles RA Forsberg BL Blad KH Asay GM Paulsen and RF Wilson, Eds. International Crop Science I: Madison, WI: Crop

[12] Bekal S, Niblack TL, Lambert KN. 2003. A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence.

[13] Bekal S, Craig JP, Hudson ME, Niblack TL, Domier LL, Lambert KN. 2008. Genomic DNA sequence comparison between two inbred soybean cyst nematode biotypes fa‐ cilitated by massively parallel 454 micro-bead sequencing. Mol Genet Genomics

[14] Bennett MK, Calakos N, Scheller RH. 1992. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257: 255-259

[15] Bernard RL, Juvik GA, Nelson RL. 1987. USDA Soybean Germplasm Collection In‐ ventory, Vol. 2. INTSOY Series Number 31. IL: International Agriculture Publica‐

infection by the biotrophic powdery mildew fungus. New Phytol 172: 563-57

lation of multiple targets in diverse species. Plant Cell 18: 1134-1151

genic powdery mildew fungus. Cell Microbiol 8: 1009-1019

the timely assembly of papillae. Mol Biol Cell 15: 5118-5129

with the host. *Mol Plant Microbe Interact* 20: 306-312

Molecular Plant-Microbe Interactions 16: 439-446

effects of combinatorial RNAi. *Int J Parasitol* 38: 1589-1597

dera glycines. Parasitology 98: 479-487

Science Society of America

tions, University of Illinois

279:535-543

160 Soybean - Pest Resistance


[31] Concibido VC, Denny RL, Boutin SR, Hautea R, Orf JH, Young ND. 1994. DNA Marker analysis of loci underlying resistance to soybean cyst nematode (*Heterodera glycines* Ichinohe). Crop Sci 34: 240–246

[44] Endo BY. 1965. Histological responses of resistant and susceptible soybean varieties, and backcross progeny to entry development of *Heterodera glycines*. Phytopathology

Engineered Soybean Cyst Nematode Resistance

http://dx.doi.org/10.5772/54514

163

[45] Endo BY. 1991. Ultrastructure of initial responses of susceptible and resistant soy‐

[46] Endo BY, Veech JA. 1970. Morphology and histochemistry of soybean roots infected

[47] Epps JM, Chambers AY. 1958. New host records for Heterodera glycines including

[48] Epps JM, Hartwig EE. 1972. Reaction of soybean varieties and strains to soybean cyst

[49] Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 1998. Potent and specific genetic interference by doublestranded RNA in Caenohrabditis elegans. Na‐

[50] Francl LJ, Dropkin VH. 1986. Heterodera glycines population dynamics and relation

[51] Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS. 2001. Identification of puta‐ tive parasitism genes expressed in the esophageal gland cells of the soybean cyst

[52] Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS. 2003. The parasitome of the phytonematode Heterodera glycines. Mol Plant Microbe Interact 16: 720-726

[53] Garner WW, Allard HA. 1930. Photoperiodic response of soybeans in relation to tem‐

[54] Gipson I, Kim KS, Riggs RD. 1971. An ultrastructural study of syncytium develop‐ ment in soybean roots infected with *Heterodera glycines*. Phytopathology 61: 347-353

[55] Golden AM, Epps JM, Riggs RD, Duclos LA, Fox JA, Bernard RL. 1970. Terminology and identity of infraspecific forms of the soybean cyst nematode (Heterodera gly‐

[56] Goto S, Bono H, Ogata H, Fujibuchi W, Nishioka T, Sato K, Kanehisa M. 1997. Organ‐ izing and computing metabolic pathway data in terms of binary relations. Pac Symp

[57] Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ. 2001. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science. 293: 1146-1150

[58] Hardham AR, Takemoto D, White RG. 2008. Rapid and dynamic subcellular reorgan‐ ization following mechanical stimulation of Arabidopsis epidermal cells mimics re‐

sponses to fungal and oomycete attack. BMC Plant Biol 8: 63

perature and other environmental factors. J. Agric. Res. 41:719-735

nematode Heterodera glycines. *Mol Plant Microbe Interact* 2001, 14:1247-1254.

of initial population density tp soybean yield. Plant Disease: 70: 791-795

bean roots to infection by *Heterodera glycines*. Revue Nématol 14: 73-84

with *Heterodera glycines*. Phytopathology 60: 1493–1498

one in the Labiate. Plant Disease Reporter 42: 194

nematode. J Nematol 4: 222

cines). Plant Dis Rep 54: 544–546

Biocomput. 1997: 175-186

ture 391:806–811

55: 375–381


[44] Endo BY. 1965. Histological responses of resistant and susceptible soybean varieties, and backcross progeny to entry development of *Heterodera glycines*. Phytopathology 55: 375–381

[31] Concibido VC, Denny RL, Boutin SR, Hautea R, Orf JH, Young ND. 1994. DNA Marker analysis of loci underlying resistance to soybean cyst nematode (*Heterodera*

[32] Concibido VC, Diers BW, Arelli PR. 2004. A decade of QTL mapping for cyst nema‐

[33] Creech JE, Johnson WG. 2006. Survey of broadleaf winter weeds in Indiana produc‐ tion fields infested with soybean cyst nematode (*Heterodera glycines*). Weed Technol.

[34] Cregan PB, Mudge J, Fickus EW, Danesh D, Denny R, Young ND. 1999a. Two simple sequence repeat markers to select for soybean cyst nematode resistance conditioned

[35] Cregan PB, Mudge J, Fickus EW, Marek LF, Danesh D, Denny R, Shoemaker RC, Matthews BF, Jarvik T, Young ND. 1999b. Targeted isolation of simple sequence re‐ peat markers through the use of bacterial artificial chromosomes. Theor Appl Genet

[36] Day TA, Ruhland CT, Grobe CW, Xiong F. 1999. Growth and reproduction of Antarc‐ tic vascular plants in response to warming and UV radiation reductions in the field.

[37] De Boer JM, Yan Y, Wang X, Smant G, ussey RS, Davis EL. 1999. Developmentla ex‐ pression of secretory beta 1, 4-endonucleases in the subventral esophageal glands of

[38] De Boer JM, Mc Dermott JP, Davis EL; Husses RS, Popeijus H, Smant G, Baum TJ. 2002. Cloning of a putative pectate lyase gene expressed in the subventral esophageal

[39] Doyle JJ, Doyle JL, Brown AH. 1999. Origins, colonization, and lineage recombina‐ tion in a widespread perennial soybean polyploid complex. Proc Natl Acad Sci 96:

[40] Edens RM, Anand SC, Bolla RI. 1995. Enzymes of the phenylpropanoid pathway in soybean infected with Meloidogyne incognita or Heterodera glycines. J Nematology.

[41] Elling AA, Mitreva M, Gai X, Martin J, Recknor J, Davis EL, Hussey RS, Nettleton D,McCarter JP, Baum TJ. 2009. Sequence mining and transcript profiling to explore

[42] Emmert-Buck MR, Bonner RF, Smith PD, Chuaqui RF, Zhuang Z, Goldstein SR, Weiss RA, Liotta LA. 1996. Laser capture microdissection. Science 274: 998–1001

[43] Endo BY. 1964. Penetration and development of *Heterodera glycines* in soybean roots

and related and related anatomical changes. Phytopathology 54: 79–88

Heterodera glycines. Molecular Plant-Microbe Interactions 12: 663-669

glands of Heterodera glycines. J. Nematology 34: 9-11

cyst nematode parasitism. BMC Genomics 10: 58

*glycines* Ichinohe). Crop Sci 34: 240–246

20: 1066-1075

162 Soybean - Pest Resistance

98:919–928

10741-10745

27: 292-303

Oecologia 119: 24–35

tode resistance in soybean. Crop Sci. 44: 1121-1131

by the rhg1 locus. Theor Appl Genet 99: 811–818


[59] Haseloff J, Siemering KR, Prasher DC, Hodge S. 1997. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark trans‐ genic Arabidopsis plants brightly. Proc Natl Acad Sci U S A 94: 2122-2127

cines regulates the expression of a large number of stress- and defense-related genes

Engineered Soybean Cyst Nematode Resistance

http://dx.doi.org/10.5772/54514

165

[74] Kalde M, Nühse TS, Findlay K, Peck SC. 2007. The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc

[75] Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J. 2003. Systematic functional analysis of the *Caenorhabditis elegans* genome using RNAi. Nature 421:

[76] Kim DG, Riggs RD. 1991. Characteristics and efficacy of a sterile hyphomycete (ARF18), a new biocontrol agent for *Heterodera glycines* and other nematodes. Journal

[77] Kim DG, Riggs RD. 1995. Efficacy of the nematophagous fungus ARF18 in alginateclay pellet formulation against *Heterodera glycines.* Journal of Nematology 23:275-282

[78] Kim KS, Riggs RD. 1992. Cytopathological reactions of resistant soybean plants to nematode invasion. Pp. 157–168 *in* J. A. Wrather and R. D. Riggs, eds. Biology and

[79] Kim M, Hyten DL, Bent AF, Diers BW. 2010. Fine mapping of the SCN resistance lo‐

[80] Kim YH, Riggs RD, Kim KS. 1987. Structural changes associated with resistance of

[81] Klink VP, MacDonald M, Alkharouf N, Matthews BF. 2005. Laser capture microdis‐ section (LCM) and expression analyses of *Glycine max* (soybean) syncytium contain‐ ing root regions formed by the plant pathogen *Heterodera glycines* (soybean cyst

[82] Klink VP, Overall CC, Alkharouf N, MacDonald MH, Matthews BF. 2007a. Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean roots infected by

[83] Klink VP, Overall CC, Alkharouf N, MacDonald MH, Matthews BF. 2007b. A compa‐ rative microarray analysis of an incompatible and compatible disease response by soybean (Glycine max) to soybean cyst nematode (Heterodera glycines) infection.

[84] Klink VP, MacDonald MH, Martins VE, Park S-C, Kim K-H, Baek S-H, Matthews BF. 2008. MiniMax, a new diminutive Glycine max variety, with a rapid life cycle, em‐ bryogenic potential and transformation capabilities. Plant Cell, Tissue and Organ

[85] Klink VP, Kim K-H, Martins VE, MacDonald MH, Beard HS, Alkharouf NW, Lee S-K, Park S-C, Matthews BF. 2009a. A correlation between host-mediated expression of

Management of the Soybean Cyst Nematode. St. Paul: APS Press

soybean cyst nematode (*Heterodera glycines*). Planta 226: 1389-1409

cus *rhg1-b* from PI 88788. The Plant Genome 3: 81-89

soybean to *Heterodera glycines*. J Nematol 19: 177–187

nematode). Plant Mol Bio 59: 969-983

Planta 226: 1423-1447

Culture 92: 183-195

in degenerating feeding cells. Plant Physiol 155: 1960-1975

Natl Acad Sci U S A 104: 11850-11855

of Nematology 23: 275–282

231–237


cines regulates the expression of a large number of stress- and defense-related genes in degenerating feeding cells. Plant Physiol 155: 1960-1975

[74] Kalde M, Nühse TS, Findlay K, Peck SC. 2007. The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc Natl Acad Sci U S A 104: 11850-11855

[59] Haseloff J, Siemering KR, Prasher DC, Hodge S. 1997. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark trans‐

[60] Hermsmeier D, Mazarei M, Baum TJ. 1998. Differential display analysis of the early compatible interaction between soybean and the soybean cyst nematode. Molecular

[61] Hofius D, Schultz-Larsen T, Joensen J, Tsitsigiannis DI, Petersen NH, Mattsson O, Jørgensen LB, Jones JD, Mundy J, Petersen M. 2009. Autophagic components contrib‐

[62] Huang G, Allen R, Davis EL, Baum TJ, Hussey RS. 2006. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-

knot nematode parasitism gene. Proc Natl Acad Sci USA 103: 14302-14306

[63] Hymowitz t. 1970. On the domestication of soybean. Economic Botany 24: 408-421

[64] Hyten DL, Choi IY, Song Q, Shoemaker RC, Nelson RI, Costa JM, Specht JE, Cregan PB. 2010. Highly variable patterns of linkage disequilibrium in multiple soybean

[65] Ichinohe M. 1952. On the soybean nematode, Heterodera glycines n. sp., from Japan.

[66] Ichinohe M. 1961. Studies on the soybean cyst nematode, *Heterodera glycines* Hakkai‐

[67] Inagaki H, Tsutsumi M. 1971. Survival of the soybean cyst nematode, Heterodera glycines Ichinohe (Tylenchida: Heteroderidae) under certain storage conditions.

[68] Inoue A, Obata K, Akagawa K. 1992. Cloning and sequence analysis of cDNA for a

[69] Isenberg G, Bielser W, Meier-Ruge W, Remy E. 1976. Cell surgery by laser micro-dis‐

[70] Ithal N, Recknor J, Nettleston D, Hearne L, Maier T, Baum TJ, Mitchum MG. 2007. Developmental transcript profiling of cyst nematode feeding cells in soybean roots.

[71] Jones MGK. 1981. The development and function of plant cells modified by endopar‐ asitic nematodes. Pages 255-279 in: Plant Parasitic Nematodes, Vol. III. B. M. Zucker‐

[72] Jones MGK, Northcote DH. 1972. Nematode-induced syncytium-a multinucleate

[73] Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D, Baum TJ, Mitchum MG. 2011. The Soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera gly‐

neuronal cell membrane antigen, HPC-1. J Biol Chem 267: 10613-10619

genic Arabidopsis plants brightly. Proc Natl Acad Sci U S A 94: 2122-2127

ute to hypersensitive cell death in Arabidopsis. Cell 137: 773-783

Plant-Microbe Interactions 11: 1258-1263

164 Soybean - Pest Resistance

populations. Genetics 175: 1937-1944

Magazine of Applied Zoology 17: 1-4

Appl Entomol Zool (Jpn) 8: 53–63

transfer cell. J Cell Sci 10: 789–809

do National Experiment Station Report no. 56

section: a preparative method. J. Microsc 107: 19–24

Molecular Plant-Microbe Interactions 20: 293-305

man and R. A. Rohde, eds. Academic Press, New York, U.S.A.


parasite genes as tandem inverted repeats and abrogation of the formation of female Heterodera glycines cysts during infection of Glycine max. Planta 230: 53-71

[96] Lenz HD, Haller E, Melzer E, Kober K, Wurster K, Stahl M, Bassham DC, Vierstra RD, Parker JE, Bautor J, Molina A, Escudero V, Shindo T, van der Hoorn RA, Gust AA, Nürnberger T. 2011. Autophagy differentially controls plant basal immunity to

Engineered Soybean Cyst Nematode Resistance

http://dx.doi.org/10.5772/54514

167

[97] Li J, Todd TC, Oakley TR, Lee J and Trick HN. 2010. Host derived suppression of nematode reproductive and fitness genes decreases fecundity of *Heterodera glycines*.

[98] Li Y-H, Qi X-T, Chang R and Qiu L-J. 2011. Evaluation and Utilization of Soybean Germplasm for Resistance to Cyst Nematode in China. in *Soybean - Molecular Aspects*

[99] Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P. 2005. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabi‐

[100] Liu X, Z, Chen SY. 2001. Screening isolates of *Hirsutella* species for biocontrol of *Het‐*

[101] Liu XZ, Li JQ, Zhang DS. 1997. History and status of soybean cyst nematode in Chi‐

[102] Ma Y, Wang W, Liu X, Ma F, Wang P, Chang R, Qiu L. 2006. Characteristics of soy‐ bean genetic diversity and establishment of applied core collection for Chinese soy‐

[103] Mahalingham R, Skorupska HT. 1996. Cytological expression of early response to in‐ fection by Heterodera glycines Ichinohe in resistant PI 437654 soybean. Genome 39:

[104] Mahalingam R, Wang G, Knap HT. 1999. Polygalacturonidase and polygalacturoni‐ dase inhibitor protein: gene isolation and transcription in Glycine max-Heterodera

[105] Malhotra V, Orci L, Glick BS, Block MR, Rothman JE. 1988. Role of an N-ethylmalei‐ mide-sensitive transport component in promoting fusion of transport vesicles with

[106] Matson AL, Williams LF. 1965. Evidence of a fourth gene for resistance to the soy‐

[107] Matsye PD, Kumar R, Hosseini P, Jones CM, Alkharouf N, Matthews BF, Klink VP. 2011. Mapping cell fate decisions that occur during soybean defense responses. Plant

[108] Matsye PD, Lawrence GW, Youssef RM, Kim K-H, Lawrence KS, Matthews BF, Klink VP. 2012. The expression of a naturally occurring mutant of an alpha soluble NSF at‐

glycines interactions. Molecular Plant-Microbe Interactions 12: 490-498

bean cyst nematode resistance. Journal of Intergrative Biology 48: 722-731

biotrophic and necrotrophic pathogens. Plant J 66: 818-830

*of Breeding* pp. 373-396. Ed. Aleksandra Sudaric. Intech Publishers

*erodera glycines.* Biocontrol Science and Technology 11:151-160

na. International Journal of Nematology 7: 18-25

cisternae of the Golgi stack. Cell 54: 221–227

bean cyst nematode. Crop Sci. 5: 477

Mol Bio 77: 513-528

Planta 232: 775-785

986–998

dopsis. Science 310: 1180-1183


[96] Lenz HD, Haller E, Melzer E, Kober K, Wurster K, Stahl M, Bassham DC, Vierstra RD, Parker JE, Bautor J, Molina A, Escudero V, Shindo T, van der Hoorn RA, Gust AA, Nürnberger T. 2011. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J 66: 818-830

parasite genes as tandem inverted repeats and abrogation of the formation of female

Heterodera glycines cysts during infection of Glycine max. Planta 230: 53-71

*Heterodera glycines* (soybean cyst nematode) Plant Mol Bio: 71: 525-567

the roots of the Glycine max genotype Peking. BMC-Genomics 10: 111

Distributors, India.

166 Soybean - Pest Resistance

technology 1-30

[86] Klink VP, Hosseini P, Matsye P, Alkharouf N, Matthews BF. 2009b. A gene expres‐ sion analysis of syncytia laser microdissected from the roots of the *Glycine max* (soy‐ bean) genotype PI 548402 (Peking) undergoing a resistant reaction after infection by

[87] Klink VP, Hosseini P, MacDonald MH, Alkharouf N, Matthews BF. 2009c. Popula‐ tion-specific gene expression in the plant pathogenic nematode Heterodera glycines exists prior to infection and during the onset of a resistant or susceptible reaction in

[88] Klink VP, Matsye PD, Lawrence GW. 2010a. Developmental Genomics of the Resist‐ ant Reaction of Soybean to the Soybean Cyst nematode, Pp. 249-270, In Plant Tissue Culture and Applied Biotechnology. Eds. Kumar A., Roy S. Aavishkar Publishers,

[89] Klink VP, Hosseini P, Matsye P, Alkharouf N, Matthews BF. 2010b. Syncytium gene expression in *Glycine max*[PI 88788] roots undergoing a resistant reaction to the parasitic

[90] Klink VP, Overall CC, Alkharouf N, MacDonald MH, Matthews BF. 2010c. Microar‐ ray detection calls as a means to compare transcripts expressed within syncytial cells isolated from incompatible and compatible soybean (Glycine max) roots infected by the soybean cyst nematode (Heterodera glycines). Journal of Biomedicine and Bio‐

[91] Klink VP, Hosseini P, Matsye PD, Alkharouf N, Matthews BF. 2011a. Differences in gene expression amplitude overlie a conserved transcriptomic program occurring be‐ tween the rapid and potent localized resistant reaction at the syncytium of the *Gly‐ cine max* genotype Peking (PI 548402) as compared to the prolonged and potent

[92] Klink VP, Matsye PD, Lawrence GW. 2011b. Cell-specific studies of soybean resist‐ ance to its major pathogen, the soybean cyst nematode as revealed by laser capture microdissection, gene pathway analyses and functional studies. in *Soybean - Molecu‐*

[93] Koenning SR, Schmitt DP, Barker KR. 1993. Effects of cropping systems on popula‐ tion density of Heterodera glycines and soybean yield. Plant Disease 77: 780-786

[94] Lai Z, Wang F, Zheng Z, Fan B, Chen Z. 2011. A critical role of autophagy in plant

[95] Lambert KN, Allen KD, Sussex IM. 1999. Cloning and characterization of an esopha‐ geal-gland specific chorismate mutase from the phytopathogenic nematode Meloido‐

resistance to necrotrophic fungal pathogens. Plant J 66: 953-968

gyne javanica. Molecular Plant-Microbe Interactions 12: 328-336

*lar Aspects of Breeding* pp. 397-428. Ed. Aleksandra Sudaric. Intech Publishers

resistant reaction of PI 88788. Plant Mol Bio 75: 141-165

nematode *Heterodera glycines* Plant Physiology and Biochemistry 48: 176-193


tachment protein gene in *Glycine max* (soybean) partially suppresses infection by the plant parasitic nematode *Heterodera glycines*. Plant Molecular Biology (in press)

[121] Noel GR. 1992. History, distribution and economics. Pp 1-13 in RD Riggs and JA Wrather, editors. Biology and Management of the soybean cyst nematode. St. Paul,

Engineered Soybean Cyst Nematode Resistance

http://dx.doi.org/10.5772/54514

169

[122] Opperman CH, Bird D McK. 1998. The soybean cyst nematode, *Heterodera glycines:* a genetic model system for the study of plant-parasitic nematodes. Current Opinion in

[123] Oyler GA, Higgins GA, Hart RA, Battenberg E, Billingsley M, Bloom FE, Wilson MC. 1989. The identification of a novel synaptosomal-associated protein, SNAP-25, differ‐

[124] Patel S, Dinesh-Kumar SP. 2008. Arabidopsis ATG6 is required to limit the pathogen-

[125] Piano F, Schetter AJ, Mangone M, Stein L, Kemphues KJ. 2000. RNAi analysis of genes expressed in the ovary of *Caenorhabditis elegans*. Current Biology 10: 1619–1622

[126] Pratt PW, Wrather JA. 1998. Soybean disease loss estimates for the southern United

[127] Puthoff DP, Nettleton D, Rodermel SR, Baum TJ. 2003. *Arabidopsis* gene expression changes during cyst nematode parasitism revealed by statistical analyses of microar‐

[128] Rao-Arelli AP. 1994. Inheritance of resistance to *Heterodera glycines* race 3 in soybean

[129] Riggs RD, Hamblen ML. 1962. Soybean-cyst nematode host studies in the Legumino‐

[130] Riggs RD, Hamblen ML. 1966. Additional weed hosts of *Heterodera glycines*. Plant Dis

[131] Riggs RD, Hamblen ML. 1966. Further studies on the host range of the soybean-cyst

[132] Riggs RD, Schmitt DP. 1988. Complete characterization of the race scheme for Heter‐

[133] Riggs RD, Schmitt DP. 1991. Optimization of the *Heterodera glycines* race test proce‐

[134] Riggs RD, Kim KS, Gipson I. 1973. Ultrastructural changes in Peking soybeans infect‐

[135] Robinson AF, Inserra RN, Caswell-Chen EP, Vovlas N, Troccoli A. 1997. *Rotylenchu‐ lus* species: Identification, distribution, host ranges, and crop plant resistance. Nema‐

[136] Ross JP, Brim CA. 1957. Resistance of soybeans to the soybean cyst nematode as de‐

entially expressed by neuronal subpopulations. J Cell Biol 109: 3039-3052

associated cell death response. Autophagy 4: 20-27

States, 1994-1996. Plant Disease 82: 114-116

ray expression profiles. Plant J 33: 911–921

sae. Ark Agric Exp Stn Rep Series 110 Fayetteville AR 17p

nematode. Ark Agric Exp Stn Bulletin 718 Fayetteville AR 19p

ed with *Heterodera glycines*. Phytopathology 63: 76–84

termined by a double-row method. Plant Dis Rep 41: 923–924

accessions. Plant Dis. 78: 898-900.

odera glycines. J Nematol 20: 392-395

dure. J Nematol 23: 149-154

tropica 27: 127-180

Rep 50: 15-16

MN: APS Press

Plant Biology 1: 1342-1346


[121] Noel GR. 1992. History, distribution and economics. Pp 1-13 in RD Riggs and JA Wrather, editors. Biology and Management of the soybean cyst nematode. St. Paul, MN: APS Press

tachment protein gene in *Glycine max* (soybean) partially suppresses infection by the plant parasitic nematode *Heterodera glycines*. Plant Molecular Biology (in press) [109] McLean MD, Hoover GJ, Bancroft B, Makhmoudova A, Clark SM, Welacky T, Sim‐ monds DH, Shelp BJ. 2007. Identification of the full-length *Hs1pro-1* coding sequence and preliminary evaluation of soybean cyst nematode resistance in soybean trans‐

formed with *Hs1pro-1* cDNA. Canadian Journal of Botany 85: 437-441

chem J 8: 387-401

Applied Nematology 19: 305–308

Crop Sci 37: 1611-1615

pathol 44: 283-303

& Associates of Marceline

Plant Physiol 129: 1241-1251

ington, D.C.: U.S. Dept. of Agriculture. 38 pp

line, MO: Schmitt & Associates of Marceline

*Heterodera glycines*. J Nematol 34: 279-288

36-42

168 Soybean - Pest Resistance

[110] Meier-Ruge W, Bielser W, Remy E, Hillenkamp F, Nitsche R, Unsold R. 1976. The la‐ ser in the Lowry technique for microdissection of freeze-dried tissue slices. Histo‐

[111] Meyer SLF, Huettel RN. 1996. Application of a sex pheromone, pheromone analogs, and *Verticillum lecanii* for management of Heterodera glycines. J. Nematology 28:

[112] Meyer SLF, Meyer RJ. 1996. Greenhouse studies comparing strains of the fungus *Ver‐ ticillium lecanii* for activity against the nematode *Heterodera glycines*. Fundamentals of

[113] Morse WJ. 1927. Soybeans: culture and varieties. Farmer's bulletin NO. 1520. Wash‐

[114] Mudge J, Cregan PB, Kenworthy JP, Kenworthy WJ, Orf JH, Young ND. 1997. Two microsatellite markers that flank the major soybean cyst nematode resistance locus.

[115] Müssig C, Fischer S, Altmann T. 2002. Brassinosteroid-regulated gene expression.

[116] Niblack TL, Chen SY. 2004. Cropping systems and crop management practices. Breeding for resistance and tolerance. Pp. 181-206. *in* D. P. Schmitt, J. A. Wrather, and R. D. Riggs, eds. Biology and management of soybean cyst nematode, 2nd ed. Marce‐

[117] Niblack TL, Heinz RD, Smith GS, Donald PA (1993) Distribution, density, and diver‐

[118] Niblack TL, Arelli PR, Noel GR, Opperman CH, Orf JH, Schmitt DP, Shannon JG, Tylka GL. 2002. A revised classification scheme for genetically diverse populations of

[119] Niblack TL, Lambert KN, Tylka GL. 2006. A model plant pathogen from the king‐ dom animalia: Heterodera glycines, the Soybean Cyst Nematode. Annu Rev Phyto‐

[120] Niblack TL, Riggs RD. 2004. Variation in virulence phenotypes. Breeding for resist‐ ance and tolerance. Pp. 57-71. *in* D. P. Schmitt, J. A. Wrather, and R. D. Riggs, eds. Biology and management of soybean cyst nematode, 2nd ed. Marceline, MO: Schmitt

sity of Heterodera glycines in Missouri. J Nematol 25:880–886


[137] Ross JP. 1958. Host-Parasite relationship of the soybean cyst nematode in resistant soybean roots. Phytopathology 48: 578-579

C, Nitzsche B, Ruer M, Stamford J, Winzi M, Heinkel R, Röder M, Finell J, Häntsch H, Jones SJ, Jones M, Piano F, Gunsalus KC, Oegema K, Gönczy P, Coulson A, Hy‐ man AA, Echeverri CJ. 2005. Full-genome RNAi profiling of early embryogenesis in

Engineered Soybean Cyst Nematode Resistance

http://dx.doi.org/10.5772/54514

171

[149] Spears JF. 1957. Review of soybean cyst nematode situation for presentation at public hearing on the need for Federal Domestic Plant Quarantine, July 24, 1957

[150] Steeves RM, Todd TC, Essig JS, Trick HN. 2006. Transgenic soybeans expressing siR‐ NAs specific to a major sperm protein gene suppress Heterodera glycines reproduc‐

[151] Stein M, Dittgen J, Sánchez-Rodríguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S. 2006. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct pen‐

[152] Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F. 2003. Quantitative nature of Arabidopsis responses during compatible and incom‐ patible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:

[153] Tenllado F, Martı´nez-Garcı´a B, Vargas M, Dı´az-Ruı´z JR. 2003. Crude extracts of bacterially expressed dsRNA can be used to protect plants against virus infections.

[154] Tepfer D. 1984. Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype. Cell 37:

[155] Timmons L, Donald LC, Andrew F (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene

[156] Timper P, Riggs RD, Crippen DL. 1999. Parasitism of sedentary stages of *Heterodera glycines* by isolates of a sterile nematophagous fungus. Phytopathology 89: 1193-1199

[157] Urwin PE, Lilley CJ, Atkinson HJ. 2002. Ingestion of double-stranded RNA by pre‐ parasitic juvenile cyst nematodes leads to RNA interference. *Mol Plant Microbe Inter‐*

[158] Vaghchhipawala Z, Bassuner R, Clayton K, Lewers K, Shoemaker R,m Mackenzie S. 2001. Modulations in gene expression and mapping of genes associated with cyst nematode infection of soybean. Molecular Plant-Microbe Interactions 14: 42-54 [159] Wang D, Stravopodis D, Teglund S, Kitazawa J, Ihle JN. 1996. Naturally occurring

[160] Wang X, Allen R, Ding X, Goellner M, Maier T, DeBoer JM, Baum TJ, Hussey RS, Da‐ vis EL. 2001. Signal peptide-selection of cDNA cloned directly from the esophageal

dominant negative variants of Stat5. Mol Cell Biol 16: 6141-6148

Caenorhabditis elegans. Nature 434: 462-429

tion. Funct Plant Biol 33: 991–999

etration. Plant Cell 18: 731-746

317-330

959-967

263:103–112

*act* 15: 747-752

BMC Biotechnol 3:3


C, Nitzsche B, Ruer M, Stamford J, Winzi M, Heinkel R, Röder M, Finell J, Häntsch H, Jones SJ, Jones M, Piano F, Gunsalus KC, Oegema K, Gönczy P, Coulson A, Hy‐ man AA, Echeverri CJ. 2005. Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434: 462-429

[149] Spears JF. 1957. Review of soybean cyst nematode situation for presentation at public hearing on the need for Federal Domestic Plant Quarantine, July 24, 1957

[137] Ross JP. 1958. Host-Parasite relationship of the soybean cyst nematode in resistant

[138] Ross JP. 1962. Crop rotation effects on the soybean cyst nematode population and

[140] Rosskopf EN, Chellemi DO, Kokalis-Burelle N, Church GT. 2005. Alternatives to Methyl Bromide: A Florida Perspective. American Phytopathological Society. APSnet feature, http://www.apsnet.org/publications/apsnetfeatures/Documents/2005/Meth‐

[141] Sasser JN, Uzzell G, Jr. 1991. Control of the soybean cyst nematode by crop rotation

[142] Scheideler M, Schlaich NL, Fellenberg K, Beissbarth T, Hauser NC, Vingron M, Slu‐ sarenko AJ, Hoheisel JD. 2001. Monitoring the switch from housekeeping to patho‐ gen defense metabolism in *Arabidopsis thaliana* using cDNA arrays. J Biol Chem 277:

[143] Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhatta‐ charyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Good‐ stein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA. 2010. Ge‐

[144] Schmelzer E. 2002. Cell polarization, a crucial process in fungal defence. Trends Plant

[145] Schneider SM, Rosskopf EN, Leesch JG, Chellemi DO, Bull CT, Mazzola M. 2003. United States Department of Agriculture-Agricultural Research Service research on alternatives to methyl bromide: pre-plant and post-harvest. Pest Manag Sci. 59:

[146] Shannon JG, Arelli PR, Young LD. 2004. Breeding for resistance and tolerance. Pp. 155-180. *in* D. P. Schmitt, J. A. Wrather, and R. D. Riggs, eds. Biology and manage‐ ment of soybean cyst nematode, 2nd ed. Marceline, MO: Schmitt & Associates of

[147] Smant GA, Stokkermans JPWG, Yan Y, De Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J. 1998. Endogenous cellulases in animals: isolation of 1,4-endoglucanase genes from two species of plant-

[148] Sönnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, Brehm M, Alleaume AM, Artelt J, Bettencourt P, Cassin E, Hewitson M, Holz C, Khan M, Lazik S, Martin

parasitic nematodes. PNAS USA 95: 4906-4911

nome sequence of the palaeopolyploid soybean. Nature 463: 178-183

[139] Brim CA, Ross JP. 1966. Registration of Pickett soybeans. Crop Science 6: 305

in combination with nematicide . J. Nematology 23: 344-347

soybean roots. Phytopathology 48: 578-579

soybean yields. Phytopathology 52: 815-818

ylBromideAlternatives.pdf

10555–10561

170 Soybean - Pest Resistance

Sci 7: 411-415

814-826

Marceline


gland cells of the soybean cyst nematode Heterodera glycines. Molecular Plant-Mi‐ crobe Interactions 14: 536-544

**Chapter 7**

**Screening of Soybean**

**(***Glycine Max* **(L.) Merrill)**

M. H. Khan, S. D. Tyagi and Z. A. Dar

http://dx.doi.org/10.5772/54697

**1. Introduction**

sives and lubricants etc.

production to a greater extent.

**Genotypes for Resistance to Rust,**

**Yellow Mosaic and Pod Shattering**

Additional information is available at the end of the chapter

Soybean (Glycine max (L.) Merrill) is known as 'Golden bean' and miracle crop of 20th century. Soybean is a native of North China, Asia belongs to family fabaceae. It is a versa‐ tile and fascinating crop with innumerable possibilities of not only improving agriculture but also supporting industries. Soybean besides having high yielding potential (40-45 q/ha) also provides cholesterol free oil (20%) and high quality protein (40%). It is a rich source of lysine (6.4%) in addition to other essential amino acids, vitamins and minerals. Its oil is also used as a raw material in manufacturing antibiotics, paints, varnishes, adhe‐

Like other economically important crops soybean is also suffering from many diseases viz, rust (*Phakopsora pachyrhizi* Syd.) and yellow mosaic (Mungbean Yellow Mosaic Virus) are the major disease under Indian conditions, which causes considerable reduction in yield up to 80 per cent under severe conditions [3]. Further, another major problem in soybean is pods shattering which also reduces yield and in some varieties 100 per cent yield losses have been observed. The extent of yield loss due to pod shattering may range from negligible to signifi‐ cance levels depending upon the time of harvesting, environmental condition and genetic endowment of the variety [11]. Hence screening for soybean genotypes for identifying resistance to above major problems with high yielding potential will help to increase the

> © 2013 Khan et al.; licensee InTech. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,

© 2013 Khan et al.; licensee InTech. This is a paper distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

distribution, and reproduction in any medium, provided the original work is properly cited.


**Chapter 7**

**Screening of Soybean (***Glycine Max* **(L.) Merrill) Genotypes for Resistance to Rust, Yellow Mosaic and Pod Shattering**

M. H. Khan, S. D. Tyagi and Z. A. Dar

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/54697
