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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)

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Abstract

Syncytial cells in soybean (Glycine max cultivar [cv.] Peking) roots infected by incompatible and compatible populations of soybean cyst nematode (SCN [Heterodera glycines]) were collected using laser capture microdissection (LCM). Gene transcript abundance was assayed using Affymetrix® soybean GeneChips®, each containing 37,744 probe sets. Our analyses identified differentially expressed genes in syncytial cells that are not differentially expressed in the whole root analyses. Therefore, our results show that the mass of transcriptional activity occurring in the whole root is obscuring identification of transcriptional events occurring within syncytial cells. In syncytial cells from incompatible roots at three dpi, genes encoding lipoxygenase (LOX), heat shock protein (HSP) 70, superoxidase dismutase (SOD) were elevated almost tenfold or more, while genes encoding several transcription factors and DNA binding proteins were also elevated, albeit at lower levels. In syncytial cells formed during the compatible interaction at three dpi, genes encoding prohibitin, the epsilon chain of ATP synthase, allene oxide cyclase and annexin were more abundant. By 8 days, several genes of unknown function and genes encoding a germin-like protein, peroxidase, LOX, GAPDH, 3-deoxy-D-arabino-heptolosonate 7-phosphate synthase, ATP synthase and a thioesterase were abundantly expressed. These observations suggest that gene expression is different in syncytial cells as compared to whole roots infected with nematodes. Our observations also show that gene expression is different between syncytial cells that were isolated from incompatible and compatible roots and that gene expression is changing over the course of syncytial cell development as it matures into a functional feeding site.

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Abbreviations

EST:

Expressed sequence tag

hpi:

Hours post inoculation

dpi:

Days post inoculation

SCN:

Soybean cyst nematode

J2:

Second stage juvenile

FS:

Farmer’s solution

PFA:

Paraformaldehyde

DEPC:

Diethylpyrocarbonate

LCM:

Laser capture microdissection

MRS:

Moisture replacement system

ROS:

Reactive oxygen species

LCM:

Laser capture microdissection

LRR:

Leucine rich repeat

BP:

Base pair

CaMKII:

Calmodulin kinase II

Avr:

Avirulence

References

  • Ahn CS, Lee JH, Reum Hwang A, Kim WT, Pai HS (2006) Prohibitin is involved in mitochondrial biogenesis in plants. Plant J 46:658–67

    Article  PubMed  CAS  Google Scholar 

  • Alkharouf N, Matthews BF (2004) SGMD: The soybean genomics and microarray database. Nucleic Acids Res 32:D398–D400

    Article  PubMed  CAS  Google Scholar 

  • Alkharouf NW, Klink VP, Chouikha IB, Beard HS, MacDonald MH, Meyer S, Knap HT, Khan R, Matthews BF (2006) Timecourse microarray analyses reveals global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224:838–52

    Article  PubMed  CAS  Google Scholar 

  • de Almeida Engler J, Van Poucke K, Karimi M, De Groodt R, Gheysen G, Engler G, Gheysen G (2004) Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J 38:12–26

    Article  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Asano T, Masumura T, Kusano H, Kikuchi S, Kurita A, Shimada H, Kadowaki K (2002) Construction of a specialized cDNA library from plant cells isolated by laser capture microdissection: toward comprehensive analysis of the genes expressed in the rice phloem. Plant J 32:401–408

    Article  PubMed  CAS  Google Scholar 

  • Bird D McK, Wilson MA (1994) DNA sequence and expression analysis of root-knot nematode-elicited giant cell transcripts. MPMI 7:419–424

    Google Scholar 

  • Bouche N, Yellin A, Snedden WA, Fromm H (2005) Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–66

    Article  PubMed  CAS  Google Scholar 

  • Byrd DW Jr, Kirkpatrick T, Barker KR (1983) An improved technique for clearing and staining plant tissue for detection of nematodes. J Nematol 15:142–143

    Google Scholar 

  • Cai D, Kleine M, Kifle S, Harloff HJ, Sandal NN, Marcker KA, Klein-Lankhorst RM, Salentijn EM, Lange W, Stiekema WJ, Wyss U, Grundler FM, Jung C (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832–4

    Article  PubMed  CAS  Google Scholar 

  • Carlsson L, Nyström LE, Sundkvist I, Markey F, Lindberg U (1977) Actin polymerizability is influenced by profilin, a low molecular weight protein in non-muscle cells. J Mol Biol 115:465–483

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–33

    Article  PubMed  CAS  Google Scholar 

  • De Koninck P, Schulman H (1998) Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279:227–30

    Article  PubMed  Google Scholar 

  • Dutilleul C, Garmier M, Noctor G, Mathieu C, Chetrit P, Foyer CH, de Paepe R (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1212–26

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Endo BY (1964) Penetration and development of Heterodera glycines in soybean roots and related and related anatomical changes. Phytopathology 54:79–88

    Google Scholar 

  • Endo BY (1965) Histological responses of resistant and susceptible soybean varieties, and backcross progeny to entry development of Heterodera glycines. Phytopathology 55:375–381

    CAS  Google Scholar 

  • Endo BY (1971) Synthesis of nucleic acids at infection sites of soybean roots parasitized by Heterodera glycines. Phytopathology 61:395–399

    CAS  Google Scholar 

  • Endo BY (1991) Ultrastructure of initial responses of resistant and susceptible soybean roots to infection by Heterodera glycines. Rev Nematol 14:73–94

    Google Scholar 

  • Endo BY (1998) Atlas on Ultrastructure of Infective Juveniles of the Soybean Cyst Nematode Heterodera glycines. Agricultural Handbook Number 711, 224 pp

  • Endo BY, Veech JA (1970) Morphology and histochemistry of soybean roots infected with Heterodera glycines. Phytopathology 60:1493–1498

    Article  CAS  Google Scholar 

  • Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW (2002) The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31:127–36

    Article  PubMed  CAS  Google Scholar 

  • Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Li FLC, Maeschler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JYH, Zhang J (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5:R80

    Article  PubMed  Google Scholar 

  • Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu Rev Phytopathol 40:191–219

    Article  PubMed  CAS  Google Scholar 

  • Gipson I, Kim KS, Riggs RD (1971) An ultrastructural study of syncytium development in soybean roots infected with Heterodera glycines. Phytopathol 61:347–353

    Google Scholar 

  • Gutierres S, Sabar M, Lelandais C, Chetrit P, Diolez P, Degand H, Boutry M, Vedel F, de Kouchkovsky Y, De Paepe R (1997) Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc Natl Acad Sci USA 4:3436–41

    Article  Google Scholar 

  • Hammond-Kosack KE, Jones JD (1997) PLANT DISEASE RESISTANCE GENES. Annu Rev Plant Physiol Plant Mol Biol 48:575–607

    Article  PubMed  CAS  Google Scholar 

  • Hwang CF, Williamson VM (2003) Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi. Plant J 34:585–93

    Article  PubMed  CAS  Google Scholar 

  • Hwang CF, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM (2000) Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12:1319–29

    Article  PubMed  CAS  Google Scholar 

  • Irizarry R, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003a) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15

    Article  PubMed  CAS  Google Scholar 

  • Irizarry R, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003b) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–64

    Article  PubMed  Google Scholar 

  • Isenberg G, Bielser W, Meier-Ruge W, Remy E (1976) Cell surgery by laser micro-dissection: a preparative method. J Microsc 107:19–24

    PubMed  CAS  Google Scholar 

  • Ithal N, Recknor J, Nettleston D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant-Microbe Interact 20:293–305

    Article  PubMed  CAS  Google Scholar 

  • Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin-Magniette ML, Renou JP, Abad P, Favery B (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 44:447–58

    Article  PubMed  CAS  Google Scholar 

  • Jones A (2000) Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?. Trends Plant Sci 5:225–30

    Article  PubMed  CAS  Google Scholar 

  • Jones MGK, Northcote DH (1972) Nematode-induced syncytium-a multinucleate transfer cell. J Cell Sci 10:789–809

    PubMed  CAS  Google Scholar 

  • Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JD (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–93

    Article  PubMed  CAS  Google Scholar 

  • Karpova OV, Kuzmin EV, Elthon TE, Newton KJ (2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell. 14:3271–84

    Article  PubMed  CAS  Google Scholar 

  • Khan R, Alkharouf N, Beard HS, MacDonald M, Chouikha I, Meyer S, Grefenstette J, Knap H, Matthews BF (2004) Resistance mechanisms in soybean: Gene expression profile at an early stage of soybean cyst nematode invasion. J Nematol 36:241–248

    CAS  PubMed  Google Scholar 

  • Kim YH, Riggs RD, Kim KS (1987) Structural changes associated with resistance of soybean to Heterodera glycines. J Nematol 19:177–187

    CAS  PubMed  Google Scholar 

  • Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–50

    Article  PubMed  CAS  Google Scholar 

  • Klink VP, MacDonald M, Alkharouf N, Matthews BF (2005) Laser capture microdissection (LCM) and expression analyses of Glycine max (soybean) syncytium containing root regions formed by the plant pathogen Heterodera glycines (soybean cyst nematode). Plant Mol Biol 59:969–983

    Article  CAS  Google Scholar 

  • Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthew BF (2007) A time-course comparative microarray analysis of an incompatible and compatible response by Glycine max (soybean) to soybean cyst nematode (Heterodera glycines) infection (submitted)

  • Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle FA (2004) Putative Ca2+ and calmodulin dependent protein kinase required for bacterial and fungal symbioses. Science. 303:1361–4

    Article  PubMed  CAS  Google Scholar 

  • Lipshutz RJ, Fodor SP, Gingeras TR, Lockhart DJ (1999) High density synthetic oligonucleotide arrays. Nat Genet (1 Suppl):20–24

  • Liu X, Bai X, Wang X, Chu C (2006) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol (in press)

  • Mathur J, Hülskamp M (2002) Microtubules and microfilaments in cell morphogenesis in higher plants. Curr Biol 12: R696–R676

    Article  Google Scholar 

  • Matthews B, MacDonald MH, Thai VK Tucker ML (2003) Molecular characterization of argenine kinase in the soybean cyst nematode (Heterodera glycines). J Nematol 35:252–258

    CAS  PubMed  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–19

    Article  PubMed  CAS  Google Scholar 

  • Mitra D, Johri MM (2000) Enhanced expression of a calcium-dependent protein kinase from the moss Funaria hygrometrica under nutritional starvation. J Biosci 25:331–8

    PubMed  CAS  Google Scholar 

  • Mujer CV, Andrews DL, Manhart JR, Pierce SK, Rumpho ME (1996) Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proc Natl Acad Sci USA 93:12333–12338

    Article  PubMed  CAS  Google Scholar 

  • 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 Heterodera glycines. J Nematol 34:279–288

    CAS  PubMed  Google Scholar 

  • Pla M, Mathieu C, De Paepe R, Chetrit P, Vedel F (1995) Deletion of the last two exons of the mitochondrial nad7 gene results in lack of the NAD7 polypeptide in a Nicotiana sylvestris CMS mutant. Mol Gen Genet. 248:79–88

    Article  PubMed  CAS  Google Scholar 

  • Puthoff DP, Nettleton D, Rodermel SR, Baum TJ (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. The Plant Journal 33:911–921

    Article  PubMed  CAS  Google Scholar 

  • Ravagnan L, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, Mak T, Jaattela M, Penninger JM, Garrido C, Kroemer G (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 3:839–43

    Article  PubMed  CAS  Google Scholar 

  • Riggs RD, Kim KS, Gipson I (1973) Ultrastructural changes in Peking soybeans infected with Heterodera glycines. Phytopathology 63:76–84

    Article  Google Scholar 

  • Riggs RD, Schmitt DP (1991) Optimization of the Heterodera glycines race test procedure. J Nematol 23:149–154

    CAS  PubMed  Google Scholar 

  • Rubio MC, James EK, Clemente MR, Bucciarelli B, Fedorova M, Vance CP, Becana M (2004) Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Mol Plant Microbe Interact 17:1294–305

    Article  PubMed  CAS  Google Scholar 

  • Ryu HS, Han M, Lee SK, Cho JI, Ryoo N, Heu S, Lee YH, Bhoo SH, Wang GL, Hahn TR, Jeon JS (2006) A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25:836–47

    Article  PubMed  CAS  Google Scholar 

  • Saleh A, Srinivasula SM, Balkir L, Robbins PD, Alnemri ES (2000) Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat Cell Biol 2:476–83

    Article  PubMed  CAS  Google Scholar 

  • Sardanelli S, Kenworthy WJ (1997) Soil Moisture Control and Direct Seeding for Bioassay of Heterodera glycines on Soybean. J Nematol (Suppl) 29:625–634

    CAS  Google Scholar 

  • Sass JE (1958) Botanical Microtechnique. Iowa State College Press, Ames

    Google Scholar 

  • Scandalios JG (1993) Oxygen Stress and Superoxide Dismutases. Plant Physiol 101:7–12

    PubMed  CAS  Google Scholar 

  • Schutz I, Gus-Mayer S, Schmelzer E (2006) Profilin and Rop GTPases are localized at infection sites of plant cells. Protoplasma 227:229–35

    Article  PubMed  CAS  Google Scholar 

  • Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315:1098–103

    Article  PubMed  CAS  Google Scholar 

  • Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 3:Article3

  • Sugimoto K, Williamson RE, Wasteneys GO (2000) New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol 124:1493–1506

    Article  PubMed  CAS  Google Scholar 

  • Sun H-Q, Kwiatkowska K, Yin H (1995) Actin monomer binding proteins. Curr Opin Cell Biol 7:102–110

    Article  PubMed  CAS  Google Scholar 

  • Sung DY, Guy CL (2003) Physiological and molecular assessment of altered expression of Hsc70–1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiol 132:979–87

    Article  PubMed  CAS  Google Scholar 

  • 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 incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–30

    Article  PubMed  CAS  Google Scholar 

  • The gene ontology consortium (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261

    Article  CAS  Google Scholar 

  • Ulker B, Shahid Mukhtar M, Somssich IE (2007) The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta 226:125–37

    Article  PubMed  CAS  Google Scholar 

  • van der Vossen EA, van der Voort JN, Kanyuka K, Bendahmane A, Sandbrink H, Baulcombe DC, Bakker J, Stiekema WJ, Klein-Lankhorst RM (2000) Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J 23:567–76

    Article  PubMed  Google Scholar 

  • Volkmann D, Baluska F (1999) Actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 47:135–154

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2:e123

    Article  PubMed  CAS  Google Scholar 

  • Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends Genet 22:396–403

    Article  PubMed  CAS  Google Scholar 

  • Wilson MA, Bird D McK van der Knaap E (1994) A comprehensive subtractive cDNA cloning approach to identify nematode-induced transcripts in tomato. Phytopathology 84:299–303

    Article  CAS  Google Scholar 

  • Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003–2005. J Nematol 38:173–180

    PubMed  Google Scholar 

  • Yamamoto E, Knap HT (2001) Soybean receptor-like protein kinase genes: paralogous divergence of a gene family. Mol Biol Evol 18:1522–31

    PubMed  CAS  Google Scholar 

  • Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors greatly appreciate the continued support provided by the United Soybean Board under grant 5214. The authors thank Dr. David Munroe and Nicole Lum at the Laboratory of Molecular Technology, SAIC-Frederick, National Cancer Institute at Frederick, Frederick, Maryland 21701, USA for the Affymetrix® array hybridizations and data acquisition. All data, raw and normalized, are stored in the Soybean Genomics and Microarray Database (Alkharouf and Matthews 2004), available through the web site [http://www.towson.edu/nalkharo/SGMD/SupplementalSites/AffyGmLCM]. The authors are indebted to Dr. Leslie Wanner, United States Department of Agriculture for the careful reading and critical comments of the manuscript. The authors thank Veronica Martins for careful editing of the manuscript. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the United States Department of Agriculture.

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  1. United States Department of Agriculture, Soybean Genomics and Improvement Laboratory, Bldg. 006, Rm. 118, 10300 Baltimore Ave., Beltsville, MD, 20705-2350, USA

    Vincent P. Klink, Christopher C. Overall, Margaret H. MacDonald & Benjamin F. Matthews

  2. Department of Bioinformatics and Computational Biology, George Mason University, Manassas, VA , 20110, USA

    Christopher C. Overall

  3. Jess and Mildred Fisher College of Science and Mathematics, Department of Computer and Information Sciences, Towson University, 7800 York Road, Towson, MD, 21252, USA

    Nadim W. Alkharouf

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  1. Vincent P. Klink
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  2. Christopher C. Overall
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  3. Nadim W. Alkharouf
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  4. Margaret H. MacDonald
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Correspondence to Vincent P. Klink.

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Vincent P. Klink and Christopher C. Overall contributed equally to this work.

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Klink, V.P., Overall, C.C., Alkharouf, N.W. et al. Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean (Glycine max) roots infected by the soybean cyst nematode (Heterodera glycines). Planta 226, 1389–1409 (2007). https://doi.org/10.1007/s00425-007-0578-z

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