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A gene expression analysis of syncytia laser microdissected from the roots of the Glycine max (soybean) genotype PI 548402 (Peking) undergoing a resistant reaction after infection by Heterodera glycines (soybean cyst nematode)

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Abstract

The syncytium is a nurse cell formed within the roots of Glycine max by the plant parasitic nematode Heterodera glycines. Its development and maintenance are essential for nematode survival. The syncytium appears to undergo two developmental phases during its maturation into a functional nurse cell. The first phase is a parasitism phase where the nematode establishes the molecular circuitry that during the second phase ensures a compatible interaction with the plant cell. The cytological features of syncytia undergoing susceptible or resistant reactions appear the same during the parasitism phase. Depending on the outcome of any defense response, the second phase is a period of syncytium maintenance (susceptible reaction) or failure (resistant reaction). In the analyses presented here, the localized gene expression occurring at the syncytium during the resistant reaction was studied. This was accomplished by isolating syncytial cells from Glycine max genotype Peking (PI 548402) by laser capture microdissection. Microarray analyses using the Affymetrix® soybean GeneChip® directly compared Peking syncytia undergoing a resistant reaction to those undergoing a susceptible reaction during the parasitism phase of the resistant reaction. Those analyses revealed lipoxygenase-9 and lipoxygenase-4 as the most highly induced genes in the resistant reaction. The analysis also identified induced levels of components of the phenylpropanoid pathway. These genes included phenylalanine ammonia lyase, chalcone isomerase, isoflavone reductase, cinnamoyl-CoA reductase and caffeic acid O-methyltransferase. The presence of induced levels of these genes implies the importance of jasmonic acid and phenylpropanoid signaling pathways locally at the site of the syncytium during the resistance phase of the resistant reaction. The analysis also identified highly induced levels of four S-adenosylmethionine synthetase genes, the EARLY-RESPONSIVE TO DEHYDRATION 2 gene and the 14-3-3 gene known as GENERAL REGULATORY FACTOR 2. Subsequent analyses studied microdissected syncytial cells at 3, 6 and 9 days post infection (dpi) during the course of the resistant reaction, resulting in the identification of signature gene expression profiles at each time point in a single G. max genotype, Peking.

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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

PAL:

Phenylalanine ammonia lyase

CCR:

Cinnamoyl-CoA reductase

COMT:

Caffeic acid O-methyltransferase

ACC oxidase:

1-Aminocyclopropane-1-carboxylate oxidase

SAM:

S-Adenosylmethionine synthetase

FSi :

Feeding site initial

QTL:

Quantitative trait loci mapping

PI:

Plant introduction

hpi:

Hours post-infection

dpi:

Days post-infection

pi-J2:

Pre-infective second stage juvenile

GO:

Gene ontology

LOX:

Lipoxygenase

AOS:

Allene oxide synthase

AOC:

Allene oxide cyclase

JA:

Jasmonic acid

TPIs:

Trypsin proteinase inhibitors

eto:

Ethylene overproducer

ein:

Ethylene insensitive

DET3:

DE-ETIOLATED 3

NPR1:

Nonexpressor of PR genes

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Acknowledgments

The authors thank the United Soybean Board for their continued support provided by grant 5214. The authors thank Dr. David Munroe, Nina Bubunenko and Nicole Lum at the Laboratory of Molecular Technology, SAIC-Frederick, National Cancer Institute at Frederick, Frederick, MD 21701, USA for the Affymetrix® soybean GeneChip® array hybridizations and data acquisition. Dr. Gary Lawrence, Department of Entomology and Plant Pathology, Mississippi State University provided helpful insight into the analysis. The authors thank Veronica Martins at the United States Department of Agriculture, Systematic Mycology and Microbiology Laboratory, Beltsville, MD, 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. Department of Biological Sciences, Mississippi State University, Harned Hall, Mississippi State, MS, 39762, USA

    Vincent P. Klink & Prachi Matsye

  2. United States Department of Agriculture, Soybean Genomics and Improvement Laboratory, Bldg. 006, Beltsville, MD, 20705, USA

    Vincent P. Klink, Parsa Hosseini & Benjamin F. Matthews

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

    Parsa Hosseini & Nadim W. Alkharouf

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Klink, V.P., Hosseini, P., Matsye, P. et al. A gene expression analysis of syncytia laser microdissected from the roots of the Glycine max (soybean) genotype PI 548402 (Peking) undergoing a resistant reaction after infection by Heterodera glycines (soybean cyst nematode). Plant Mol Biol 71, 525–567 (2009). https://doi.org/10.1007/s11103-009-9539-1

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