DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization

Abstract

Soybean aphids (Aphis glycines Matsumura) are specialized insects that feed on soybean (Glycine max) phloem sap. Transcriptome analyses have shown that resistant soybean plants mount a fast response that limits aphid feeding and population growth. Conversely, defense responses in susceptible plants are slower and it is hypothesized that aphids block effective defenses in the compatible interaction. Unlike other pests, aphids can colonize plants for long periods of time; yet the effect on the plant transcriptome after long-term aphid feeding has not been analyzed for any plant– aphid interaction. We analyzed the susceptible and resistant (Rag1) transcriptome response to aphid feeding in soybean plants colonized by aphids (biotype 1) for 21 days. We found a reduced resistant response and a low level of aphid growth on Rag1 plants, while susceptible plants showed a strong response consistent with pattern-triggered immunity. GO-term analyses identified chitin regulation as one of the most overrepresented classes of genes, suggesting that chitin could be one of the hemipteran-associated molecular pattern that triggers this defense response. Transcriptome analyses also indicated the phenylpropanoid pathway, specifically isoflavonoid biosynthesis, was induced in susceptible plants in response to long-term aphid feeding. Metabolite analyses corroborated this finding. Aphid-treated susceptible plants accumulated daidzein, formononetin,more » and genistein, although glyceollins were present at low levels in these plants. Choice experiments indicated that daidzein may have a deterrent effect on aphid feeding. Mass spectrometry imaging showed these isoflavones accumulate likely in the mesophyll cells or epidermis and are absent from the vasculature, suggesting that isoflavones are part of a non-phloem defense response that can reduce aphid feeding. While it is likely that aphid can initially block defense responses in compatible interactions, it appears that susceptible soybean plants can eventually mount an effective defense in response to long-term soybean aphid colonization.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [3];  [6]
  1. Iowa State Univ., Ames, IA (United States). Genetics and Genomics Graduate Program
  2. Iowa State Univ., Ames, IA (United States). Bioinformatics and Computational Biology Graduate Program
  3. Ames Lab., Ames, IA (United States)
  4. West Virginia Univ., Morgantown, WV (United States). Natural Resources and Design. Davis College of Agriculture. Division of Plant and Soil Sciences
  5. Iowa State Univ., Ames, IA (United States). Roy J. Carver dpt. of Biochemistry, Biophysics, and Molecular Biology
  6. Iowa State Univ., Ames, IA (United States). Genetics and Genomics Graduate Program; Iowa State Univ., Ames, IA (United States). Bioinformatics and Computational Biology Graduate Program; Iowa State Univ., Ames, IA (United States). Roy J. Carver dpt. of Biochemistry, Biophysics, and Molecular Biology
Publication Date:
Research Org.:
Ames Laboratory (AMES), Ames, IA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1628292
Grant/Contract Number:  
AC02-07CH11358
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 10; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Plant Sciences; plant–insect interaction; soybean defense; isoflavones; feeding deterrence; Aphis glycines

Citation Formats

Hohenstein, Jessica D., Studham, Matthew E., Klein, Adam, Kovinich, Nik, Barry, Kia, Lee, Young-Jin, and MacIntosh, Gustavo C. Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization. United States: N. p., 2019. Web. doi:10.3389/fpls.2019.00310.
Hohenstein, Jessica D., Studham, Matthew E., Klein, Adam, Kovinich, Nik, Barry, Kia, Lee, Young-Jin, & MacIntosh, Gustavo C. Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization. United States. https://doi.org/10.3389/fpls.2019.00310
Hohenstein, Jessica D., Studham, Matthew E., Klein, Adam, Kovinich, Nik, Barry, Kia, Lee, Young-Jin, and MacIntosh, Gustavo C. Wed . "Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization". United States. https://doi.org/10.3389/fpls.2019.00310. https://www.osti.gov/servlets/purl/1628292.
@article{osti_1628292,
title = {Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization},
author = {Hohenstein, Jessica D. and Studham, Matthew E. and Klein, Adam and Kovinich, Nik and Barry, Kia and Lee, Young-Jin and MacIntosh, Gustavo C.},
abstractNote = {Soybean aphids (Aphis glycines Matsumura) are specialized insects that feed on soybean (Glycine max) phloem sap. Transcriptome analyses have shown that resistant soybean plants mount a fast response that limits aphid feeding and population growth. Conversely, defense responses in susceptible plants are slower and it is hypothesized that aphids block effective defenses in the compatible interaction. Unlike other pests, aphids can colonize plants for long periods of time; yet the effect on the plant transcriptome after long-term aphid feeding has not been analyzed for any plant– aphid interaction. We analyzed the susceptible and resistant (Rag1) transcriptome response to aphid feeding in soybean plants colonized by aphids (biotype 1) for 21 days. We found a reduced resistant response and a low level of aphid growth on Rag1 plants, while susceptible plants showed a strong response consistent with pattern-triggered immunity. GO-term analyses identified chitin regulation as one of the most overrepresented classes of genes, suggesting that chitin could be one of the hemipteran-associated molecular pattern that triggers this defense response. Transcriptome analyses also indicated the phenylpropanoid pathway, specifically isoflavonoid biosynthesis, was induced in susceptible plants in response to long-term aphid feeding. Metabolite analyses corroborated this finding. Aphid-treated susceptible plants accumulated daidzein, formononetin, and genistein, although glyceollins were present at low levels in these plants. Choice experiments indicated that daidzein may have a deterrent effect on aphid feeding. Mass spectrometry imaging showed these isoflavones accumulate likely in the mesophyll cells or epidermis and are absent from the vasculature, suggesting that isoflavones are part of a non-phloem defense response that can reduce aphid feeding. While it is likely that aphid can initially block defense responses in compatible interactions, it appears that susceptible soybean plants can eventually mount an effective defense in response to long-term soybean aphid colonization.},
doi = {10.3389/fpls.2019.00310},
journal = {Frontiers in Plant Science},
number = ,
volume = 10,
place = {United States},
year = {Wed Mar 13 00:00:00 EDT 2019},
month = {Wed Mar 13 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

FIGURE 1 FIGURE 1: Aphid population levels after 20 days of infestation. Susceptible (SD01-76R) and aphid-resistant (LD16060) soybean plants were infested with 30 aphids and aphid populations were quantified after 20 days. The difference in aphid number between resistant and susceptible plants was statistically significant (p ≤ 0.05; two-tailed Student’s $t$-test). Errormore » bars represent standard error of the mean (n = 18).« less

Save / Share:

Works referenced in this record:

Investigation of the Chemical Interface in the Soybean–Aphid and Rice–Bacteria Interactions Using MALDI-Mass Spectrometry Imaging
journal, May 2015


The transcriptional network of WRKY53 in cereals links oxidative responses to biotic and abiotic stress inputs
journal, April 2014

  • Van Eck, Leon; Davidson, Rebecca M.; Wu, Shuchi
  • Functional & Integrative Genomics, Vol. 14, Issue 2
  • DOI: 10.1007/s10142-014-0374-3

BLAST: at the core of a powerful and diverse set of sequence analysis tools
journal, July 2004

  • McGinnis, S.; Madden, T. L.
  • Nucleic Acids Research, Vol. 32, Issue Web Server
  • DOI: 10.1093/nar/gkh435

SoyBase, the USDA-ARS soybean genetics and genomics database
journal, December 2009

  • Grant, David; Nelson, Rex T.; Cannon, Steven B.
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp798

Fine mapping the soybean aphid resistance gene Rag1 in soybean
journal, December 2009

  • Kim, Ki-Seung; Bellendir, Stephanie; Hudson, Karen A.
  • Theoretical and Applied Genetics, Vol. 120, Issue 5
  • DOI: 10.1007/s00122-009-1234-8

A Model-Based Background Adjustment for Oligonucleotide Expression Arrays
journal, December 2004

  • Wu, Zhijin; Irizarry, Rafael A.; Gentleman, Robert
  • Journal of the American Statistical Association, Vol. 99, Issue 468
  • DOI: 10.1198/016214504000000683

Plant Immunity to Insect Herbivores
journal, June 2008


P HYTOALEXINS : What Have We Learned After 60 Years?
journal, September 1999


Fine mapping of the soybean aphid-resistance genes Rag6 and Rag3c from Glycine soja 85-32
journal, September 2017

  • Zhang, Shichen; Zhang, Zhongnan; Wen, Zixiang
  • Theoretical and Applied Genetics, Vol. 130, Issue 12
  • DOI: 10.1007/s00122-017-2979-0

Soybean defense responses to the soybean aphid
journal, July 2008


First Report of Transmission of Soybean mosaic virus and Alfalfa mosaic virus by Aphis glycines in the New World
journal, May 2001


RNA-Seq reveals a xenobiotic stress response in the soybean aphid, Aphis glycines, when fed aphid-resistant soybean
journal, January 2014


New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants
journal, May 2009

  • Briat, Jean-Francois; Ravet, Karl; Arnaud, Nicolas
  • Annals of Botany, Vol. 105, Issue 5
  • DOI: 10.1093/aob/mcp128

Hormone Crosstalk in Plant Disease and Defense: More Than Just JASMONATE-SALICYLATE Antagonism
journal, September 2011


Transcriptome analyses and virus induced gene silencing identify genes in the Rpp4-mediated Asian soybean rust resistance pathway
journal, January 2013

  • Morales, Aguida M. A. P.; O'Rourke, Jamie A.; van de Mortel, Martijn
  • Functional Plant Biology, Vol. 40, Issue 10
  • DOI: 10.1071/FP12296

Gene Expression Omnibus: NCBI gene expression and hybridization array data repository
journal, January 2002


Genome sequence of the palaeopolyploid soybean
journal, January 2010

  • Schmutz, Jeremy; Cannon, Steven B.; Schlueter, Jessica
  • Nature, Vol. 463, Issue 7278
  • DOI: 10.1038/nature08670

Flavonoids and Isoflavonoids: From Plant Biology to Agriculture and Neuroscience
journal, October 2010


Differential innate immune signalling via Ca2+ sensor protein kinases
journal, February 2010

  • Boudsocq, Marie; Willmann, Matthew R.; McCormack, Matthew
  • Nature, Vol. 464, Issue 7287
  • DOI: 10.1038/nature08794

A new mathematical model for relative quantification in real-time RT-PCR
journal, May 2001


Recognition of Herbivory-Associated Molecular Patterns
journal, March 2008


Structural Features of the Endogenous CHS Silencing and Target Loci in the Soybean Genome
journal, March 2008


Biology of the Soybean Aphid, Aphis glycines (Hemiptera: Aphididae) in the United States
journal, October 2011

  • Tilmon, K. J.; Hodgson, E. W.; O'Neal, M. E.
  • Journal of Integrated Pest Management, Vol. 2, Issue 2
  • DOI: 10.1603/ipm10016

An Isoflavone Conjugate-hydrolyzing β-Glucosidase from the Roots of Soybean ( Glycine max ) Seedlings: PURIFICATION, GENE CLONING, PHYLOGENETICS, AND CELLULAR LOCALIZATION
journal, August 2006

  • Suzuki, Hirokazu; Takahashi, Seiji; Watanabe, Ryoko
  • Journal of Biological Chemistry, Vol. 281, Issue 40
  • DOI: 10.1074/jbc.M605726200

Functional analysis of members of the isoflavone and isoflavanone O-methyltransferase enzyme families from the model legume Medicago truncatula
journal, September 2006

  • Deavours, Bettina E.; Liu, Chang-Jun; Naoumkina, Marina A.
  • Plant Molecular Biology, Vol. 62, Issue 4-5
  • DOI: 10.1007/s11103-006-9050-x

Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants
journal, January 2013

  • Nuruzzaman, Mohammed; Sharoni, Akhter M.; Kikuchi, Shoshi
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00248

Mining the plant-herbivore interface with a leafmining Drosophila of Arabidopsis: A MODEL HERBIVORE OF ARABIDOPSIS
journal, November 2010


Intraspecific variation in alkaloid profile of four lupine species with implications for the pea aphid probing behaviour
journal, March 2012


Flavonoids with mosquito larval toxicity
journal, June 1990

  • Rao, Koppaka V.; Chattopadhyay, Sunil K.; Reddy, G. Chandrasekhara
  • Journal of Agricultural and Food Chemistry, Vol. 38, Issue 6
  • DOI: 10.1021/jf00096a028

Exploration, normalization, and summaries of high density oligonucleotide array probe level data
journal, April 2003


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Antifeedant activity of luteolin and genistein against the pea aphid, Acyrthosiphon pisum
journal, June 2012


Recognizing Plant Defense Priming
journal, October 2016


On testing the significance of sets of genes
journal, June 2007

  • Efron, Bradley; Tibshirani, Robert
  • The Annals of Applied Statistics, Vol. 1, Issue 1
  • DOI: 10.1214/07-AOAS101

Salivary secretions by aphids interacting with proteins of phloem wound responses
journal, February 2006

  • Tjallingii, W. Fred
  • Journal of Experimental Botany, Vol. 57, Issue 4
  • DOI: 10.1093/jxb/erj088

Avoiding Effective Defenses: Strategies Employed by Phloem-Feeding Insects
journal, March 2008


Global Switches and Fine-Tuning—ABA Modulates Plant Pathogen Defense
journal, June 2008

  • Asselbergh, Bob; De Vleesschauwer, David; Höfte, Monica
  • Molecular Plant-Microbe Interactions®, Vol. 21, Issue 6
  • DOI: 10.1094/mpmi-21-6-0709

Plant–aphid interactions: molecular and ecological perspectives
journal, August 2007


Iron Deficiency Induced by Chrysobactin in Saintpaulia Leaves Inoculated with Erwinia chrysanthemi
journal, July 1993

  • Neema, C.; Laulhere, J. P.; Expert, D.
  • Plant Physiology, Vol. 102, Issue 3
  • DOI: 10.1104/pp.102.3.967

Plant immunity in plant–aphid interactions
journal, December 2014

  • Jaouannet, Maëlle; Rodriguez, Patricia A.; Thorpe, Peter
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00663

Signal Signature and Transcriptome Changes of Arabidopsis During Pathogen and Insect Attack
journal, September 2005

  • De Vos, Martin; Van Oosten, Vivian R.; Van Poecke, Remco M. P.
  • Molecular Plant-Microbe Interactions®, Vol. 18, Issue 9
  • DOI: 10.1094/mpmi-18-0923

MedicCyc: a biochemical pathway database for Medicago truncatula
journal, March 2007


Functional analysis of soybean genes involved in flavonoid biosynthesis by virus-induced gene silencing
journal, November 2007


The role of sinigrin in host plant recognition by aphids during initial plant penetration
journal, July 2002


Resistance to Aphis glycines (Hemiptera: Aphididae) in Various Soybean Lines Under Controlled Laboratory Conditions
journal, August 2007

  • Hesler, Louis S.; Dashiell, Kenton E.
  • Journal of Economic Entomology, Vol. 100, Issue 4
  • DOI: 10.1093/jee/100.4.1464

Mechanisms and evolution of plant resistance to aphids
journal, January 2016


Networking by small-molecule hormones in plant immunity
journal, April 2009

  • Pieterse, Corné M. J.; Leon-Reyes, Antonio; Van der Ent, Sjoerd
  • Nature Chemical Biology, Vol. 5, Issue 5
  • DOI: 10.1038/nchembio.164

QTL underlying the resistance to soybean aphid (Aphis glycines Matsumura) through isoflavone-mediated antibiosis in soybean cultivar ‘Zhongdou 27’
journal, August 2011


The molecular bases of plant resistance and defense responses to aphid feeding: current status
journal, January 2007


A Single Dominant Gene for Resistance to the Soybean Aphid in the Soybean Cultivar Dowling
journal, July 2006


Chemical basis of resistance in soya bean to cabbage looper,Trichoplusia ni
journal, January 1991

  • Sharma, H. C.; Norris, Dale M.
  • Journal of the Science of Food and Agriculture, Vol. 55, Issue 3
  • DOI: 10.1002/jsfa.2740550304

Constitutive and Induced Differential Accumulation of Amino Acid in Leaves of Susceptible and Resistant Soybean Plants in Response to the Soybean Aphid (Hemiptera: Aphididae)
journal, June 2010

  • Chiozza, Mariana V.; O'Neal, Matthew E.; MacIntosh, Gustavo C.
  • Environmental Entomology, Vol. 39, Issue 3
  • DOI: 10.1603/en09338

Effector proteins that modulate plant–insect interactions
journal, August 2011


Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae
journal, November 2006


Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach
journal, February 2004

  • Storey, John D.; Taylor, Jonathan E.; Siegmund, David
  • Journal of the Royal Statistical Society: Series B (Statistical Methodology), Vol. 66, Issue 1
  • DOI: 10.1111/j.1467-9868.2004.00439.x

Compatible plant-aphid interactions: How aphids manipulate plant responses
journal, June 2010

  • Giordanengo, Philippe; Brunissen, Laurence; Rusterucci, Christine
  • Comptes Rendus Biologies, Vol. 333, Issue 6-7
  • DOI: 10.1016/j.crvi.2010.03.007

The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases
journal, October 2009

  • Caspi, Ron; Altman, Tomer; Dale, Joseph M.
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp875

Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects
journal, February 2006

  • Thompson, Gary A.; Goggin, Fiona L.
  • Journal of Experimental Botany, Vol. 57, Issue 4
  • DOI: 10.1093/jxb/erj135

Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes
journal, February 2000

  • Jung, Woosuk; Yu, Oliver; Lau, Sze-Mei Cindy
  • Nature Biotechnology, Vol. 18, Issue 2
  • DOI: 10.1038/72671

Soybean Aphid Infestation Induces Changes in Fatty Acid Metabolism in Soybean
journal, December 2015


Arabidopsis immune secretory pathways to powdery mildew fungi
journal, August 2016


SG2-Type R2R3-MYB Transcription Factor MYB15 Controls Defense-Induced Lignification and Basal Immunity in Arabidopsis
journal, July 2017

  • Chezem, William R.; Memon, Altamash; Li, Fu-Shuang
  • The Plant Cell, Vol. 29, Issue 8
  • DOI: 10.1105/tpc.16.00954

Toward Understanding the Role of Aphid Effectors in Plant Infestation
journal, January 2013

  • Rodriguez, Patricia A.; Bos, Jorunn I. B.
  • Molecular Plant-Microbe Interactions®, Vol. 26, Issue 1
  • DOI: 10.1094/mpmi-05-12-0119-fi

Phosphorylation of a WRKY Transcription Factor by Two Pathogen-Responsive MAPKs Drives Phytoalexin Biosynthesis in Arabidopsis
journal, April 2011


Phytohormone signaling pathway analysis method for comparing hormone responses in plant-pest interactions
journal, July 2012


Performance and prospects of Rag genes for management of soybean aphid
journal, May 2013

  • Hesler, Louis S.; Chiozza, Mariana V.; O'Neal, Matthew E.
  • Entomologia Experimentalis et Applicata, Vol. 147, Issue 3
  • DOI: 10.1111/eea.12073

Identification of Soybean Proteins and Genes Differentially Regulated in Near Isogenic Lines Differing in Resistance to Aphid Infestation
journal, August 2015


Soybean Aphid Resistance in Soybean Jackson Is Controlled by a Single Dominant Gene
journal, July 2006


Are Chemical Compounds Important for Soybean Resistance to Anticarsia gemmatalis?
journal, July 2005

  • Piubelli, Giorla Carla; Hoffmann-Campo, Clara Beatriz; Moscardi, Flávio
  • Journal of Chemical Ecology, Vol. 31, Issue 7
  • DOI: 10.1007/s10886-005-5794-z

Effect of infestation by aphids on the water status of barley and insect development
journal, November 1995


Regiospecific methylation of naringenin to ponciretin by soybean O-methyltransferase expressed in Escherichia coli
journal, September 2005


Evaluation of Artificial Diets for Rearing Aphis glycines (Hemiptera: Aphididae)
journal, August 2008


A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity
journal, November 2010

  • Humphry, M.; Bednarek, P.; Kemmerling, B.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 50
  • DOI: 10.1073/pnas.1003619107

HOS3, an ELO-Like Gene, Inhibits Effects of ABA and Implicates a S-1-P/Ceramide Control System for Abiotic Stress Responses in Arabidopsis thaliana
journal, January 2009

  • Quist, Tanya M.; Sokolchik, Irina; Shi, Huazhong
  • Molecular Plant, Vol. 2, Issue 1
  • DOI: 10.1093/mp/ssn085

Discovery of Soybean Aphid Biotypes
journal, January 2008


Role of plant hormones in plant defence responses
journal, December 2008


Flavone synthase II (CYP93B16) from soybean (Glycine max L.)
journal, April 2010


MAP kinase signalling cascade in Arabidopsis innate immunity
journal, February 2002

  • Asai, Tsuneaki; Tena, Guillaume; Plotnikova, Joulia
  • Nature, Vol. 415, Issue 6875
  • DOI: 10.1038/415977a

Economic Threshold for Soybean Aphid (Hemiptera: Aphididae)
journal, August 2007

  • Ragsdale, D. W.; McCornack, B. P.; Venette, R. C.
  • Journal of Economic Entomology, Vol. 100, Issue 4
  • DOI: 10.1093/jee/100.4.1258

WRKY transcription factors: Jack of many trades in plants
journal, February 2014

  • Bakshi, Madhunita; Oelmüller, Ralf
  • Plant Signaling & Behavior, Vol. 9, Issue 2
  • DOI: 10.4161/psb.27700

Transcript Profiling of Wheat Genes Expressed During Feeding by Two Different Biotypes of Diuraphis noxia
journal, August 2010

  • Botha, Anna-Maria; Swanevelder, Zacharias H.; Lapitan, Nora L. V.
  • Environmental Entomology, Vol. 39, Issue 4
  • DOI: 10.1603/en09248

Abscisic acid deficiency increases defence responses against Myzus persicae in Arabidopsis: ABA deficiency and increased resistance to aphids
journal, June 2015

  • Hillwig, Melissa S.; Chiozza, Mariana; Casteel, Clare L.
  • Molecular Plant Pathology, Vol. 17, Issue 2
  • DOI: 10.1111/mpp.12274

Partial Reconstruction of Flavonoid and Isoflavonoid Biosynthesis in Yeast Using Soybean Type I and Type II Chalcone Isomerases
journal, March 2005

  • Ralston, Lyle; Subramanian, Senthil; Matsuno, Michiyo
  • Plant Physiology, Vol. 137, Issue 4
  • DOI: 10.1104/pp.104.054502

Signaling Mechanisms in Pattern-Triggered Immunity (PTI)
journal, April 2015


Insect-Induced Daidzein, Formononetin and Their Conjugates in Soybean Leaves
journal, July 2014

  • Murakami, Shinichiro; Nakata, Ryu; Aboshi, Takako
  • Metabolites, Vol. 4, Issue 3
  • DOI: 10.3390/metabo4030532

Transcriptional responses of tolerant and susceptible soybeans to soybean aphid (Aphis glycines Matsumura) herbivory
journal, March 2015

  • Prochaska, T. J.; Donze-Reiner, T.; Marchi-Werle, L.
  • Arthropod-Plant Interactions, Vol. 9, Issue 4
  • DOI: 10.1007/s11829-015-9371-2

Activation of members of a MAPK module in β-glucan elicitor-mediated non-host resistance of soybean
journal, November 2006


Differential expression of CHS7 and CHS8 genes in soybean
journal, December 2009


Secondary Metabolites from Glycine soja and Their Growth Inhibitory Effect against Spodoptera litura
journal, June 2011

  • Zhou, Yan-Ying; Luo, Shi-Hong; Yi, Ting-Shuang
  • Journal of Agricultural and Food Chemistry, Vol. 59, Issue 11
  • DOI: 10.1021/jf200821p

Structural Elucidation of Chalcone Reductase and Implications for Deoxychalcone Biosynthesis
journal, June 2005

  • Bomati, Erin K.; Austin, Michael B.; Bowman, Marianne E.
  • Journal of Biological Chemistry, Vol. 280, Issue 34
  • DOI: 10.1074/jbc.M502239200

Constitutive and Induced Activities of Defense-Related Enzymes in Aphid-Resistant and Aphid-Susceptible Cultivars of Wheat
journal, January 2009


Phytohormonal signaling in plant responses to aphid feeding
journal, April 2011

  • Morkunas, Iwona; Mai, Van Chung; Gabryś, Beata
  • Acta Physiologiae Plantarum, Vol. 33, Issue 6
  • DOI: 10.1007/s11738-011-0751-7

Ethylene-Responsive Element-Binding Factor 5, ERF5, Is Involved in Chitin-Induced Innate Immunity Response
journal, January 2012

  • Son, Geon Hui; Wan, Jinrong; Kim, Hye Jin
  • Molecular Plant-Microbe Interactions®, Vol. 25, Issue 1
  • DOI: 10.1094/mpmi-06-11-0165

Components of the SNARE-containing regulon are co-regulated in root cells undergoing defense
journal, February 2017


Inheritance of Soybean Aphid Resistance in PI 567541B and PI 567598B
journal, September 2008


SNARE-protein-mediated disease resistance at the plant cell wall
journal, October 2003

  • Collins, Nicholas C.; Thordal-Christensen, Hans; Lipka, Volker
  • Nature, Vol. 425, Issue 6961
  • DOI: 10.1038/nature02076

Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M
journal, November 2006


Resistance to Aphis glycines (Hemiptera: Aphididae) in Various Soybean Lines Under Controlled Laboratory Conditions
journal, August 2007


Evaluation of Artificial Diets for Rearing Aphis glycines (Hemiptera: Aphididae)
journal, August 2008


Mechanisms and evolution of plant resistance to aphids
text, January 2016


The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases
journal, November 2011

  • Caspi, R.; Altman, T.; Dreher, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1014

Soybean Aphid Resistance in Soybean Jackson Is Controlled by a Single Dominant Gene
journal, January 2007


Components of the SNARE-containing regulon are co-regulated in root cells undergoing defense
dataset, January 2016


Components of the SNARE-containing regulon are co-regulated in root cells undergoing defense
dataset, January 2016


QTL underlying the resistance to soybean aphid (Aphis glycines Matsumura) through isoflavone-mediated antibiosis in soybean cultivar ‘Zhongdou 27’
journal, August 2011


Activation of members of a MAPK module in β-glucan elicitor-mediated non-host resistance of soybean
journal, November 2006


Differential expression of CHS7 and CHS8 genes in soybean
journal, December 2009


The transcriptional network of WRKY53 in cereals links oxidative responses to biotic and abiotic stress inputs
journal, April 2014

  • Van Eck, Leon; Davidson, Rebecca M.; Wu, Shuchi
  • Functional & Integrative Genomics, Vol. 14, Issue 2
  • DOI: 10.1007/s10142-014-0374-3

Antifeedant activity of luteolin and genistein against the pea aphid, Acyrthosiphon pisum
journal, June 2012


Constitutive and Induced Activities of Defense-Related Enzymes in Aphid-Resistant and Aphid-Susceptible Cultivars of Wheat
journal, January 2009


Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M
journal, November 2006


Transcriptional responses of tolerant and susceptible soybeans to soybean aphid (Aphis glycines Matsumura) herbivory
journal, March 2015

  • Prochaska, T. J.; Donze-Reiner, T.; Marchi-Werle, L.
  • Arthropod-Plant Interactions, Vol. 9, Issue 4
  • DOI: 10.1007/s11829-015-9371-2

Effect of infestation by aphids on the water status of barley and insect development
journal, November 1995


Compatible plant-aphid interactions: How aphids manipulate plant responses
journal, June 2010

  • Giordanengo, Philippe; Brunissen, Laurence; Rusterucci, Christine
  • Comptes Rendus Biologies, Vol. 333, Issue 6-7
  • DOI: 10.1016/j.crvi.2010.03.007

Regiospecific methylation of naringenin to ponciretin by soybean O-methyltransferase expressed in Escherichia coli
journal, September 2005


Signaling Mechanisms in Pattern-Triggered Immunity (PTI)
journal, April 2015


Effector proteins that modulate plant–insect interactions
journal, August 2011


Flavone synthase II (CYP93B16) from soybean (Glycine max L.)
journal, April 2010


Intraspecific variation in alkaloid profile of four lupine species with implications for the pea aphid probing behaviour
journal, March 2012


Recognizing Plant Defense Priming
journal, October 2016


Investigation of the Chemical Interface in the Soybean–Aphid and Rice–Bacteria Interactions Using MALDI-Mass Spectrometry Imaging
journal, May 2015


Flavonoids with mosquito larval toxicity
journal, June 1990

  • Rao, Koppaka V.; Chattopadhyay, Sunil K.; Reddy, G. Chandrasekhara
  • Journal of Agricultural and Food Chemistry, Vol. 38, Issue 6
  • DOI: 10.1021/jf00096a028

Secondary Metabolites from Glycine soja and Their Growth Inhibitory Effect against Spodoptera litura
journal, June 2011

  • Zhou, Yan-Ying; Luo, Shi-Hong; Yi, Ting-Shuang
  • Journal of Agricultural and Food Chemistry, Vol. 59, Issue 11
  • DOI: 10.1021/jf200821p

MAP kinase signalling cascade in Arabidopsis innate immunity
journal, February 2002

  • Asai, Tsuneaki; Tena, Guillaume; Plotnikova, Joulia
  • Nature, Vol. 415, Issue 6875
  • DOI: 10.1038/415977a

Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes
journal, February 2000

  • Jung, Woosuk; Yu, Oliver; Lau, Sze-Mei Cindy
  • Nature Biotechnology, Vol. 18, Issue 2
  • DOI: 10.1038/72671

SNARE-protein-mediated disease resistance at the plant cell wall
journal, October 2003

  • Collins, Nicholas C.; Thordal-Christensen, Hans; Lipka, Volker
  • Nature, Vol. 425, Issue 6961
  • DOI: 10.1038/nature02076

Genome sequence of the palaeopolyploid soybean
journal, January 2010

  • Schmutz, Jeremy; Cannon, Steven B.; Schlueter, Jessica
  • Nature, Vol. 463, Issue 7278
  • DOI: 10.1038/nature08670

Networking by small-molecule hormones in plant immunity
journal, April 2009

  • Pieterse, Corné M. J.; Leon-Reyes, Antonio; Van der Ent, Sjoerd
  • Nature Chemical Biology, Vol. 5, Issue 5
  • DOI: 10.1038/nchembio.164

Synergism between IL7R and CXCR4 drives BCR-ABL induced transformation in Philadelphia chromosome-positive acute lymphoblastic leukemia
journal, June 2020


The role of sinigrin in host plant recognition by aphids during initial plant penetration
journal, July 2002


Plant–aphid interactions with a focus on legumes
journal, January 2013

  • Kamphuis, Lars G.; Zulak, Katherine; Gao, Ling-Ling
  • Functional Plant Biology, Vol. 40, Issue 12
  • DOI: 10.1071/fp13090

Components of the SNARE-containing regulon are co-regulated in root cells undergoing defense
journal, February 2017


MedicCyc: a biochemical pathway database for Medicago truncatula
journal, March 2007


Economic Threshold for Soybean Aphid (Hemiptera: Aphididae)
journal, August 2007

  • Ragsdale, D. W.; McCornack, B. P.; Venette, R. C.
  • Journal of Economic Entomology, Vol. 100, Issue 4
  • DOI: 10.1093/jee/100.4.1258

Resistance to Aphis glycines (Hemiptera: Aphididae) in Various Soybean Lines Under Controlled Laboratory Conditions
journal, August 2007

  • Hesler, Louis S.; Dashiell, Kenton E.
  • Journal of Economic Entomology, Vol. 100, Issue 4
  • DOI: 10.1093/jee/100.4.1464

Evaluation of Artificial Diets for Rearing Aphis glycines (Hemiptera: Aphididae)
journal, August 2008


Salivary secretions by aphids interacting with proteins of phloem wound responses
journal, February 2006

  • Tjallingii, W. Fred
  • Journal of Experimental Botany, Vol. 57, Issue 4
  • DOI: 10.1093/jxb/erj088

Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects
journal, February 2006

  • Thompson, Gary A.; Goggin, Fiona L.
  • Journal of Experimental Botany, Vol. 57, Issue 4
  • DOI: 10.1093/jxb/erj135

HOS3, an ELO-Like Gene, Inhibits Effects of ABA and Implicates a S-1-P/Ceramide Control System for Abiotic Stress Responses in Arabidopsis thaliana
journal, January 2009

  • Quist, Tanya M.; Sokolchik, Irina; Shi, Huazhong
  • Molecular Plant, Vol. 2, Issue 1
  • DOI: 10.1093/mp/ssn085

BLAST: at the core of a powerful and diverse set of sequence analysis tools
journal, July 2004

  • McGinnis, S.; Madden, T. L.
  • Nucleic Acids Research, Vol. 32, Issue Web Server
  • DOI: 10.1093/nar/gkh435

SoyBase, the USDA-ARS soybean genetics and genomics database
journal, December 2009

  • Grant, David; Nelson, Rex T.; Cannon, Steven B.
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp798

The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases
journal, November 2011

  • Caspi, R.; Altman, T.; Dreher, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1014

Toward Understanding the Role of Aphid Effectors in Plant Infestation
journal, January 2013

  • Rodriguez, Patricia A.; Bos, Jorunn I. B.
  • Molecular Plant-Microbe Interactions®, Vol. 26, Issue 1
  • DOI: 10.1094/mpmi-05-12-0119-fi

Multiple Phytohormone Signals Control the Transcriptional Response to Soybean Aphid Infestation in Susceptible and Resistant Soybean Plants
journal, January 2013

  • Studham, Matthew E.; MacIntosh, Gustavo C.
  • Molecular Plant-Microbe Interactions, Vol. 26, Issue 1
  • DOI: 10.1094/mpmi-05-12-0124-fi

Ethylene-Responsive Element-Binding Factor 5, ERF5, Is Involved in Chitin-Induced Innate Immunity Response
journal, January 2012

  • Son, Geon Hui; Wan, Jinrong; Kim, Hye Jin
  • Molecular Plant-Microbe Interactions®, Vol. 25, Issue 1
  • DOI: 10.1094/mpmi-06-11-0165

Signal Signature and Transcriptome Changes of Arabidopsis During Pathogen and Insect Attack
journal, September 2005

  • De Vos, Martin; Van Oosten, Vivian R.; Van Poecke, Remco M. P.
  • Molecular Plant-Microbe Interactions®, Vol. 18, Issue 9
  • DOI: 10.1094/mpmi-18-0923

Recognition of Herbivory-Associated Molecular Patterns
journal, March 2008


Avoiding Effective Defenses: Strategies Employed by Phloem-Feeding Insects
journal, March 2008


Flavonoids and Isoflavonoids: From Plant Biology to Agriculture and Neuroscience
journal, October 2010


Phosphorylation of a WRKY Transcription Factor by Two Pathogen-Responsive MAPKs Drives Phytoalexin Biosynthesis in Arabidopsis
journal, April 2011


Performance and prospects of Rag genes for management of soybean aphid
journal, May 2013

  • Hesler, Louis S.; Chiozza, Mariana V.; O'Neal, Matthew E.
  • Entomologia Experimentalis et Applicata, Vol. 147, Issue 3
  • DOI: 10.1111/eea.12073

Functional analysis of soybean genes involved in flavonoid biosynthesis by virus-induced gene silencing
journal, November 2007


Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach
journal, February 2004

  • Storey, John D.; Taylor, Jonathan E.; Siegmund, David
  • Journal of the Royal Statistical Society: Series B (Statistical Methodology), Vol. 66, Issue 1
  • DOI: 10.1111/j.1467-9868.2004.00439.x

Soybean defense responses to the soybean aphid
journal, July 2008


The molecular bases of plant resistance and defense responses to aphid feeding: current status
journal, January 2007


Abscisic acid deficiency increases defence responses against Myzus persicae in Arabidopsis: ABA deficiency and increased resistance to aphids
journal, June 2015

  • Hillwig, Melissa S.; Chiozza, Mariana; Casteel, Clare L.
  • Molecular Plant Pathology, Vol. 17, Issue 2
  • DOI: 10.1111/mpp.12274

Hormone Crosstalk in Plant Disease and Defense: More Than Just JASMONATE-SALICYLATE Antagonism
journal, September 2011


Plant Immunity to Insect Herbivores
journal, June 2008


Phytohormone signaling pathway analysis method for comparing hormone responses in plant-pest interactions
journal, July 2012


A Model-Based Background Adjustment for Oligonucleotide Expression Arrays
journal, December 2004

  • Wu, Zhijin; Irizarry, Rafael A.; Gentleman, Robert
  • Journal of the American Statistical Association, Vol. 99, Issue 468
  • DOI: 10.1198/016214504000000683

Soybean Aphid Infestation Induces Changes in Fatty Acid Metabolism in Soybean
journal, December 2015


Constitutive and Induced Differential Accumulation of Amino Acid in Leaves of Susceptible and Resistant Soybean Plants in Response to the Soybean Aphid (Hemiptera: Aphididae)
journal, June 2010

  • Chiozza, Mariana V.; O'Neal, Matthew E.; MacIntosh, Gustavo C.
  • Environmental Entomology, Vol. 39, Issue 3
  • DOI: 10.1603/en09338

Biology of the Soybean Aphid, Aphis glycines (Hemiptera: Aphididae) in the United States
journal, October 2011

  • Tilmon, K. J.; Hodgson, E. W.; O'Neal, M. E.
  • Journal of Integrated Pest Management, Vol. 2, Issue 2
  • DOI: 10.1603/ipm10016

A Single Dominant Gene for Resistance to the Soybean Aphid in the Soybean Cultivar Dowling
journal, July 2006


Soybean Aphid Resistance in Soybean Jackson Is Controlled by a Single Dominant Gene
journal, July 2006


Discovery of Soybean Aphid Biotypes
journal, January 2008


Inheritance of Soybean Aphid Resistance in PI 567541B and PI 567598B
journal, September 2008


Structural Features of the Endogenous CHS Silencing and Target Loci in the Soybean Genome
journal, March 2008


Determinación y cuantificación de bacterias acidolácticas por PCR en tiempo real
journal, January 2010

  • Phandanouvong, Vienvilay; Betancourt, Liliana; Rodriguez, Fernando
  • Revista MVZ Córdoba, Vol. 15, Issue 1
  • DOI: 10.21897/rmvz.327

Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants
journal, January 2013

  • Nuruzzaman, Mohammed; Sharoni, Akhter M.; Kikuchi, Shoshi
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00248

Insect-Induced Daidzein, Formononetin and Their Conjugates in Soybean Leaves
journal, July 2014

  • Murakami, Shinichiro; Nakata, Ryu; Aboshi, Takako
  • Metabolites, Vol. 4, Issue 3
  • DOI: 10.3390/metabo4030532

Negative regulation of ABA signaling by WRKY33 is critical for Arabidopsis immunity towards Botrytis cinerea 2100
journal, June 2015


Works referencing / citing this record:

Molecular Basis of Soybean Resistance to Soybean Aphids and Soybean Cyst Nematodes
journal, September 2019

  • Neupane, Surendra; Purintun, Jordan M.; Mathew, Febina M.
  • Plants, Vol. 8, Issue 10
  • DOI: 10.3390/plants8100374

Molecular Basis of Soybean Resistance to Soybean Aphids and Soybean Cyst Nematodes
journal, September 2019

  • Neupane, Surendra; Purintun, Jordan M.; Mathew, Febina M.
  • Plants, Vol. 8, Issue 10
  • DOI: 10.3390/plants8100374