Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores

Appel, Heidi M.; Fescemyer, Howard; Ehlting, Juergen; Weston, David; Rehrig, Erin; Joshi, Trupti; Xu, Dong; Bohlmann, Joerg; Schultz, Jack

doi:10.3389/fpls.2014.00565

Title: Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores

Journal Article · Fri Nov 14 00:00:00 EST 2014 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2014.00565· OSTI ID:1265717

Appel, Heidi M. ^[1]; Fescemyer, Howard ^[2]; Ehlting, Juergen ^[3]; Weston, David ^[4]; Rehrig, Erin ^[5]; Joshi, Trupti ^[1]; Xu, Dong ^[1]; Bohlmann, Joerg ^[6]; Schultz, Jack ^[1]

Univ. of Missouri, Columbia, MO (United States)
Pennsylvania State Univ., University Park, PA (United States)
Univ. of British Columbia, Vancouver, BC (Canada); Univ. of Victoria, BC (Canada)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Fitchburg State Univ., Fitchburg, MA (United States)
Univ. of British Columbia, Vancouver, BC (Canada)

We tested the hypothesis that Arabidopsis can recognize and respond differentially to insect species at the transcriptional level using a genome wide microarray. Transcriptional reprogramming was characterized using co-expression analysis in damaged and undamaged leaves at two times in response to mechanical wounding and four insect species. In all, 2778 (10.6%) of annotated genes on the array were differentially expressed in at least one treatment. Responses differed mainly between aphid and caterpillar and sampling times. Responses to aphids and caterpillars shared only 10% of up-regulated and 8% of down-regulated genes. Responses to two caterpillars shared 21 and 12% of up- and down-regulated genes, whereas responses to the two aphids shared only 7 and 4% of up-regulated and down-regulated genes. Overlap in genes expressed between 6 and 24 h was 3–15%, and depended on the insect species. Responses in attacked and unattacked leaves differed at 6 h but converged by 24 h. Genes responding to the insects are also responsive to many stressors and included primary metabolism. Aphids down-regulated amino acid catabolism; caterpillars stimulated production of amino acids involved in glucosinolate synthesis. Co-expression analysis revealed 17 response networks. Transcription factors were a major portion of differentially expressed genes throughout and responsive genes shared most of the known or postulated binding sites. However, cis-element composition of genes down regulated by the aphid M. persicae was unique, as were those of genes down-regulated by caterpillars. As many as 20 cis-elements were over-represented in one or more treatments, including some from well-characterized classes and others as yet uncharacterized. We suggest that transcriptional changes elicited by wounding and insects are heavily influenced by transcription factors and involve both enrichment of a common set of cis-elements and a unique enrichment of a few cis-elements in responding genes.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1265717

Journal Information:: Frontiers in Plant Science, Vol. 5; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 55 works

Citation information provided by
Web of Science

References (110)

Balancing act: matching growth with environment by the TOR signalling pathway Henriques, Rossana; Bögre, László; Horváth, Beátrix Journal of Experimental Botany, Vol. 65, Issue 10 https://doi.org/10.1093/jxb/eru049	journal	February 2014
Characterization of the VIER F-BOX PROTEINE Genes from Arabidopsis Reveals Their Importance for Plant Growth and Development Schwager, Katja M.; Calderon-Villalobos, Luz Irina A.; Dohmann, Esther M. N. The Plant Cell, Vol. 19, Issue 4 https://doi.org/10.1105/tpc.105.040675	journal	April 2007
SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots Schwachtje, J.; Minchin, P. E. H.; Jahnke, S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 34 https://doi.org/10.1073/pnas.0602316103	journal	August 2006
Transcriptional Regulation of Sorghum Defense Determinants against a Phloem-Feeding Aphid Zhu-Salzman, Keyan; Salzman, Ron A.; Ahn, Ji-Eun Plant Physiology, Vol. 134, Issue 1 https://doi.org/10.1104/pp.103.028324	journal	December 2003
A General Framework for Weighted Gene Co-Expression Network Analysis Zhang, Bin; Horvath, Steve Statistical Applications in Genetics and Molecular Biology, Vol. 4, Issue 1 https://doi.org/10.2202/1544-6115.1128	journal	January 2005
Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense Arnold, Tom; Appel, Heidi; Patel, Vishal New Phytologist, Vol. 164, Issue 1 https://doi.org/10.1111/j.1469-8137.2004.01157.x	journal	July 2004
The TOR Pathway Modulates the Structure of Cell Walls in Arabidopsis Leiber, Ruth-Maria; John, Florian; Verhertbruggen, Yves The Plant Cell, Vol. 22, Issue 6 https://doi.org/10.1105/tpc.109.073007	journal	June 2010
Comparative physiology and transcriptional networks underlying the heat shock response in Populus trichocarpa, Arabidopsis thaliana and Glycine max: Comparative analysis of the heat shock response Weston, David J.; Karve, Abhijit A.; Gunter, Lee E. Plant, Cell & Environment, Vol. 34, Issue 9 https://doi.org/10.1111/j.1365-3040.2011.02347.x	journal	June 2011
Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Abe, H.; Yamaguchi-Shinozaki, K.; Urao, T. The Plant Cell, Vol. 9, Issue 10 https://doi.org/10.1105/tpc.9.10.1859	journal	October 1997
The role of protein effectors in plant–aphid interactions Elzinga, Dezi A.; Jander, Georg Current Opinion in Plant Biology, Vol. 16, Issue 4 https://doi.org/10.1016/j.pbi.2013.06.018	journal	August 2013
A Gibbs Sampling Method to Detect Overrepresented Motifs in the Upstream Regions of Coexpressed Genes Thijs, Gert; Marchal, Kathleen; Lescot, Magali Journal of Computational Biology, Vol. 9, Issue 2 https://doi.org/10.1089/10665270252935566	journal	April 2002
beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Mattiacci, L.; Dicke, M.; Posthumus, M. A. Proceedings of the National Academy of Sciences, Vol. 92, Issue 6 https://doi.org/10.1073/pnas.92.6.2036	journal	March 1995
Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor) Aggarwal, Rajat; Subramanyam, Subhashree; Zhao, Chaoyang PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0100958	journal	June 2014
Biological functions of asparagine synthetase in plants Gaufichon, Laure; Reisdorf-Cren, Michèle; Rothstein, Steven J. Plant Science, Vol. 179, Issue 3 https://doi.org/10.1016/j.plantsci.2010.04.010	journal	September 2010
Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory Verhage, Adriaan Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00047	journal	January 2011
Connecting genes, coexpression modules, and molecular signatures to environmental stress phenotypes in plants Weston, David J.; Gunter, Lee E.; Rogers, Alistair BMC Systems Biology, Vol. 2, Issue 1 https://doi.org/10.1186/1752-0509-2-16	journal	February 2008
Role of phytohormones in insect-specific plant reactions Erb, Matthias; Meldau, Stefan; Howe, Gregg A. Trends in Plant Science, Vol. 17, Issue 5 https://doi.org/10.1016/j.tplants.2012.01.003	journal	May 2012
The nematode resistance gene Mi of tomato confers resistance against the potato aphid Rossi, M.; Goggin, F. L.; Milligan, S. B. Proceedings of the National Academy of Sciences, Vol. 95, Issue 17 https://doi.org/10.1073/pnas.95.17.9750	journal	August 1998
Transcriptional and metabolic signatures of Arabidopsis responses to chewing damage by an insect herbivore and bacterial infection and the consequences of their interaction Appel, Heidi M.; Maqbool, Shahina B.; Raina, Surabhi Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00441	journal	September 2014
Sensing nutrient and energy status by SnRK1 and TOR kinases Robaglia, Christophe; Thomas, Martine; Meyer, Christian Current Opinion in Plant Biology, Vol. 15, Issue 3 https://doi.org/10.1016/j.pbi.2012.01.012	journal	June 2012
An Elicitor of Plant Volatiles from Beet Armyworm Oral Secretion Alborn, H. T.; Turlings, T. C. J.; Jones, T. H. Science, Vol. 276, Issue 5314 https://doi.org/10.1126/science.276.5314.945	journal	May 1997
In silico analysis of promoter regions from cold-induced genes in rice (Oryza sativa L.) and Arabidopsis thaliana reveals the importance of combinatorial control Lindlöf, Angelica; Bräutigam, Marcus; Chawade, Aakash Bioinformatics, Vol. 25, Issue 11 https://doi.org/10.1093/bioinformatics/btp172	journal	March 2009
Prediction of transcriptional regulatory elements for plant hormone responses based on microarray data Yamamoto, Yoshiharu Y.; Yoshioka, Yohei; Hyakumachi, Mitsuro BMC Plant Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2229-11-39	journal	January 2011
From signatures to models: understanding cancer using microarrays Segal, Eran; Friedman, Nir; Kaminski, Naftali Nature Genetics, Vol. 37, Issue S6 https://doi.org/10.1038/ng1561	journal	June 2005
Biotic stress globally downregulates photosynthesis genes: Biotic stress downregulates photosynthesis Bilgin, Damla D.; Zavala, Jorge A.; Zhu, Jin Plant, Cell & Environment, Vol. 33, Issue 10 https://doi.org/10.1111/j.1365-3040.2010.02167.x	journal	September 2010
The unfolded protein response in plants: A fundamental adaptive cellular response to internal and external stresses Journal of Proteomics, Vol. 93 https://doi.org/10.1016/j.jprot.2013.04.023	journal	November 2013
Induced Responses to Herbivory Karban, Richard; Baldwin, Ian T. University of Chicago Press https://doi.org/10.7208/chicago/9780226424972.001.0001	book	January 1997
Aphid saliva Miles, Peter W. Biological Reviews of the Cambridge Philosophical Society, Vol. 74, Issue 1 https://doi.org/10.1017/S0006323198005271	journal	February 1999
Evidence for an Important Role of WRKY DNA Binding Proteins in the Regulation of NPR1 Gene Expression Yu, D. THE PLANT CELL ONLINE, Vol. 13, Issue 7 https://doi.org/10.1105/tpc.13.7.1527	journal	July 2001
Measuring ‘normalcy’ in plant gene expression after herbivore attack: TECHNICAL ADVANCES Rehrig, ERIN MacNEAL; Appel, Heidi M.; Schultz, Jack C. Molecular Ecology Resources, Vol. 11, Issue 2 https://doi.org/10.1111/j.1755-0998.2010.02929.x	journal	November 2010
The Tomato Transcription Factor Pti4 Regulates Defense-Related Gene Expression via GCC Box and Non-GCC Box cis Elements Chakravarthy, Suma; Tuori, Robert P.; D'Ascenzo, Mark D. The Plant Cell, Vol. 15, Issue 12 https://doi.org/10.1105/tpc.017574	journal	November 2003
ABI1 and PP2CA Phosphatases Are Negative Regulators of Snf1-Related Protein Kinase1 Signaling in Arabidopsis Rodrigues, Américo; Adamo, Mattia; Crozet, Pierre The Plant Cell, Vol. 25, Issue 10 https://doi.org/10.1105/tpc.113.114066	journal	October 2013
An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Giuliano, G.; Pichersky, E.; Malik, V. S. Proceedings of the National Academy of Sciences, Vol. 85, Issue 19 https://doi.org/10.1073/pnas.85.19.7089	journal	October 1988
Experience‐based food consumption by larvae of Pieris rapae : addiction to glucosinolates? Renwick, J. A. A.; Lopez, Kimberly Entomologia Experimentalis et Applicata, Vol. 91, Issue 1 https://doi.org/10.1046/j.1570-7458.1999.00465.x	journal	April 1999
Predicting Gene Expression from Sequence Beer, Michael A.; Tavazoie, Saeed Cell, Vol. 117, Issue 2 https://doi.org/10.1016/S0092-8674(04)00304-6	journal	April 2004
Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation: Global transcript profiling of stems Ehlting, Jürgen; Mattheus, Nathalie; Aeschliman, Dana S. The Plant Journal, Vol. 42, Issue 5 https://doi.org/10.1111/j.1365-313X.2005.02403.x	journal	April 2005
Flexible resource allocation during plant defense responses Schultz, Jack C.; Appel, Heidi M.; Ferrieri, Abigail P. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00324	journal	January 2013
Insect Herbivores Drive Real-Time Ecological and Evolutionary Change in Plant Populations Agrawal, Anurag A.; Hastings, Amy P.; Johnson, Marc T. J. Science, Vol. 338, Issue 6103 https://doi.org/10.1126/science.1225977	journal	October 2012
DELLA proteins modulate Arabidopsis defences induced in response to caterpillar herbivory Lan, Zhiyi; Krosse, Sebastian; Achard, Patrick Journal of Experimental Botany, Vol. 65, Issue 2 https://doi.org/10.1093/jxb/ert420	journal	January 2014
Comparative transcriptome analysis of Arabidopsis thaliana infested by diamond back moth (Plutella xylostella) larvae reveals signatures of stress response, secondary metabolism, and signaling Ehlting, Juergen; Chowrira, Sunita G.; Mattheus, Nathalie BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-154	journal	January 2008
Different Lepidopteran Elicitors Account for Cross-Talk in Herbivory-Induced Phytohormone Signaling Diezel, Celia; von Dahl, Caroline C.; Gaquerel, Emmanuel Plant Physiology, Vol. 150, Issue 3 https://doi.org/10.1104/pp.109.139550	journal	May 2009
A critical review of translation initiation factor eIF2α kinases in plants - regulating protein synthesis during stress Immanuel, Tracey M.; Greenwood, David R.; MacDiarmid, Robin M. Functional Plant Biology, Vol. 39, Issue 9 https://doi.org/10.1071/FP12116	journal	January 2012
AREB1 Is a Transcription Activator of Novel ABRE-Dependent ABA Signaling That Enhances Drought Stress Tolerance in Arabidopsis Fujita, Yasunari; Fujita, Miki; Satoh, Rie The Plant Cell, Vol. 17, Issue 12 https://doi.org/10.1105/tpc.105.035659	journal	November 2005
Experimentally Determined Sequence Requirement of ACGT-Containing Abscisic Acid Response Element Hattori, Tsukaho; Totsuka, Masako; Hobo, Tokunori Plant and Cell Physiology, Vol. 43, Issue 1 https://doi.org/10.1093/pcp/pcf014	journal	January 2002
Herbivore-associated elicitors: FAC signaling and metabolism Bonaventure, Gustavo; VanDoorn, Arjen; Baldwin, Ian T. Trends in Plant Science, Vol. 16, Issue 6 https://doi.org/10.1016/j.tplants.2011.01.006	journal	June 2011
Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways Mewis, Inga; Tokuhisa, James G.; Schultz, Jack C. Phytochemistry, Vol. 67, Issue 22 https://doi.org/10.1016/j.phytochem.2006.09.004	journal	November 2006
Impact of folivory on photosynthesis is greater than the sum of its holes Zangerl, A. R.; Hamilton, J. G.; Miller, T. J. Proceedings of the National Academy of Sciences, Vol. 99, Issue 2 https://doi.org/10.1073/pnas.022647099	journal	January 2002
Natural Enemies Drive Geographic Variation in Plant Defenses Züst, Tobias; Heichinger, Christian; Grossniklaus, Ueli Science, Vol. 338, Issue 6103 https://doi.org/10.1126/science.1226397	journal	October 2012
Damaged-self recognition in plant herbivore defence Heil, Martin Trends in Plant Science, Vol. 14, Issue 7 https://doi.org/10.1016/j.tplants.2009.04.002	journal	July 2009
Variance stabilization applied to microarray data calibration and to the quantification of differential expression Huber, W.; von Heydebreck, A.; Sultmann, H. Bioinformatics, Vol. 18, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/18.suppl_1.S96	journal	July 2002
Aphid Gel Saliva: Sheath Structure, Protein Composition and Secretory Dependence on Stylet-Tip Milieu Will, Torsten; Steckbauer, Kathrin; Hardt, Martin PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0046903	journal	October 2012
Induction and Suppression of Herbivore-Induced Indirect Defenses Alba, Juan M.; Allmann, Silke; Glas, Joris J. Biocommunication of Plants https://doi.org/10.1007/978-3-642-23524-5_11	book	December 2011
Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases Crozet, Pierre; Margalha, Leonor; Confraria, Ana Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00190	journal	May 2014
Feeding and Life History of <I>Spodoptera exigua</I> (Lepidoptera: Noctuidae) on Different Host Plants Greenberg, S. M.; Sappington, T. W.; Legaspi, B. C. Annals of the Entomological Society of America, Vol. 94, Issue 4 https://doi.org/10.1603/0013-8746(2001)094[0566:FALHOS]2.0.CO;2	journal	July 2001
The role of WRKY transcription factors in plant abiotic stresses Chen, Ligang; Song, Yu; Li, Shujia Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1819, Issue 2 https://doi.org/10.1016/j.bbagrm.2011.09.002	journal	February 2012
RuBPCase activase (RCA) mediates growth-defense trade-offs: silencing RCA redirects jasmonic acid (JA) flux from JA-isoleucine to methyl jasmonate (MeJA) to attenuate induced defense responses in Nicotiana attenuata Mitra, Sirsha; Baldwin, Ian T. New Phytologist, Vol. 201, Issue 4 https://doi.org/10.1111/nph.12591	journal	November 2013
Transcriptional Regulation in Plants: The Importance of Combinatorial Control Singh, Karam B. Plant Physiology, Vol. 118, Issue 4 https://doi.org/10.1104/pp.118.4.1111	journal	December 1998
Effects of jasmonic acid, branching and girdling on carbon and nitrogen transport in poplar Appel, Heidi M.; Arnold, Thomas M.; Schultz, Jack C. New Phytologist, Vol. 195, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04171.x	journal	May 2012
Specialist versus generalist insect herbivores and plant defense Ali, Jared G.; Agrawal, Anurag A. Trends in Plant Science, Vol. 17, Issue 5 https://doi.org/10.1016/j.tplants.2012.02.006	journal	May 2012
Comparison of Transcript Profiling on Arabidopsis Microarray Platform Technologies Pylatuik, Jeffrey D.; Fobert, Pierre R. Plant Molecular Biology, Vol. 58, Issue 5 https://doi.org/10.1007/s11103-005-6506-3	journal	July 2005
HORMONOMETER: A Tool for Discerning Transcript Signatures of Hormone Action in the Arabidopsis Transcriptome Volodarsky, Dina; Leviatan, Noam; Otcheretianski, Andrei Plant Physiology, Vol. 150, Issue 4 https://doi.org/10.1104/pp.109.138289	journal	June 2009
Energy Signaling in the Regulation of Gene Expression during Stress Baena-González, Elena Molecular Plant, Vol. 3, Issue 2 https://doi.org/10.1093/mp/ssp113	journal	March 2010
Insect oral secretions suppress wound-induced responses in Arabidopsis Consales, Floriane; Schweizer, Fabian; Erb, Matthias Journal of Experimental Botany, Vol. 63, Issue 2 https://doi.org/10.1093/jxb/err308	journal	October 2011
Phylogenetic and Molecular Evidence for Allochronic Speciation in Gall-Forming Aphids (Pemphigus) Abbot, Patrick; Withgott, James H. Evolution, Vol. 58, Issue 3 https://doi.org/10.1111/j.0014-3820.2004.tb01677.x	journal	March 2004
Unifying concepts and mechanisms in the specificity of plant–enemy interactions Barrett, Luke G.; Heil, Martin Trends in Plant Science, Vol. 17, Issue 5 https://doi.org/10.1016/j.tplants.2012.02.009	journal	May 2012
The interface between metabolic and stress signalling Hey, S. J.; Byrne, E.; Halford, N. G. Annals of Botany, Vol. 105, Issue 2 https://doi.org/10.1093/aob/mcp285	journal	December 2009
Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata . VII. Changes in the Plant's Proteome Giri, Ashok P.; Wünsche, Hendrik; Mitra, Sirsha Plant Physiology, Vol. 142, Issue 4 https://doi.org/10.1104/pp.106.088781	journal	October 2006
Convergent energy and stress signaling Baena-González, Elena; Sheen, Jen Trends in Plant Science, Vol. 13, Issue 9 https://doi.org/10.1016/j.tplants.2008.06.006	journal	September 2008
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
Conserved versatile master regulators in signalling pathways in response to stress in plants Balderas-Hernandez, V. E.; Alvarado-Rodriguez, M.; Fraire-Velazquez, S. AoB PLANTS, Vol. 5, Issue 0 https://doi.org/10.1093/aobpla/plt033	journal	January 2013
Orchestrated Transcription of Key Pathways in Arabidopsis by the Circadian Clock Harmer, S. L.; Hogenesch, J. B.; Straume, M. Science, Vol. 290, Issue 5499 https://doi.org/10.1126/science.290.5499.2110	journal	December 2000
Roles for jasmonate- and ethylene-induced transcription factors in the ability of Arabidopsis to respond differentially to damage caused by two insect herbivores Rehrig, Erin M.; Appel, Heidi M.; Jones, A. Daniel Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00407	journal	August 2014
Major Signaling Pathways Modulate Arabidopsis Glucosinolate Accumulation and Response to Both Phloem-Feeding and Chewing Insects Mewis, Inga; Appel, Heidi M.; Hom, Amanda Plant Physiology, Vol. 138, Issue 2 https://doi.org/10.1104/pp.104.053389	journal	May 2005
Master regulators in plant glucose signaling networks Sheen, Jen Journal of Plant Biology, Vol. 57, Issue 2 https://doi.org/10.1007/s12374-014-0902-7	journal	March 2014
The differential effects of herbivory by first and fourth instars of Trichoplusia ni (Lepidoptera: Noctuidae) on photosynthesis in Arabidopsis thaliana Tang, Jennie Y.; Zielinski, Raymond E.; Zangerl, Arthur R. Journal of Experimental Botany, Vol. 57, Issue 3 https://doi.org/10.1093/jxb/erj032	journal	December 2005
Expression Profile Matrix of Arabidopsis Transcription Factor Genes Suggests Their Putative Functions in Response to Environmental Stresses Chen, Wenqiong; Provart, Nicholas J.; Glazebrook, Jane The Plant Cell, Vol. 14, Issue 3 https://doi.org/10.1105/tpc.010410	journal	March 2002
Butterflies and Plants: A Study in Coevolution Ehrlich, Paul R.; Raven, Peter H. Evolution, Vol. 18, Issue 4 https://doi.org/10.2307/2406212	journal	December 1964
Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors Xu, Xinping; Chen, Chunhong; Fan, Baofang The Plant Cell, Vol. 18, Issue 5 https://doi.org/10.1105/tpc.105.037523	journal	April 2006
Sucrose and invertases, a part of the plant defense response to the biotic stresses Tauzin, Alexandra S.; Giardina, Thierry Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00293	journal	June 2014
β -Subunits of the SnRK1 Complexes Share a Common Ancestral Function Together with Expression and Function Specificities; Physical Interaction with Nitrate Reductase Specifically Occurs via AKIN β 1-Subunit Polge, Cécile; Jossier, Mathieu; Crozet, Pierre Plant Physiology, Vol. 148, Issue 3 https://doi.org/10.1104/pp.108.123026	journal	September 2008
Plant cis-acting regulatory DNA elements (PLACE) database: 1999 Higo, K.; Ugawa, Y.; Iwamoto, M. Nucleic Acids Research, Vol. 27, Issue 1 https://doi.org/10.1093/nar/27.1.297	journal	January 1999
An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores Bidart-Bouzat, M. Gabriela; Kliebenstein, Daniel Oecologia, Vol. 167, Issue 3 https://doi.org/10.1007/s00442-011-2015-z	journal	May 2011
Transcriptional profiling of an Fd-GOGAT1/GLU1 mutant in Arabidopsis thaliana reveals a multiple stress response and extensive reprogramming of the transcriptome Kissen, Ralph; Winge, Per; Tran, Diem BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-190	journal	January 2010
Induced plant defences: from molecular biology to evolutionary ecology Dicke, Marcel; Hilker, Monika Basic and Applied Ecology, Vol. 4, Issue 1 https://doi.org/10.1078/1439-1791-00129	journal	January 2003
Macroevolution and the biological diversity of plants and herbivores Futuyma, D. J.; Agrawal, A. A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 43 https://doi.org/10.1073/pnas.0904106106	journal	October 2009
Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana Zou, C.; Sun, K.; Mackaluso, J. D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 36 https://doi.org/10.1073/pnas.1103202108	journal	August 2011
Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences O'Connor, T. R.; Dyreson, C.; Wyrick, J. J. Bioinformatics, Vol. 21, Issue 24 https://doi.org/10.1093/bioinformatics/bti714	journal	October 2005
The HERBIVORE ELICITOR-REGULATED1 Gene Enhances Abscisic Acid Levels and Defenses against Herbivores in Nicotiana attenuata Plants Dinh, Son Truong; Baldwin, Ian T.; Galis, Ivan Plant Physiology, Vol. 162, Issue 4 https://doi.org/10.1104/pp.113.221150	journal	June 2013
Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase Luna, Estrella; van Hulten, Marieke; Zhang, Yuhua Nature Chemical Biology, Vol. 10, Issue 6 https://doi.org/10.1038/nchembio.1520	journal	April 2014
Coexpression landscape in ATTED-II: usage of gene list and gene network for various types of pathways Obayashi, Takeshi; Kinoshita, Kengo Journal of Plant Research, Vol. 123, Issue 3 https://doi.org/10.1007/s10265-010-0333-6	journal	April 2010
Why Does Herbivore Attack Reconfigure Primary Metabolism? Schwachtje, Jens; Baldwin, Ian T. Plant Physiology, Vol. 146, Issue 3 https://doi.org/10.1104/pp.107.112490	journal	March 2008
A higher-order background model improves the detection of promoter regulatory elements by Gibbs sampling Thijs, G.; Lescot, M.; Marchal, K. Bioinformatics, Vol. 17, Issue 12 https://doi.org/10.1093/bioinformatics/17.12.1113	journal	December 2001
Phytohormonal signaling in plant responses to aphid feeding Morkunas, Iwona; Mai, Van Chung; Gabryś, Beata Acta Physiologiae Plantarum, Vol. 33, Issue 6 https://doi.org/10.1007/s11738-011-0751-7	journal	April 2011
The GCN2 homologue in Arabidopsis thaliana interacts with uncharged tRNA and uses Arabidopsis eIF2α molecules as direct substrates : AtGCN2 interacts with uncharged tRNA and acts on eIF2α Li, M. -W.; AuYeung, W. -K.; Lam, H. -M. Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1111/j.1438-8677.2012.00606.x	journal	June 2012
Natural elicitors, effectors and modulators of plant responses Maffei, Massimo E.; Arimura, Gen-Ichiro; Mithöfer, Axel Natural Product Reports, Vol. 29, Issue 11 https://doi.org/10.1039/c2np20053h	journal	January 2012
Plant Transcriptomic Responses to Herbivory Heidel-Fischer, Hanna M.; Musser, Richard O.; Vogel, Heiko Annual Plant Reviews: Insect‐Plant Interactions https://doi.org/10.1002/9781118829783.ch5	book	January 2014
Interactions between the jasmonic and salicylic acid pathway modulate the plant metabolome and affect herbivores of different feeding types: Phytohormone interactions affect metabolome and herbivores Schweiger, R.; Heise, A. -M.; Persicke, M. Plant, Cell & Environment, Vol. 37, Issue 7 https://doi.org/10.1111/pce.12257	journal	February 2014
Voluntary exposure to a toxin: the genetic influence on ethanol consumption Hoffman, Paula L.; Saba, Laura M.; Vanderlinden, Lauren A. Mammalian Genome, Vol. 29, Issue 1-2 https://doi.org/10.1007/s00335-017-9726-3	journal	December 2017
Perception, signaling and molecular basis of oviposition-mediated plant responses Reymond, Philippe Planta, Vol. 238, Issue 2 https://doi.org/10.1007/s00425-013-1908-y	journal	June 2013
Into a dilemma of plants: the antagonism between chemical defenses and growth Sestari, Ivan; Campos, Marcelo Lattarulo Plant Molecular Biology, Vol. 109, Issue 4-5 https://doi.org/10.1007/s11103-021-01213-0	journal	November 2021
Interactions of Bacillus thuringiensis Cry1Ac toxin in genetically engineered cotton with predatory heteropterans Torres, Jorge B.; Ruberson, John R. Transgenic Research, Vol. 17, Issue 3 https://doi.org/10.1007/s11248-007-9109-8	journal	June 2007
New fatty acid amides from regurgitant of Lepidopteran (Noctuidae, Geometridae) caterpillars Pohnert, Georg; Jung, Verena; Haukioja, Erkki Tetrahedron, Vol. 55, Issue 37 https://doi.org/10.1016/s0040-4020(99)00639-0	journal	September 1999
Identification and Distinct Regulation of Yeast TATA Box-Containing Genes Basehoar, Andrew D.; Zanton, Sara J.; Pugh, B. Franklin Cell, Vol. 116, Issue 5 https://doi.org/10.1016/s0092-8674(04)00205-3	journal	March 2004
Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways Shinozaki, Kazuo; Yamaguchi-Shinozaki, Kazuko Current Opinion in Plant Biology, Vol. 3, Issue 3 https://doi.org/10.1016/s1369-5266(00)80068-0	journal	January 2000
Genome-wide characterization of the sorghum JAZ gene family and their responses to phytohormone treatments and aphid infestation Shrestha, Kumar; Huang, Yinghua Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-07181-9	journal	February 2022
Constitutive Activation of Jasmonate Signaling in an Arabidopsis Mutant Correlates with Enhanced Resistance to Erysiphe cichoracearum , Pseudomonas syringae , and Myzus persicae Ellis, Christine; Karafyllidis, Ioannis; Turner, John G. Molecular Plant-Microbe Interactions, Vol. 15, Issue 10 https://doi.org/10.1094/mpmi.2002.15.10.1025	journal	October 2002
Phylogenetic and Molecular Evidence for Allochronic Speciation in Gall-Forming Aphids (Pemphigus) Abbot, Patrick; Withgott, James H. Evolution, Vol. 58, Issue 3 https://doi.org/10.1554/03-043	journal	January 2004
Self-assembly of embryonic and two extra-embryonic stem cell types into gastrulating embryo-like structures. Sozen, Berna; Amadei, Gianluca; Cox, Andy Springer Science and Business Media LLC https://doi.org/10.17863/cam.41771	journalarticle	January 2018
Evidence for an Important Role of WRKY DNA Binding Proteins in the Regulation of NPR1 Gene Expression Yu, Diqiu; Chen, Chunhong; Chen, Zhixiang The Plant Cell, Vol. 13, Issue 7 https://doi.org/10.2307/3871384	journal	July 2001
The TOR pathway modulates the structure of cell walls in Arabidopsis M., Leiber, R.; F., John,; Y., Verhertbruggen, American Society of Plant Biologists https://doi.org/10.5167/uzh-43473	text	January 2010

Cited By (14)

Different soybean cultivars respond differentially to damage in a herbivore-specific manner and decreas herbivore performance Romero, Berenice; Dillon, Francisco M.; Zavala, Jorge A. Arthropod-Plant Interactions, Vol. 14, Issue 1 https://doi.org/10.1007/s11829-019-09730-y	journal	November 2019
Moth oviposition shapes the species-specific transcriptional and phytohormonal response of Nicotiana attenuata to larval feeding Drok, Sylvia; Bandoly, Michele; Stelzer, Sandra Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-28233-z	journal	July 2018
Functional characterization of drought-responsive modules and genes in Oryza sativa: a network-based approach Sircar, Sanchari; Parekh, Nita Frontiers in Genetics, Vol. 6 https://doi.org/10.3389/fgene.2015.00256	journal	July 2015
Spatiotemporal Transcriptome Analysis Provides Insights into Bicolor Tepal Development in Lilium “Tiny Padhye” Xu, Leifeng; Yang, Panpan; Feng, Yayan Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00398	journal	March 2017
Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thaliana Body, Mélanie J. A.; Neer, William C.; Vore, Caitlin Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00810	journal	June 2019
Brevicoryne brassicae aphids interfere with transcriptome responses of Arabidopsis thaliana to feeding by Plutella xylostella caterpillars in a density-dependent manner Kroes, Anneke; Broekgaarden, Colette; Castellanos Uribe, Marcos Oecologia, Vol. 183, Issue 1 https://doi.org/10.1007/s00442-016-3758-3	journal	October 2016
Resource allocation in response to herbivory and gall formation in Linaria vulgaris Zorić, Ana Sedlarević; Morina, Filis; Toševski, Ivo Plant Physiology and Biochemistry, Vol. 135 https://doi.org/10.1016/j.plaphy.2018.11.032	journal	February 2019
Simulated herbivory in chickpea causes rapid changes in defense pathways and hormonal transcription networks of JA/ethylene/GA/auxin within minutes of wounding Pandey, Saurabh Prakash; Srivastava, Shruti; Goel, Ridhi Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep44729	journal	March 2017
Rapid defense responses in maize leaves induced by Spodoptera exigua caterpillar feeding Tzin, Vered; Hojo, Yuko; Strickler, Susan R. Journal of Experimental Botany, Vol. 68, Issue 16 https://doi.org/10.1093/jxb/erx274	journal	July 2017
Natural variation in life history strategy of Arabidopsis thaliana determines stress responses to drought and insects of different feeding guilds Davila Olivas, Nelson H.; Frago, Enric; Thoen, Manus P. M. Molecular Ecology, Vol. 26, Issue 11 https://doi.org/10.1111/mec.14100	journal	April 2017
Combined transcriptome and metabolome analyses to understand the dynamic responses of rice plants to attack by the rice stem borer Chilo suppressalis (Lepidoptera: Crambidae) Liu, Qingsong; Wang, Xingyun; Tzin, Vered BMC Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12870-016-0946-6	journal	December 2016
Co-expression network analysis of the transcriptomes of rice roots exposed to various cadmium stresses reveals universal cadmium-responsive genes Tan, Mingpu; Cheng, Dan; Yang, Yuening BMC Plant Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12870-017-1143-y	journal	November 2017
Transcriptomics and Alternative Splicing Analyses Reveal Large Differences between Maize Lines B73 and Mo17 in Response to Aphid Rhopalosiphum padi Infestation Song, Juan; Liu, Hui; Zhuang, Huifu Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01738	journal	October 2017
Acibenzolar-S-Methyl Reprograms Apple Transcriptome Toward Resistance to Rosy Apple Aphid Warneys, Romain; Gaucher, Matthieu; Robert, Philippe Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01795	journal	December 2018

Similar Records

Insecticide Resistance Mechanisms in the Green Peach Aphid Myzus persicae (Hemiptera: Aphididae) I: A Transcriptomic Survey

Journal Article · Thu Jun 07 00:00:00 EDT 2012 · PLoS ONE · OSTI ID:1265717

Silva, Andrea X.; Jander, Georg; Samaniego, Horacio; +2 more

Modeling temporal and hormonal regulation of plant transcriptional response to wounding

Journal Article · Fri Dec 03 00:00:00 EST 2021 · The Plant Cell · OSTI ID:1265717

Moore, Bethany M.; Lee, Yun Sun; Wang, Peipei; +3 more

Cytochrome P450s CYP380C6 and CYP380C9 in green peach aphid facilitate its adaptation to indole glucosinolate‐mediated plant defense

Journal Article · Thu Aug 20 00:00:00 EDT 2020 · Pest Management Science · OSTI ID:1265717

Ji, Rui; Lei, Jiaxin; Chen, Ivy W.; +4 more

Related Subjects

60 APPLIED LIFE SCIENCES

Title: Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores

Citation Formats

References (110)

Cited By (14)

Similar Records

Related Subjects