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

Abstract

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 responsivemore » 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.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [1];  [1];  [6];  [1]
  1. Univ. of Missouri, Columbia, MO (United States)
  2. Pennsylvania State Univ., University Park, PA (United States)
  3. Univ. of British Columbia, Vancouver, BC (Canada); Univ. of Victoria, BC (Canada)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  5. Fitchburg State Univ., Fitchburg, MA (United States)
  6. Univ. of British Columbia, Vancouver, BC (Canada)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1265717
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES

Citation Formats

Appel, Heidi M., Fescemyer, Howard, Ehlting, Juergen, Weston, David, Rehrig, Erin, Joshi, Trupti, Xu, Dong, Bohlmann, Joerg, and Schultz, Jack. Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores. United States: N. p., 2014. Web. doi:10.3389/fpls.2014.00565.
Appel, Heidi M., Fescemyer, Howard, Ehlting, Juergen, Weston, David, Rehrig, Erin, Joshi, Trupti, Xu, Dong, Bohlmann, Joerg, & Schultz, Jack. Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores. United States. https://doi.org/10.3389/fpls.2014.00565
Appel, Heidi M., Fescemyer, Howard, Ehlting, Juergen, Weston, David, Rehrig, Erin, Joshi, Trupti, Xu, Dong, Bohlmann, Joerg, and Schultz, Jack. Fri . "Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores". United States. https://doi.org/10.3389/fpls.2014.00565. https://www.osti.gov/servlets/purl/1265717.
@article{osti_1265717,
title = {Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores},
author = {Appel, Heidi M. and Fescemyer, Howard and Ehlting, Juergen and Weston, David and Rehrig, Erin and Joshi, Trupti and Xu, Dong and Bohlmann, Joerg and Schultz, Jack},
abstractNote = {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.},
doi = {10.3389/fpls.2014.00565},
journal = {Frontiers in Plant Science},
number = ,
volume = 5,
place = {United States},
year = {Fri Nov 14 00:00:00 EST 2014},
month = {Fri Nov 14 00:00:00 EST 2014}
}

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journal, September 2010


Convergent energy and stress signaling
journal, September 2008


Damaged-self recognition in plant herbivore defence
journal, July 2009


Herbivore-associated elicitors: FAC signaling and metabolism
journal, June 2011


Role of phytohormones in insect-specific plant reactions
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Specialist versus generalist insect herbivores and plant defense
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Natural elicitors, effectors and modulators of plant responses
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Experience‐based food consumption by larvae of Pieris rapae : addiction to glucosinolates?
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Impact of folivory on photosynthesis is greater than the sum of its holes
journal, January 2002

  • Zangerl, A. R.; Hamilton, J. G.; Miller, T. J.
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  • DOI: 10.1073/pnas.022647099

SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots
journal, August 2006

  • Schwachtje, J.; Minchin, P. E. H.; Jahnke, S.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 34
  • DOI: 10.1073/pnas.0602316103

Macroevolution and the biological diversity of plants and herbivores
journal, October 2009

  • Futuyma, D. J.; Agrawal, A. A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 43
  • DOI: 10.1073/pnas.0904106106

Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana
journal, August 2011

  • Zou, C.; Sun, K.; Mackaluso, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 36
  • DOI: 10.1073/pnas.1103202108

An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene.
journal, October 1988

  • Giuliano, G.; Pichersky, E.; Malik, V. S.
  • Proceedings of the National Academy of Sciences, Vol. 85, Issue 19
  • DOI: 10.1073/pnas.85.19.7089

The nematode resistance gene Mi of tomato confers resistance against the potato aphid
journal, August 1998

  • Rossi, M.; Goggin, F. L.; Milligan, S. B.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 17
  • DOI: 10.1073/pnas.95.17.9750

Induced plant defences: from molecular biology to evolutionary ecology
journal, January 2003


A Gibbs Sampling Method to Detect Overrepresented Motifs in the Upstream Regions of Coexpressed Genes
journal, April 2002

  • Thijs, Gert; Marchal, Kathleen; Lescot, Magali
  • Journal of Computational Biology, Vol. 9, Issue 2
  • DOI: 10.1089/10665270252935566

The interface between metabolic and stress signalling
journal, December 2009

  • Hey, S. J.; Byrne, E.; Halford, N. G.
  • Annals of Botany, Vol. 105, Issue 2
  • DOI: 10.1093/aob/mcp285

Conserved versatile master regulators in signalling pathways in response to stress in plants
journal, January 2013

  • Balderas-Hernandez, V. E.; Alvarado-Rodriguez, M.; Fraire-Velazquez, S.
  • AoB PLANTS, Vol. 5, Issue 0
  • DOI: 10.1093/aobpla/plt033

A higher-order background model improves the detection of promoter regulatory elements by Gibbs sampling
journal, December 2001


Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences
journal, October 2005


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