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Aphid Feeding Activates Expression of a Transcriptome of Oxylipin-based Defense Signals in Wheat Involved in Resistance to Herbivory

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Abstract

Damage by the Russian wheat aphid (RWA), Diuraphis noxia, significantly reduces wheat and barley yields worldwide. In compatible interactions, virulent RWA populations flourish and susceptible plants suffer extensive leaf chlorophyll loss. In incompatible interactions, RWA reproduction and population growth are significantly reduced and RWA-related chlorophyll loss in resistant plants is minor. The objectives of this study were to develop an understanding of the molecular and phytochemical bases of RWA resistance in plants containing the Dnx resistance gene. Microarray, real-time polymerase chain reaction, and phytohormone assays were conducted to identify transcriptome components unique to RWA-infested Dnx plants and susceptible (Dn0) plants, and to identify and characterize putative genes involved in Dnx plant defense responses. We found that RWA-infested Dnx plants upregulated >180 genes related to reactive oxygen species, signaling, pathogen defense, and arthropod allelochemical and physical defense. The expression of several of these genes in RWA-infested Dnx plants increased significantly from 6- to 24-h post infestation (hpi), but their expression in Dn0 plants, when present, was delayed until 48- to 96 hpi. Concentrations of 16- and 18-carbon fatty acids, trans-methyl-12-oxophytodienoic acid, and abscisic acid were significantly greater in Dnx foliage than in Dn0 foliage after RWA infestation, suggesting that Dnx RWA defense and resistance genes may be regulated via the oxylipin pathway. These findings provide a foundation for the elucidation of the molecular basis for compatible- and incompatible plant-aphid interactions.

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Acknowledgments

We thank Nanyan Lu for helpful comments and support in the Affymetrix array data acquisition. This research was supported by a Kansas Crop Improvement Association grant to CMS and is contribution No. 08-151-J of the Kansas Agricultural Experiment Station. This research was performed in the Gene Expression Facility at Kansas State University, which is supported through the National Science Foundation grant, DBI 0421427. Plant phytohormone analyses were performed at the Kansas Lipidomics Research Center Analytical Laboratory, supported by the Functional Genomics Consortium initiative of Kansas State University’s Targeted Excellence Program. The Kansas Lipidomics Research Center is supported by National Science Foundation (EPS 0236913, MCB 0455318, DBI 0521587), Kansas Technology Enterprise Corporation, K-IDeA Networks of Biomedical Research Excellence (INBRE) of National Institute of Health (P20RR16475), and Kansas State University.

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Authors and Affiliations

  1. Department of Entomology, Kansas State University, Manhattan, KS, 66506, USA

    Charles Michael Smith, Xuming Liu & Sharon Starkey

  2. Division of Biology, Clemson University, Clemson, SC, 29631, USA

    Liang J. Wang

  3. Department of Plant Biology, North Carolina State University, Raleigh, NC, 27695, USA

    Xiang Liu

  4. USDA/ARS Plant Science Laboratory, Manhattan, KS, 66506, USA

    Ming-Shun Chen

  5. Department of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS, 66506, USA

    Jianfa Bai

Authors
  1. Charles Michael Smith
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  2. Xuming Liu
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  3. Liang J. Wang
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  4. Xiang Liu
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  6. Sharon Starkey
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Correspondence to Charles Michael Smith.

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Supplemental Table 1

Mean gene upregulation (fold change) in wheat plant leaves containing the Dnx gene for resistance at 24 h after phloem feeding by Russian wheat aphid biotype 1 (DOC 62 kb)

Supplemental Table 2

Mean gene up regulation (fold change) in leaves of Russian wheat aphid (RWA)-susceptible (Dn0) wheat plants at 24 hr after phloem feeding by RWA biotype 1 (DOC 57 kb)

Supplemental Table 3

Mean gene down regulation (fold change) in wheat plant leaves containing the Dnx gene for resistance at 24 h after phloem feeding by Russian wheat aphid biotype 1 (DOC 34 kb)

Supplemental Table 4

Mean gene down regulation (fold change) in leaves of Russian wheat aphid (RWA)-susceptible (Dn0) wheat plants at 24 h after phloem feeding by RWA biotype 1 (DOC 38 kb)

Supplemental Data Fig. 1

The reaction versus cycle graph of Q9P3N1 Real-time PCR. (PPT 73 kb)

Supplemental Data Fig. 2

The standard curve of Q9P3N1 Real-Time PCR: K = −2.511, B = 14.570, R2 = 0.998. (PPT 72 kb)

Supplemental Data Fig. 3

The reaction versus cycle graph of Q5ZD81 Real-time PCR. (PPT 73 kb)

Supplemental Data Fig. 4

The standard curve of Q5ZD81 Real-time PCR: K = −2.132, B = 2.126, R2 = 1.000. (PPT 72 kb)

Supplemental Data Fig. 5

The reaction versus cycle graph of Q6Z1A3 Real-time PCR. (PPT 76 kb)

Supplemental Data Fig. 6

The standard curve of Q6Z1A3 Real-time PCR: K = −3.423, B = −23.048, R2 = 0.996. (PPT 72 kb)

Supplemental Data Fig. 7

The reaction versus cycle graph of Q6Z1A3 Real-time PCR. (PPT 73 kb)

Supplemental Data Fig. 8

The standard curve of Q6Z1A3 Real-time PCR: K = −3.207, B = −4.493, R2 = 0.999. (PPT 72 kb)

Supplemental Data Fig. 9

The reaction versus cycle graph of Q7XN01 Real-time PCR. (PPT 75 kb)

Supplemental Data Fig. 10

The standard curve of Q7XN01 Real-time PCR: K = −3.726, B = 24.987, R2 = 0.995. (PPT 73 kb)

Supplemental Data Fig. 11

The reaction versus cycle graph of Q6I5G9 Real-time PCR. (PPT 75 kb)

Supplemental Data Fig. 12

The standard curve of Q6I5G9 Real-time PCR: K = −3.250, B = 14.675, R2 = 0.994. (PPT 72 kb)

Supplemental Data Fig. 13

The reaction versus cycle graph of AB18199 (actin control) Real-time PCR. (PPT 74 kb)

Supplemental Data Fig. 14

The standard curve of AB18199 (actin control) Real-time PCR: K = −3.129, B = −34.47, R2 = 0.991. (PPT 73 kb)

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Smith, C.M., Liu, X., Wang, L.J. et al. Aphid Feeding Activates Expression of a Transcriptome of Oxylipin-based Defense Signals in Wheat Involved in Resistance to Herbivory. J Chem Ecol 36, 260–276 (2010). https://doi.org/10.1007/s10886-010-9756-8

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  • DOI: https://doi.org/10.1007/s10886-010-9756-8

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