Plant Bio-Wars: Maize Protein Networks Reveal Tissue-Specific Defense Strategies in Response to a Root Herbivore

Lina Castano-Duque, Anjel Helms, Jared Gregory Ali, Dawn S. Luthe

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

In this study we examined global changes in protein expression in both roots and leaves of maize plants attacked by the root herbivore, Western corn rootworm (WCR, Diabrotica virgifera virgifera). The changes in protein expression Are indicative of metabolic changes during WCR feeding that enable the plant to defend itself. This is one of the first studies to look above- and below-ground at global protein expression patterns of maize plants grown in soil and infested with a root herbivore. We used advanced proteomic and network analyses to identify metabolic pathways that contribute to global defenses deployed by the insect resistant maize genotype, Mp708, infested with WCR. Using proteomic analysis, 4878 proteins in roots and leaves were detected and of these 863 showed significant changes of abundance during WCR infestation. Protein abundance patterns were analyzed using hierarchical clustering, protein correlation and protein-protein interaction networks. All three data analysis pipelines showed that proteins such as jasmonic acid biosynthetic enzymes, serine proteases, protease inhibitors, proteins involved in biosynthesis and signaling of ethylene, and enzymes producing reactive oxygen species and isopentenyl pyrophosphate, a precursor for volatile production, were upregulated in roots during WCR infestation. In leaves, highly abundant proteins were involved in signal perception suggesting activation of systemic signaling. We conclude that these protein networks contribute to the overall herbivore defense mechanisms in Mp708. Because the plants were grown in potting mix and not sterilized sand, we found that both microbial and insect defense-related proteins were present in the roots. The presence of the high constitutive levels of reduced ascorbate in roots and benzothiazole in the root volatile profiles suggest a tight tri-trophic interaction among the plant, soil microbiomes and WCR-infested roots suggesting that defenses against insects coexist with defenses against bacteria and fungi due to the interaction between roots and soil microbiota. In this study, which is one of the most complete descriptions of plant responses to root-feeding herbivore, we established an analysis pipeline for proteomics data that includes network biology that can be used with different types of “omics” data from a variety of organisms.

Original languageEnglish (US)
Pages (from-to)727-745
Number of pages19
JournalJournal of Chemical Ecology
Volume44
Issue number7-8
DOIs
StatePublished - Aug 1 2018

Fingerprint

Herbivory
Zea mays
herbivore
herbivores
maize
Tissue
protein
corn
Proteins
proteins
protein synthesis
proteomics
Proteomics
Diabrotica virgifera virgifera
Insects
Soil
Microbiota
insects
insect
Soils

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Biochemistry

Cite this

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title = "Plant Bio-Wars: Maize Protein Networks Reveal Tissue-Specific Defense Strategies in Response to a Root Herbivore",
abstract = "In this study we examined global changes in protein expression in both roots and leaves of maize plants attacked by the root herbivore, Western corn rootworm (WCR, Diabrotica virgifera virgifera). The changes in protein expression Are indicative of metabolic changes during WCR feeding that enable the plant to defend itself. This is one of the first studies to look above- and below-ground at global protein expression patterns of maize plants grown in soil and infested with a root herbivore. We used advanced proteomic and network analyses to identify metabolic pathways that contribute to global defenses deployed by the insect resistant maize genotype, Mp708, infested with WCR. Using proteomic analysis, 4878 proteins in roots and leaves were detected and of these 863 showed significant changes of abundance during WCR infestation. Protein abundance patterns were analyzed using hierarchical clustering, protein correlation and protein-protein interaction networks. All three data analysis pipelines showed that proteins such as jasmonic acid biosynthetic enzymes, serine proteases, protease inhibitors, proteins involved in biosynthesis and signaling of ethylene, and enzymes producing reactive oxygen species and isopentenyl pyrophosphate, a precursor for volatile production, were upregulated in roots during WCR infestation. In leaves, highly abundant proteins were involved in signal perception suggesting activation of systemic signaling. We conclude that these protein networks contribute to the overall herbivore defense mechanisms in Mp708. Because the plants were grown in potting mix and not sterilized sand, we found that both microbial and insect defense-related proteins were present in the roots. The presence of the high constitutive levels of reduced ascorbate in roots and benzothiazole in the root volatile profiles suggest a tight tri-trophic interaction among the plant, soil microbiomes and WCR-infested roots suggesting that defenses against insects coexist with defenses against bacteria and fungi due to the interaction between roots and soil microbiota. In this study, which is one of the most complete descriptions of plant responses to root-feeding herbivore, we established an analysis pipeline for proteomics data that includes network biology that can be used with different types of “omics” data from a variety of organisms.",
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Plant Bio-Wars : Maize Protein Networks Reveal Tissue-Specific Defense Strategies in Response to a Root Herbivore. / Castano-Duque, Lina; Helms, Anjel; Ali, Jared Gregory; Luthe, Dawn S.

In: Journal of Chemical Ecology, Vol. 44, No. 7-8, 01.08.2018, p. 727-745.

Research output: Contribution to journalArticle

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T2 - Maize Protein Networks Reveal Tissue-Specific Defense Strategies in Response to a Root Herbivore

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