Dynamic Maize Responses to Aphid Feeding Are Revealed by a Time Series of Transcriptomic and Metabolomic Assays

Autoren

Vered Tzin
Noe Fernandez-Pozo
Annett Richter
Eric A Schmelz
Matthias Schoettner
Martin Schäfer
Kevin R Ahern
Lisa N Meihls
Harleen Kaur
Alisa Huffaker
Naoki Mori
Jorg Degenhardt
Lukas A Mueller
Georg Jander

DOI

10.1104/pp.15.01039

eISSN

1532-2548

ISSN

0032-0889

Zeitschrift

Plant Physiology

Sprache

en

Online publication date

2015

Paginierung

pp.01039.2015 - pp.01039.2015

Status

Published online

Herausgeber

Oxford University Press (OUP)

Herausgeber URL

http://dx.doi.org/10.1104/pp.15.01039

Datum der Datenerfassung

2021

Titel

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

Data source: Crossref

Abstract

As a response to insect attack, maize (Zea mays) has inducible defenses that involve large changes in gene expression and metabolism. Piercing/sucking insects such as corn leaf aphid (Rhopalosiphum maidis) cause direct damage by acquiring phloem nutrients as well as indirect damage through the transmission of plant viruses. To elucidate the metabolic processes and gene expression changes involved in maize responses to aphid attack, leaves of inbred line B73 were infested with corn leaf aphids for 2 to 96 h. Analysis of infested maize leaves showed two distinct response phases, with the most significant transcriptional and metabolic changes occurring in the first few hours after the initiation of aphid feeding. After 4 d, both gene expression and metabolite profiles of aphid-infested maize reverted to being more similar to those of control plants. Although there was a predominant effect of salicylic acid regulation, gene expression changes also indicated prolonged induction of oxylipins, although not necessarily jasmonic acid, in aphid-infested maize. The role of specific metabolic pathways was confirmed using Dissociator transposon insertions in maize inbred line W22. Mutations in three benzoxazinoid biosynthesis genes, Bx1, Bx2, and Bx6, increased aphid reproduction. In contrast, progeny production was greatly decreased by a transposon insertion in the single W22 homolog of the previously uncharacterized B73 terpene synthases TPS2 and TPS3. Together, these results show that maize leaves shift to implementation of physical and chemical defenses within hours after the initiation of aphid feeding and that the production of specific metabolites can have major effects in maize-aphid interactions.

Addresses

Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (V.T., N.F.-P., K.R.A., L.N.M., H.K., L.A.M., G.J.);Martin Luther University Halle, Wittenberg Institute for Pharmacy, D-06108 Halle, Germany (A.R., J.D.);Division of Biological Sciences, University of California, La Jolla, California 92093 (E.A.S., A.H.);Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany (M.Scho., M.Schä.); andGraduate School of Agriculture, Kyoto University, Kyoto 808-8502, Japan (N.M.).

Autoren

Vered Tzin
Noe Fernandez-Pozo
Annett Richter
Eric A Schmelz
Matthias Schoettner
Martin Schäfer
Kevin R Ahern
Lisa N Meihls
Harleen Kaur
Alisa Huffaker
Naoki Mori
Joerg Degenhardt
Lukas A Mueller
Georg Jander

DOI

10.1104/pp.15.01039

eISSN

1532-2548

Externe Identifier

PubMed Identifier: 26378100

Funding acknowledgements

US National Science Foundation: 1139327
Vaadia-BARD: FI-471-2012
Triad Foundation:
Japan Science and Technology:
Alexander von Humboldt-Stiftung (Humboldt Foundation):
US Department of Agriculture: 2011-67012-30675
US National Science Foundation: 1139329

Open access

false

ISSN

0032-0889

Ausgabe der Veröffentlichung

3

Zeitschrift

Plant physiology

Schlüsselwörter

Animals
Aphids
Zea mays
Plant Leaves
Salicylic Acid
Cyclopentanes
Benzoxazines
Plant Growth Regulators
DNA Transposable Elements
Gene Expression Profiling
Plant Diseases
Gene Expression Regulation, Plant
Mutation
Time Factors
Phloem
Host-Parasite Interactions
Oxylipins
Metabolomics

Sprache

eng

Medium

Print-Electronic

Online publication date

2015

Paginierung

1727 - 1743

Datum der Veröffentlichung

2015

Status

Published

Datum der Datenerfassung

2015

Titel

Dynamic Maize Responses to Aphid Feeding Are Revealed by a Time Series of Transcriptomic and Metabolomic Assays.

Sub types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Journal Article

Ausgabe der Zeitschrift

169

Data source: Europe PubMed Central

Abstract

As a response to insect attack, maize (Zea mays) has inducible defenses that involve large changes in gene expression and metabolism. Piercing/sucking insects such as corn leaf aphid (Rhopalosiphum maidis) cause direct damage by acquiring phloem nutrients as well as indirect damage through the transmission of plant viruses. To elucidate the metabolic processes and gene expression changes involved in maize responses to aphid attack, leaves of inbred line B73 were infested with corn leaf aphids for 2 to 96 h. Analysis of infested maize leaves showed two distinct response phases, with the most significant transcriptional and metabolic changes occurring in the first few hours after the initiation of aphid feeding. After 4 d, both gene expression and metabolite profiles of aphid-infested maize reverted to being more similar to those of control plants. Although there was a predominant effect of salicylic acid regulation, gene expression changes also indicated prolonged induction of oxylipins, although not necessarily jasmonic acid, in aphid-infested maize. The role of specific metabolic pathways was confirmed using Dissociator transposon insertions in maize inbred line W22. Mutations in three benzoxazinoid biosynthesis genes, Bx1, Bx2, and Bx6, increased aphid reproduction. In contrast, progeny production was greatly decreased by a transposon insertion in the single W22 homolog of the previously uncharacterized B73 terpene synthases TPS2 and TPS3. Together, these results show that maize leaves shift to implementation of physical and chemical defenses within hours after the initiation of aphid feeding and that the production of specific metabolites can have major effects in maize-aphid interactions.

Date of acceptance

2015

Autoren

Vered Tzin
Noe Fernandez-Pozo
Annett Richter
Eric A Schmelz
Matthias Schoettner
Martin Schäfer
Kevin R Ahern
Lisa N Meihls
Harleen Kaur
Alisa Huffaker
Naoki Mori
Joerg Degenhardt
Lukas A Mueller
Georg Jander

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/26378100

DOI

10.1104/pp.15.01039

eISSN

1532-2548

Externe Identifier

PubMed Central ID: PMC4634079

Ausgabe der Veröffentlichung

3

Zeitschrift

Plant Physiol

Schlüsselwörter

Animals
Aphids
Benzoxazines
Cyclopentanes
DNA Transposable Elements
Gene Expression Profiling
Gene Expression Regulation, Plant
Host-Parasite Interactions
Metabolomics
Mutation
Oxylipins
Phloem
Plant Diseases
Plant Growth Regulators
Plant Leaves
Salicylic Acid
Time Factors
Zea mays

Sprache

eng

Country

United States

Paginierung

1727 - 1743

PII

pp.15.01039

Datum der Veröffentlichung

2015

Status

Published

Datum, an dem der Datensatz öffentlich gemacht wurde

2016

Titel

Dynamic Maize Responses to Aphid Feeding Are Revealed by a Time Series of Transcriptomic and Metabolomic Assays.

Sub types

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Ausgabe der Zeitschrift

169

Data source: PubMed

Dynamic Maize Responses to Aphid Feeding Are Revealed by a Time Series of Transcriptomic and Metabolomic Assays

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