Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana

Abstract
Data availability
Article and author information
Metrics

Abstract

Herbivore-induced defenses are widespread, rapidly evolving and relevant for plant fitness. Such induced defenses are often mediated by early defense signaling (EDS) rapidly activated by the perception of herbivore associated elicitors (HAE) that includes transient accumulations of jasmonic acid (JA). Analyzing 60 HAE-induced leaf transcriptomes from closely-related Nicotiana species revealed a key gene co-expression network (M4 module) which is co-activated with the HAE-induced JA accumulations but is elicited independently of JA, as revealed in plants silenced in JA signaling. Functional annotations of the M4 module were consistent with roles in EDS and a newly identified hub gene of the M4 module (NaLRRK1) mediates a negative feedback loop with JA signaling. Phylogenomic analysis revealed preferential gene retention after genome-wide duplications shaped the evolution of HAE-induced EDS in Nicotiana. These results highlight the importance of genome-wide duplications in the evolution of adaptive traits in plants.

Data availability

The following data sets were generated

1. Xu S
(2016) Evolution of the herbivore associated elicitor induced early defence signalling networks in Nicotiana
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE75006).

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE75006
1. Zhou W
2. Brockmöller T
3. Ling Z
4. Omdahl A
5. Baldwin IT
6. Xu S
(2016) Evolution of the herbivore associated elicitor induced early defence signalling networks in Nicotiana
Publicly available at the NCBI BioProject (accession no: PRJNA301787).

http://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA301787

The following previously published data sets were used

1. Kim S
2. Gaquerel E
3. Gulati J
4. Baldwin IT
(2011) Tissue specific diurnal rhythm of transcripts and their regulation during herbivore attack in Nicotiana attenuata
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE30287).

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE30287

Article and author information

Author details

Wenwu Zhou

Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

Competing interests
No competing interests declared.
Thomas Brockmöller

Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

Competing interests
No competing interests declared.
Zhihao Ling

Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

Competing interests
No competing interests declared.
Ashton Omdahl

Brigham Young University, Provo, United States

Competing interests
No competing interests declared.
Ian T Baldwin

Department of Molecular Ecology, Max-Planck Institute for Chemical Ecology, Jena, Germany

Competing interests
Ian T Baldwin, Senior editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0001-5371-2974
Shuqing Xu

Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

For correspondence
sxu@ice.mpg.de

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-7010-4604

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PEBZP3-142886)

Shuqing Xu

European Research Council (293926)

Ian T Baldwin

European Commission (328935)

Shuqing Xu

Max-Planck-Gesellschaft

Wenwu Zhou
Thomas Brockmöller
Zhihao Ling
Ashton Omdahl
Ian T Baldwin
Shuqing Xu

Sutter-Stötner-Stiftung

Shuqing Xu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.