Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana
- Max Planck Institute for Chemical Ecology, Germany
- Brigham Young University, United States
- Max-Planck Institute for Chemical Ecology, Germany
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
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Evolution of the herbivore associated elicitor induced early defence signalling networks in NicotianaPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE75006).
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Evolution of the herbivore associated elicitor induced early defence signalling networks in NicotianaPublicly available at the NCBI BioProject (accession no: PRJNA301787).
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Tissue specific diurnal rhythm of transcripts and their regulation during herbivore attack in Nicotiana attenuataPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE30287).
Article and author information
Author details
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
© 2016, Zhou et al.
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.
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Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana
eLife 5:e19531.
https://doi.org/10.7554/eLife.19531
Further reading
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Spatial patterns in genetic diversity are shaped by individuals dispersing from their parents and larger-scale population movements. It has long been appreciated that these patterns of movement shape the underlying genealogies along the genome leading to geographic patterns of isolation by distance in contemporary population genetic data. However, extracting the enormous amount of information contained in genealogies along recombining sequences has, until recently, not been computationally feasible. Here we capitalize on important recent advances in genome-wide gene-genealogy reconstruction and develop methods to use thousands of trees to estimate per-generation dispersal rates and to locate the genetic ancestors of a sample back through time. We take a likelihood approach in continuous space using a simple approximate model (branching Brownian motion) as our prior distribution of spatial genealogies. After testing our method with simulations we apply it to Arabidopsis thaliana. We estimate a dispersal rate of roughly 60km2 per generation, slightly higher across latitude than across longitude, potentially reflecting a northward post-glacial expansion. Locating ancestors allows us to visualize major geographic movements, alternative geographic histories, and admixture. Our method highlights the huge amount of information about past dispersal events and population movements contained in genome-wide genealogies.
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The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than ten alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognized.
