Evidence of an evolutionary hourglass pattern in herbivory-induced transcriptomic responses

New Phytol. 2017 Aug;215(3):1264-1273. doi: 10.1111/nph.14644. Epub 2017 Jun 15.

Abstract

Herbivory-induced defenses are specific and activated in plants when elicitors, frequently found in the herbivores' oral secretions, are introduced into wounds during attack. While complex signaling cascades are known to be involved, it remains largely unclear how natural selection has shaped the evolution of these induced defenses. We analyzed herbivory-induced transcriptomic responses in wild tobacco, Nicotiana attenuata, using a phylotranscriptomic approach that measures the origin and sequence divergence of herbivory-induced genes. Highly conserved and evolutionarily ancient genes of primary metabolism were activated at intermediate time points (2-6 h) after elicitation, while less constrained and young genes associated with defense signaling and biosynthesis of specialized metabolites were activated at early (before 2 h) and late (after 6 h) stages of the induced response, respectively - a pattern resembling the evolutionary hourglass pattern observed during embryogenesis in animals and the developmental process in plants and fungi. The hourglass patterns found in herbivory-induced defense responses and developmental process are both likely to be a result of signaling modularization and differential evolutionary constraints on the modules involved in the signaling cascade.

Keywords: Nicotiana attenuata; defense signaling; evolutionary hourglass; herbivory-induced defense; phylotranscriptomic analysis; primary metabolism; specialized metabolism.

MeSH terms

  • Evolution, Molecular*
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Herbivory / genetics*
  • Nicotiana / genetics*
  • Nicotiana / immunology
  • Signal Transduction
  • Transcriptome / genetics*

Associated data

  • GENBANK/GSE90951