Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant-defense related specialized metabolic pathway

Elife. 2017 Aug 30;6:e28468. doi: 10.7554/eLife.28468.

Abstract

The diversity of life on Earth is a result of continual innovations in molecular networks influencing morphology and physiology. Plant specialized metabolism produces hundreds of thousands of compounds, offering striking examples of these innovations. To understand how this novelty is generated, we investigated the evolution of the Solanaceae family-specific, trichome-localized acylsugar biosynthetic pathway using a combination of mass spectrometry, RNA-seq, enzyme assays, RNAi and phylogenomics in different non-model species. Our results reveal hundreds of acylsugars produced across the Solanaceae family and even within a single plant, built on simple sugar cores. The relatively short biosynthetic pathway experienced repeated cycles of innovation over the last 100 million years that include gene duplication and divergence, gene loss, evolution of substrate preference and promiscuity. This study provides mechanistic insights into the emergence of plant chemical novelty, and offers a template for investigating the ~300,000 non-model plant species that remain underexplored.

Keywords: Solanum lycopersicum; enzyme evolution; evolutionary biology; genomics; phylogenetic reconstruction; plant biology; plant defense; specialized metabolism; trichome.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acylation
  • Acyltransferases / genetics
  • Acyltransferases / metabolism
  • Base Sequence
  • Biological Evolution
  • Carbohydrate Metabolism / genetics*
  • Carbohydrate Metabolism / physiology*
  • Evolution, Molecular*
  • Gene Amplification
  • Gene Knockdown Techniques
  • Gene Silencing
  • Mass Spectrometry
  • Metabolic Networks and Pathways*
  • Phylogeny
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • RNA, Plant
  • Solanaceae / classification
  • Solanaceae / enzymology
  • Solanaceae / genetics
  • Solanaceae / metabolism*
  • Substrate Specificity
  • Sucrose / metabolism
  • Sugars / chemistry
  • Sugars / metabolism
  • Transcriptome
  • Trichomes / enzymology
  • Trichomes / genetics
  • Trichomes / metabolism*

Substances

  • Plant Proteins
  • RNA, Plant
  • Sugars
  • Sucrose
  • Acyltransferases