Modularity of plant metabolic gene clusters: a trio of linked genes that are collectively required for acylation of triterpenes in oat.

Sam T Mugford,George P Lomonossoff,Lionel Hill,Xiaoquan Qi,Anne Osbourn,Rachel Melton,Thomas Louveau,Susan J Rosser,Saleha Bakht,Suvi Honkanen,Tetsu Tsurushima

doi:10.1105/tpc.113.110551

Sam T Mugford, George P Lomonossoff + Show 9 more

Open Access

https://doi.org/10.1105/tpc.113.110551

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Abstract

Operon-like gene clusters are an emerging phenomenon in the field of plant natural products. The genes encoding some of the best-characterized plant secondary metabolite biosynthetic pathways are scattered across plant genomes. However, an increasing number of gene clusters encoding the synthesis of diverse natural products have recently been reported in plant genomes. These clusters have arisen through the neo-functionalization and relocation of existing genes within the genome, and not by horizontal gene transfer from microbes. The reasons for clustering are not yet clear, although this form of gene organization is likely to facilitate co-inheritance and co-regulation. Oats (Avena spp) synthesize antimicrobial triterpenoids (avenacins) that provide protection against disease. The synthesis of these compounds is encoded by a gene cluster. Here we show that a module of three adjacent genes within the wider biosynthetic gene cluster is required for avenacin acylation. Through the characterization of these genes and their encoded proteins we present a model of the subcellular organization of triterpenoid biosynthesis.

Highlights

Plants synthesize a diverse range of specialized metabolites, many of which have important roles in protection against disease, herbivory, and/or abiotic stress (Dixon, 2001; Osbourn and Lanzotti 2009)
Avenacins are synthesized in the epidermal cells of the root tip, and the expression of genes that encode the previously characterized steps in the biosynthetic pathway is restricted to these cells (Qi et al, 2006; Wegel et al, 2009; Mugford et al, 2009)
We have shown that three consecutive genes within the avenacin gene cluster are involved in the acylation of avenacins at the C-21 position and that the failure to correctly acylate avenacins results in enhanced disease susceptibility

Summary

Introduction

Plants synthesize a diverse range of specialized metabolites ( commonly referred to as natural products), many of which have important roles in protection against disease, herbivory, and/or abiotic stress (Dixon, 2001; Osbourn and Lanzotti 2009). Oats (Avena spp) produce antimicrobial triterpene glycosides (avenacins) in their roots that protect against soil-borne pathogens (Hostettmann and Marston, 1995; Papadopoulou et al, 1999; Osbourn et al, 2011). Avenacins exhibit some unusual structural features that are not shared by other plant triterpene glycosides. Most notably, they are acylated at the carbon-21 (C-21) position with either N-methyl anthranilate or benzoate (Figure 1). Understanding the mechanisms underlying this type of modification has potential to provide powerful biotechnological tools for the modification of triterpene structure and function in different biological systems

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