Abstract

Lignin is incorporated into plant cell walls to maintain plant architecture and to ensure long-distance water transport. Lignin composition affects the industrial value of plant material for forage, wood and paper production, and biofuel technologies. Industrial demands have resulted in an increase in the use of genetic engineering to modify lignified plant cell wall composition. However, the interaction of the resulting plants with the environment must be analyzed carefully to ensure that there are no undesirable side effects of lignin modification. We show here that Arabidopsis thaliana mutants with impaired 5-hydroxyguaiacyl O-methyltransferase (known as caffeate O-methyltransferase; COMT) function were more susceptible to various bacterial and fungal pathogens. Unexpectedly, asexual sporulation of the downy mildew pathogen, Hyaloperonospora arabidopsidis, was impaired on these mutants. Enhanced resistance to downy mildew was not correlated with increased plant defense responses in comt1 mutants but coincided with a higher frequency of oomycete sexual reproduction within mutant tissues. Comt1 mutants but not wild-type Arabidopsis accumulated soluble 2-O-5-hydroxyferuloyl-l-malate. The compound weakened mycelium vigor and promoted sexual oomycete reproduction when applied to a homothallic oomycete in vitro. These findings suggested that the accumulation of 2-O-5-hydroxyferuloyl-l-malate accounted for the observed comt1 mutant phenotypes during the interaction with H. arabidopsidis. Taken together, our study shows that an artificial downregulation of COMT can drastically alter the interaction of a plant with the biotic environment.

Highlights

  • Lignin accounts for about 30% of the organic carbon in the biosphere and is the second most abundant terrestrial biopolymer after cellulose [1]

  • Because the technological value of plants is determined by the amount and composition of lignin, genetic engineering approaches frequently aim at altering these parameters

  • Data showing how plants with modified lignin content interact with the biotic environment are still scarce

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Summary

Introduction

Lignin accounts for about 30% of the organic carbon in the biosphere and is the second most abundant terrestrial biopolymer after cellulose [1]. Lignin fortifies plant cell walls, is the essential composite of wood, and allows terrestrial plants to gain size and volume. This polymer renders the walls of water-conducting cells impermeable, making it possible for the xylem vessels to transport water [2]. Lignin is a complex aromatic heteropolymer composed of the three phenylalanine-derived monolignols, p-coumaryl-, coniferyl-, and sinapyl alcohol [1,4] (Figure 1). Studies investigating the side effects of changes in COMT gene expression in mutant and transgenic plants remain scarce, it was shown 30 years ago that the bm mutation decreases vascular integrity and stalk robustness in maize [14]

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