A Cell Wall–Degrading Esterase of Xanthomonas oryzae Requires a Unique Substrate Recognition Module for Pathogenesis on Rice

Abstract

Xanthomonas oryzae pv oryzae (Xoo) causes bacterial blight, a serious disease of rice (Oryza sativa). LipA is a secretory virulence factor of Xoo, implicated in degradation of rice cell walls and the concomitant elicitation of innate immune responses, such as callose deposition and programmed cell death. Here, we present the high-resolution structural characterization of LipA that reveals an all-helical ligand binding module as a distinct functional attachment to the canonical hydrolase catalytic domain. We demonstrate that the enzyme binds to a glycoside ligand through a rigid pocket comprising distinct carbohydrate-specific and acyl chain recognition sites where the catalytic triad is situated 15 Å from the anchored carbohydrate. Point mutations disrupting the carbohydrate anchor site or blocking the pocket, even at a considerable distance from the enzyme active site, can abrogate in planta LipA function, exemplified by loss of both virulence and the ability to elicit host defense responses. A high conservation of the module across genus Xanthomonas emphasizes the significance of this unique plant cell wall-degrading function for this important group of plant pathogenic bacteria. A comparison with the related structural families illustrates how a typical lipase is recruited to act on plant cell walls to promote virulence, thus providing a remarkable example of the emergence of novel functions around existing scaffolds for increased proficiency of pathogenesis during pathogen-plant coevolution.

Genome Content and Phylogenomics Reveal both Ancestral and Lateral Evolutionary Pathways in Plant-Pathogenic Streptomyces Species

“…Pectate lyases, cellulases, and lipases are virulence factors in other plant pathogens (37). Pectate lyases have been described in the plant-pathogenic bacterium Erwinia chrysanthemi.…”

Isolation of a Novel Cutinase Homolog with Polyethylene Terephthalate-Degrading Activity from Leaf-Branch Compost by Using a Metagenomic Approach

“…For example, the plant pathogenic bacterium Xanthomonas oryzae secrets an esterase, LipA, which is involved in degradation of cell walls in a synergetic manner with other cell wall-degrading enzymes (5). In EXPO Park, Japan, leaves and branches cut from the trees are collected periodically, mixed with urea, and agitated for composting.…”

The short form of the recombinant CAL-A-type lipase UM03410 from the smut fungus Ustilago maydis exhibits an inherent trans-fatty acid selectivity

“…A rice cell wall-degrading esterase (PDB entry: 3h2g) with a high structural homology to CAL-A (PDB entries: 2veo and 3guu) has been recently identified. This esterase belongs to X. oryzae, which is the causing agent of bacterial blight of rice plants (Aparna et al 2009). Despite of a sequence identity of only 17%, the crystal structures of the prototypic CAL-A and the X. oryzae esterase have a long substrate-binding tunnel in common, which is formed by a series of consecutive α-helices.…”