Four Arabidopsis berberine bridge enzyme‐like proteins are specific oxidases that inactivate the elicitor‐active oligogalacturonides

• Published in: The Plant journal : for cell and molecular biology Vol. 94; no. 2; pp. 260 - 273
• Main Authors: Benedetti, Manuel, Verrascina, Ilaria, Pontiggia, Daniela, Locci, Federica, Mattei, Benedetta, De Lorenzo, Giulia, Cervone, Felice
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.04.2018
• Subjects: Accumulation; Acrylamide; Affinity chromatography; Alarmins - metabolism; Arabidopsis; Arabidopsis - enzymology; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Berberine; Berberine - metabolism; berberine bridge enzyme BBE‐like proteins; Cell death; Damage patterns; damage‐associated molecular patterns; Degree of polymerization; Enzymes; Flavin-adenine dinucleotide; Homeostasis; Hydrogen peroxide; Immune response; Immunity; Oligogalacturonides; oxidized OGs; Oxidoreductases - metabolism; Pattern recognition; Pectin; Plant Immunity; Plant protection; Polygalacturonase; polygalacturonase‐inhibiting protein; Polymerization; Proteins; Arabidopsis thaliana; oligogalacturonides; damage-associated molecular patterns; polygalacturonase-inhibiting protein; berberine bridge enzyme BBE-like proteins; polygalacturonase; oxidized OGs
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.13852

Summary Recognition of endogenous molecules acting as ‘damage‐associated molecular patterns’ (DAMPs) is a key feature of immunity in both animals and plants. Oligogalacturonides (OGs), i.e. fragments derived from the hydrolysis of homogalacturonan, a major component of pectin are a well known class of DAMPs that activate immunity and protect plants against several microbes. However, hyper‐accumulation of OGs severely affects growth, eventually leading to cell death and clearly pointing to OGs as players in the growth‐defence trade‐off. Here we report a mechanism that may control the homeostasis of OGs avoiding their deleterious hyper‐accumulation. By combining affinity chromatography on acrylamide‐trapped OGs and other procedures, an Arabidopsis thaliana enzyme that specifically oxidizes OGs was purified and identified. The enzyme was named OG OXIDASE 1 (OGOX1) and shown to be encoded by the gene At4g20830. As a typical flavo‐protein, OGOX1 is a sulphite‐sensitive H2O2‐producing enzyme that displays maximal activity on OGs with a degree of polymerization >4. OGOX1 belongs to a large gene family of mainly apoplastic putative FAD‐binding proteins [Berberine Bridge Enzyme‐like (BBE‐like); 27 members], whose biochemical and biological function is largely unexplored. We have found that at least four BBE‐like enzymes in Arabidopsis are OG oxidases (OGOX1–4). Oxidized OGs display a reduced capability of activating the immune responses and are less hydrolysable by fungal polygalacturonases. Plants overexpressing OGOX1 are more resistant to Botrytis cinerea, pointing to a crucial role of OGOX enzymes in plant immunity. Significance Statement An enzyme activity that oxidizes and strongly reduces the elicitor activity of oligogalacturonides (OGs), a class of plant DAMPs, has been identified in Arabidopsis, where at least four genes belonging to the BBE‐like family encode OG oxidases. Oxidation of OGs may play a homeostatic role and finely tune the elicitor‐activity of these molecules, which exert inhibitory effects on plant growth when accumulated at high concentrations.