An Arabidopsis berberine bridge enzyme‐like protein specifically oxidizes cellulose oligomers and plays a role in immunity

Abstract

Summary The plant cell wall is the barrier that pathogens must overcome to cause a disease, and to this end they secrete enzymes that degrade the various cell wall components. Due to the complexity of these components, several types of oligosaccharide fragments may be released during pathogenesis and some of these can act as damage‐associated molecular patterns (DAMPs). Well‐known DAMPs are the oligogalacturonides (OGs) released upon degradation of homogalacturonan and the products of cellulose breakdown, i.e. the cellodextrins (CDs). We have previously reported that four Arabidopsis berberine bridge enzyme‐like (BBE‐like) proteins (OGOX1–4) oxidize OGs and impair their elicitor activity. We show here that another Arabidopsis BBE‐like protein, which is expressed coordinately with OGOX1 during immunity, specifically oxidizes CDs with a preference for cellotriose (CD3) and longer fragments (CD4–CD6). Oxidized CDs show a negligible elicitor activity and are less easily utilized as a carbon source by the fungus Botrytis cinerea. The enzyme, named CELLOX (cellodextrin oxidase), is encoded by the gene At4 g20860. Plants overexpressing CELLOX display an enhanced resistance to B. cinerea, probably because oxidized CDs are a less valuable carbon source. Thus, the capacity to oxidize and impair the biological activity of cell wall‐derived oligosaccharides seems to be a general trait of the family of BBE‐like proteins, which may serve to homeostatically control the level of DAMPs to prevent their hyperaccumulation.

The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics

“…Moreover, oxidized cellodextrins are a less valuable carbon source for the pathogenic fungus, further limiting fungal growth. Based on these results, the authors speculated that other members of the large BBE-like family may control the homeostasis of CW fragments other than OGs and cellodextrins (Locci et al, 2019). The pectin matrix is the main CW target of B. cinerea.…”

“…Besides OGs, cellodextrins, which are by-products of cellulose breakdown, are also well-known DAMPs. Recently, Locci et al (2019) showed enhanced resistance to B. cinerea in Arabidopsis plants overexpressing a berberine bridge enzyme-like (BBE-like) protein named CELLOX (cellodextrin oxidase), which is the only BBE-like enzyme identified so far that oxidizes cellulose fragments but not glucose. Restriction of fungal growth might arise from the overexpression of BBE-like enzyme which may have prevented the accumulation of the cellodextrins-type DAMPS.…”

Green Production and Biotechnological Applications of Cell Wall Lytic Enzymes

“…Moreover, the degradation of cell wall polysaccharides provides sugars for sustaining the heterotrophic growth of phytopathogens inside the plant tissue [84]. In order to counteract the various CWLEs secreted by the pathogen, plants synthesize different specialized defense proteins that hinder their hydrolytic activity [38,[85][86][87][88]. Moreover, plants have evolved a complex system of cell surface receptors that promptly perceive CWLEs by sensing the products of their activity (i.e., cell wall derived fragments, formerly known as damage-associated molecular patterns (DAMPs) [89][90][91]), or to perceive the CWLEs themselves [92,93] as microbe-associated molecular patterns (MAMPs) by specific recognition mechanisms [94].…”

“…Therefore, an uncontrolled activity of cellulolytic enzymes could lead to hyperactivation of immune responses and, consequently, largely affect plant growth and development. This scenario is avoided naturally by plants, since they are endowed with an enzymatic system that can inactivate, through specific modifications, the elicitor activity of different types of oligosaccharins [87,88]. This plant characteristic should be further investigated and exploited to optimize CWLE production in this host.…”

“…Transgenic microbes from Thricoderma species (commonly used as biocontrol agents) expressing a glucose oxidase from Aspergillus niger (goxA) showed an improved ability both to inhibit phytopathogens and to induce systemic resistance in plants [165]. Interestingly, five berberine-bridge enzyme-like proteins (BBEls) from Arabidopsis thaliana are capable of oxidizing oligosaccharides released from the plant cell wall by microbial CWLEs [87,88]. Amongst them, BBEls encoded by the genes AT4G20830 and AT4G20860, named as OG-oxidase 1 (OGOX1) and Cellodextrin-oxidase (CELLOX), specifically oxidized OGs and cellodextrins (CDs), respectively.…”