Arabinoxylan-Oligosaccharides Act as Damage Associated Molecular Patterns in Plants Regulating Disease Resistance

Abstract

Immune responses in plants can be triggered by damage/microbe-associated molecular patterns (DAMPs/MAMPs) upon recognition by plant pattern recognition receptors (PRRs). DAMPs are signaling molecules synthesized by plants or released from host cellular structures (e.g., plant cell walls) upon pathogen infection or wounding. Despite the hypothesized important role of plant cell wall-derived DAMPs in plant-pathogen interactions, a very limited number of these DAMPs are well characterized. Recent work demonstrated that pectin-enriched cell wall fractions extracted from the cell wall mutant impaired in Arabidopsis Response Regulator 6 (arr6), that showed altered disease resistance to several pathogens, triggered more intense immune responses than those activated by similar cell wall fractions from wild-type plants. It was hypothesized that arr6 cell wall fractions could be differentially enriched in DAMPs. In this work, we describe the characterization of the previous immune-active fractions of arr6 showing the highest triggering capacities upon further fractionation by chromatographic means. These analyses pointed to a role of pentose-based oligosaccharides triggering plant immune responses. The characterization of several pentose-based oligosaccharide structures revealed that b-1,4-xylooligosaccharides of specific degrees of polymerization and carrying arabinose decorations are sensed as DAMPs by plants. Moreover, the pentasaccharide 3 3-a-L-arabinofuranosyl-xylotetraose (XA3XX) was found as a highly active DAMP structure triggering strong immune responses in Arabidopsis thaliana and enhancing crop disease resistance.

Dampening the DAMPs: How Plants Maintain the Homeostasis of Cell Wall Molecular Patterns and Avoid Hyper-Immunity

“…The pentasaccharide XA3XX triggers an oxidative burst, a rapid calcium influx, the phosphorylation of MPK3 and MPK6, and the upregulation of genes involved in innate immunity, including several PTI marker genes (CYP81F2, WRKY53, PHI1, FRK1, and NHL10). Moreover, tomato plants treated with XA3XX are more resistant to P. syringae pv tomato DC3000, and XA3XX-treated pepper plants are more resistant to Sclerotinia sclerotiorum (Mélida et al, 2020).…”

“…Arabinoxylan (AX), another hemicellulose present in both the primary and secondary walls, consists of copolymers of two pentoses: arabinose and xylose. Very recently, by analyzing mutants in Arabidopsis Response Regulators (ARRs), which mediate cytokinin signaling and modulate the disease resistance (Bacete and Hamann, 2020), it was demonstrated that the AX-derived pentasaccharide 3 3 -α-L-arabinofuranosylxylotetraose (XA3XX) triggers a strong immune response in Arabidopsis and enhances disease resistance of some crop plants (Mélida et al, 2020).…”

“…Arabinoxylan oligosaccharides have been recently identified as novel DAMPs (Mélida et al, 2020). This group of hemicelluloses consists of a main backbone of β-1,4-linked D-xylose residues decorated with single L-arabinose residues linked to the C2/ C3 position of a D-xylose unit (Ebringerová and Heinze, 2000).…”

Fructans Prime ROS Dynamics and Botrytis cinerea Resistance in Arabidopsis

“…Fructans, polysaccharides mainly consisting of 5-membered fructose (Fru) rings, specifically inulin from plant origin, like those derived from chicory (Cichorium intybus) and burdock (Arctium lappa), are able to induce resistance against B. cinerea in lettuce [19]. Recently, xylo-oligosaccharides with 5-membered arabinose side branches were shown to act as DAMPs and elicit immune responses in plants [20]. Hitherto, β-aminobutyric acid (BABA), chitosan and OGs are among the most popular environmentally friendly agents to induce disease resistance in the agronomical context, next to the widespread use of biological control organisms and their culture filtrates (e.g., Trichoderma sp.)…”

Arabidopsiscell wall composition determines disease resistance specificity and fitness

“…Alteration of CWI can initiate the release of DAMPs that regulate plant immune responses in a similar way to those triggered by microbe-associated molecular patterns (MAMPs) ( 6 , 24 , 47 ). Despite the diversity of glycan structures of plant cell walls, only a limited number of wall-associated DAMPs have been identified so far, including some oligosaccharides structures derived from β-1,3-glucan (callose), cellulose, xyloglucan, mannan, homogalacturonan, and arabinoxylan polysaccharides of plant cell walls ( 6 , 8 – 10 , 12 , 47 – 51 ). Modification of CWI also leads to developmental phenotype alterations (e.g., reduced plant size and biomass or fertility), indicating that the cell wall contributes to plant fitness ( 5 , 19 , 52 , 53 ).…”