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Sweet Immunity: plant cell wall is a dynamic structure determining plant disease resistance to pathogens and fitness

Plant cells are surrounded by an extracellular matrix known as cell wall, composed of sugars-based polymers (glycans) and structural glycoproteins. Plant wall is subjected to dynamic remodeling and compositional changes in response to developmental and environmental cues, like those occurring during pathogens infection. It was known that cell wall plays essential functions in plant disease resistance responses, however the specific contributions of cell wall composition on plant resistance and fitness had not been characterized in detail. This key question has been now addressed in the article recently published in the prestigious journal PNAS by the group of Dr. Molina from CBGP (UPM-INA) and collaborators from Complutense University of Madrid, and University and INRAE/CNRS of Toulouse (France) and CRCC of University of Georgia (USA). They used a biosystem approach consisting in the analysis of the disease resistance/fitness phenotypes of a large set of Arabidopsis thaliana mutants with different cell wall composition alterations. The resistance of these mutants to three main type of pathogens (vascular, necrotrophic and biotrophic) that cause important disease and yield losses in crops was determined. The article nicely shows that plant cell wall is a key determinant of plant immune responses since modification of wall composition in this set of plant mutants resulted in a non-anticipated and high impact on their disease resistance with 85% of the mutants tested showing alterations in their defensive responses to at least one of the pathogens analyzed. Notably, authors demonstrate that increasing the resistance of mutants to necrotrophic or vascular pathogens negatively impacted on their biomass and seed yield. Using mathematical modelling they identified correlations between the amounts of specific wall glycans moieties in the cell wall of these plant mutants and their disease resistance and developmental phenotypes. The enhanced resistance to pathogens observed in the Arabidopsis cell wall mutants tested is not mediated by canonical immune pathways and might be determined by glycans released from their cell walls, since wall fractions isolated from the mutants´ walls triggered immune responses when applied to wild-type plants. These data provide the basis for using wall traits in crops breeding programs and for the identification of new cell wall-derived immune-active glycans that could trigger immune responses upon their application to crops and be used to replace chemical pesticides in crop protection, thus contributing to a more sustainable agriculture.

Figure 1. Arabidopsis cell wall mutants show alterations of their disease-resistance phenotypes in comparison to wild-type plants. (A) Clustering of disease-resistance phenotypes of Arabidopsis cell wall mutants to (B) the necrotrophic fungus Plectosphaerella cucumerina (Pc), (C) th vascular bacterium R.alstonia pseudosolanacearum (Rp), and (D) the biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa). Clusters were computed using Euclidean distances using disease-resistance indexes relative to wild-type (wt) plants (DR for Pc and Rp; number of conidiospores per milligram of rosette fresh weight (mg fw) for Hpa).

Original Paper:

Molina, A., Miedes, E., Bacete, L., Rodríguez, T., Mélida, H., Denancé, N., Sánchez-Vallet, A., Rivière, M.-P., López, G., Freydier, A., Barlet, X., Pattathil, S., Hahn, M., Goffner, D. 2021. Arabidopsis cell wall composition determines disease resistance specificity and fitness. Proceedings of the National Academy of Sciences 118, e2010243118. DOI: 10.1073/pnas.2010243118

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