Abstract
Plant cell walls are complex structures subject to dynamic remodeling in response to developmental and environmental cues and play essential functions in disease resistance responses. We tested the specific contribution of plant cell walls to immunity by determining the susceptibility of a set of Arabidopsis cell wall mutants (cwm) to pathogens with different parasitic styles: a vascular bacterium, a necrotrophic fungus, and a biotrophic oomycete. Remarkably, most cwm mutants tested (29/34; 85.3%) showed alterations in their resistance responses to at least one of these pathogens in comparison to wild-type plants, illustrating the relevance of wall composition in determining disease-resistance phenotypes. We found that the enhanced resistance of cwm plants to the necrotrophic and vascular pathogens negatively impacted cwm fitness traits, such as biomass and seed yield. Enhanced resistance of cwm plants is not only mediated by canonical immune pathways, like those modulated by phytohormones or microbe-associated molecular patterns, which are not deregulated in the cwm tested. Pectin-enriched wall fractions isolated from cwm plants triggered immune responses in wild-type plants, suggesting that wall-mediated defensive pathways might contribute to cwm resistance. Cell walls of cwm plants show a high diversity of composition alterations as revealed by glycome profiling that detect specific wall carbohydrate moieties. Mathematical analysis of glycome profiling data identified correlations between the amounts of specific wall carbohydrate moieties and disease resistance phenotypes of cwm plants. These data support the relevant and specific function of plant wall composition in plant immune response modulation and in balancing disease resistance/development trade-offs.
Highlights
Plant cell walls are complex structures subject to dynamic remodeling in response to developmental and environmental cues and play essential functions in disease resistance responses
The second cwm set was composed of 16 transfer DNA (T-DNA) insertional mutants, which were impaired in orthologs of Zinnia elegans genes differentially expressed during xylogenesis, a process involving secondary wall biosynthesis (SI Appendix, Fig. S1) [22]
The majority of these mutations resulted in loss-of-function mutants, as expression of the impaired genes was not detected by RT-PCR or led to truncated proteins, but hypomorphic alleles were included in the analyses
Summary
Plant cell walls are complex structures subject to dynamic remodeling in response to developmental and environmental cues and play essential functions in disease resistance responses. We demonstrate that plant cell walls are determinants of immune responses since modification of their composition in a set of Arabidopsis cell wall mutants has an impact on their disease resistance and fitness phenotypes. In these genotypes, we identified specific correlations between the amounts of specific wall carbohydrate epitopes and disease resistance/fitness phenotypes through mathematical analyses. We identified specific correlations between the amounts of specific wall carbohydrate epitopes and disease resistance/fitness phenotypes through mathematical analyses These data support the relevant and specific function of plant cell wall composition in plant immune responses and provide the basis for using wall traits in crop breeding programs. Notwithstanding the evidence of the roles of plant cell walls in immunity and fitness, correlations between variations in cell wall carbohydrate moiety composition and specific phenotypes have not been described until recently [12, 41, 54]
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