Arabidopsis Response Regulator 6 (ARR6) Modulates Plant Cell-Wall Composition and Disease Resistance

Abstract

The cytokinin signaling pathway, which is mediated by Arabidopsis response regulator (ARR) proteins, has been involved in the modulation of some disease-resistance responses. Here, we describe novel functions of ARR6 in the control of plant disease-resistance and cell-wall composition. Plants impaired in ARR6 function (arr6) were more resistant and susceptible, respectively, to the necrotrophic fungus Plectosphaerella cucumerina and to the vascular bacterium Ralstonia solanacearum, whereas Arabidopsis plants that overexpress ARR6 showed the opposite phenotypes, which further support a role of ARR6 in the modulation of disease-resistance responses against these pathogens. Transcriptomics and metabolomics analyses revealed that, in arr6 plants, canonical disease-resistance pathways, like those activated by defensive phytohormones, were not altered, whereas immune responses triggered by microbe-associated molecular patterns were slightly enhanced. Cell-wall composition of arr6 plants was found to be severely altered compared with that of wild-type plants. Remarkably, pectin-enriched cell-wall fractions extracted from arr6 walls triggered more intense immune responses than those activated by similar wall fractions from wild-type plants, suggesting that arr6 pectin fraction is enriched in wall-related damage-associated molecular patterns, which trigger immune responses. This work supports a novel function of ARR6 in the control of cell-wall composition and disease resistance and reinforces the role of the plant cell wall in the modulation of specific immune responses.

Arabidopsiscell wall composition determines disease resistance specificity and fitness

“…1A). These data support the diverse and significant functions of cell walls on plant disease resistance responses to vascular and necrotrophic pathogens, as previously described (20,29,54). Our data also identified an unanticipated contribution of cell walls to plant resistance to biotrophic oomycetes, like H. arabidopsidis (Fig.…”

“…Similar immune responses triggered by elicitor activities have been described in wall extracts of additional Arabidopsis wall mutants (12,44). We found that the PEC1 and PEC2 wall extracts from cwm plants, and particularly PEC1 from at1g23170-1, acs8-2, namt1-1, arr6-3 and irx10-1, triggered early immune responses, like Ca +2 bursts, upon their application to Arabidopsis pMAQ lines expressing the apoaequorin Ca +2 sensor protein (20,47; SI Appendix, Fig. S12).…”

“…We have recently shown that pectin wall fractions of Col-0 and arr6-3 plants contain potential glycanderived DAMPs that regulate immune responses when applied to Col-0 plants (20). Similar immune responses triggered by elicitor activities have been described in wall extracts of additional Arabidopsis wall mutants (12,44).…”

“…S1; 22). We evaluated the resistance phenotypes of these 38 (20,29,31,39). We found that 31 of the 38 cwm lines tested (81.6%) showed, in comparison to wild-type plants, altered resistance responses (mainly enhanced resistance) to at least one of these pathogens: 22 of 38 mutants to Pc and Ha (57,9%) and 16 of 38 mutants to Rp (42.1%; Fig.…”

“…isoxaben). These wall modifications have a direct effect on cell wall integrity (CWI) and can initiate molecular adaptive mechanisms like cell wall composition remodeling and defensive responses activation (12,(18)(19)(20)(21). CWI alteration also occurs in plants impaired in or overexpressing cell wall-related genes.…”