Arabidopsis Heterotrimeric G-protein Regulates Cell Wall Defense and Resistance to Necrotrophic Fungi

Abstract

The Arabidopsis heterotrimeric G-protein controls defense responses to necrotrophic and vascular fungi. The agb1 mutant impaired in the Gβ subunit displays enhanced susceptibility to these pathogens. Gβ/AGB1 forms an obligate dimer with either one of the Arabidopsis Gγ subunits (γ1/AGG1 and γ2/AGG2). Accordingly, we now demonstrate that the agg1 agg2 double mutant is as susceptible as agb1 plants to the necrotrophic fungus Plectosphaerella cucumerina. To elucidate the molecular basis of heterotrimeric G-protein-mediated resistance, we performed a comparative transcriptomic analysis of agb1-1 mutant and wild-type plants upon inoculation with P. cucumerina. This analysis, together with metabolomic studies, demonstrated that G-protein-mediated resistance was independent of defensive pathways required for resistance to necrotrophic fungi, such as the salicylic acid, jasmonic acid, ethylene, abscisic acid, and tryptophan-derived metabolites signaling, as these pathways were not impaired in agb1 and agg1 agg2 mutants. Notably, many mis-regulated genes in agb1 plants were related with cell wall functions, which was also the case in agg1 agg2 mutant. Biochemical analyses and Fourier Transform InfraRed (FTIR) spectroscopy of cell walls from G-protein mutants revealed that the xylose content was lower in agb1 and agg1 agg2 mutants than in wild-type plants, and that mutant walls had similar FTIR spectratypes, which differed from that of wild-type plants. The data presented here suggest a canonical functionality of the Gβ and Gγ1/γ2 subunits in the control of Arabidopsis immune responses and the regulation of cell wall composition.

On plant defense signaling networks and early land plant evolution

“…[77],); the role of β- and γ-subunits in defense is also implicated to be mediated by FLS2, EF-Tu and CERK1 in A. thaliana [78]. Homologs of all three subunits are present in land plants and streptophyte algae [79,80].…”

Dissecting Arabidopsis Gβ Signal Transduction on the Protein Surface

“…The enhanced susceptibility of agb1 mutants to F. oxysporum may result from the altered function of MYC2, a basic helix-loop-helix transcription factor regulating diverse jasmonate-dependent biological processes (Trusov et al, 2009). More recent data also suggest a link between AGB1-mediated P. cucumerina resistance and the modification of cell wall architecture (Delgado-Cerezo et al, 2012). Another important agricultural trait regulated by the heterotrimeric G protein is transpiration efficiency, which is increased in gpa1 mutants (Nilson and Assmann, 2010).…”

“…The Arabidopsis agb1 null mutant shows reduced accumulation of reactive oxygen species (ROS) in response to microbial inducers such as bacterial flagellin and EF-Tu (Ishikawa, 2009). Moreover, agb1 null mutants are hypersensitive to the necrotrophic fungi Plectosphaerella cucumerina and Alternaria brassicicola and the hemibiotrophic fungus Fusarium oxysporum (Llorente et al, 2005;Trusov et al, 2006Trusov et al, , 2009Delgado-Cerezo et al, 2012). Moreover, rice Ga mutants (rga1) are more susceptible to the rice blast fungus Magnaporthe grisea (Suharsono et al, 2002).…”

Heterotrimeric G Proteins Serve as a Converging Point in Plant Defense Signaling Activated by Multiple Receptor-Like Kinases

“…Analysis of rice dwarf1 mutants with defects in the Ga subunit indicates that the rice Ga subunit plays an important role in resistance against rice blast (Suharsono et al, 2002). In Arabidopsis, loss of function of the Gb or Gg subunits leads to compromised resistance against the necrotrophic pathogen Plectosphaerella cucumerina (Llorente et al, 2005;Delgado-Cerezo et al, 2012). By contrast, loss of function of the Ga subunit GPA1 results in enhanced resistance against the pathogen (Llorente et al, 2005).…”