Arabidopsis Clade I TGA Factors Regulate Apoplastic Defences against the Bacterial Pathogen Pseudomonas syringae through Endoplasmic Reticulum-Based Processes

Abstract

During the plant immune response, large-scale transcriptional reprogramming is modulated by numerous transcription (co) factors. The Arabidopsis basic leucine zipper transcription factors TGA1 and TGA4, which comprise the clade I TGA factors, have been shown to positively contribute to disease resistance against virulent strains of the bacterial pathogen Pseudomonas syringae. Despite physically interacting with the key immune regulator, NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1), following elicitation with salicylic acid (SA), clade I function was shown to be largely independent of NPR1. Unlike mutants in NPR1, tga1-1 tga4-1 plants do not display reductions in steady-state levels of SA-pathway marker genes following treatment with this phenolic signaling metabolite or after challenge with virulent or avirulent P. syringae. By exploiting bacterial strains that have limited capacity to suppress Arabidopsis defence responses, the present study demonstrates that tga1-1 tga4-1 plants are compromised in basal resistance and defective in several apoplastic defence responses, including the oxidative burst of reactive oxygen species, callose deposition, as well as total and apoplastic PATHOGENESIS-RELATED 1 (PR-1) protein accumulation. Furthermore, analysis of npr1-1 and the tga1-1 tga4-1 npr1-1 triple mutant indicates that clade I TGA factors act substantially independent of NPR1 in mediating disease resistance against these strains of P. syringae. Increased sensitivity to the N-glycosylation inhibitor tunicamycin and elevated levels of endoplasmic reticulum (ER) stress marker genes encoding ER-resident chaperones in mutant seedlings suggest that loss of apoplastic defence responses is associated with aberrant protein secretion and implicate clade I TGA factors as positive regulators of one or more ER-related secretion pathways.

The Potyviral P3 Protein Targets Eukaryotic Elongation Factor 1A to Promote the Unfolded Protein Response and Viral Pathogenesis

“…Reduced expression of BiP in GmEF1A knockdown plants likely enhanced susceptibility to Psg because BiP negatively regulates ER stress. It is possible that Psginduced ER stress is dependent on pathogen-encoded effectors that are directed to the ER (Wang and Fobert, 2013). Indeed, at least one P. syringae effector (HopD1) is known to localize to the ER (Block et al, 2014).…”

Clade I TGACG-Motif Binding Basic Leucine Zipper Transcription Factors Mediate BLADE-ON-PETIOLE-Dependent Regulation of Development

“…9A). The activity of fusion proteins was further monitored by complementation of tga1 tga4 sensitivity to tunicamycin-induced endoplasmic reticulum stress (Wang and Fobert, 2013). Two TGA1pro:TGA1-GFP tga1 tga4 and TGA4pro:TGA4-GFP tga1 tga4 lines showing complementation of this defect were used for ChIP assays (Fig.…”

“…Asterisk, significant difference between DEX-treated wild-type and tga1 tga4 background plants (Student's t test, *P , 0.01). (Després et al, 2003;Kesarwani et al, 2007;Wang and Fobert, 2013;Sun et al, 2018). Clade I TGAs are required for the full induction of SYSTEMIC ACQUIRED RESISTANCE1 (SARD1) and CALMODULIN-BINDING PROTEIN 60g (CBP60g) genes needed for biosynthesis of SA and pipecolic acid during both types of immune response .…”

“…This interaction also occurs in SA-treated leaves but is not critical for SAR (Després et al, 2003;Kesarwani et al, 2007). Clade I TGAs function primarily in innate immunity based on transcriptome studies and backed by phenotypic data (Kesarwani et al, 2007;Shearer et al, 2012;Wang and Fobert, 2013;Sun et al, 2018). Interestingly, redox mimic mutations that promote NPR1 interaction with TGA1 and TGA4 (Després et al, 2003) reduce the interaction with BOP1 and BOP2 in yeast cells.…”

Arabidopsis UBC13 differentially regulates two programmed cell death pathways in responses to pathogen and low‐temperature stress

“…In planta bacterial growth assays were as described previously (Wang & Fobert, 2013). Briefly, Pseudomonas syringae pv.…”