Differential regulation of TNL‐mediated immune signaling by redundant helper CNLs

Abstract

Summary Higher plants utilize nucleotide‐binding leucine‐rich repeat domain proteins (NLRs) as intracellular immune receptors to recognize pathogen‐derived effectors and trigger a robust defense. The Activated Disease Resistance 1 (ADR1) family of coiled‐coil NLRs (CNLs) have evolved as helper NLRs that function downstream of many TIR‐type sensor NLRs (TNLs). Close homologs of ADR1s form the N REQUIREMENT GENE 1 (NRG1) family in Arabidopsis, the function of which is unclear. Through CRISPR/Cas9 gene editing methods, we discovered that the tandemly repeated NRG1A and NRG1B are functionally redundant and operate downstream of TNLs with differential strengths. Interestingly, ADR1s and NRG1s function in two distinct parallel pathways contributing to TNL‐specific immunity. Synergistic effects on basal and TNL‐mediated defense were detected among ADR1s and NRG1s. An intact P‐loop of NRG1s is not required for mediating signals from sensor TNLs, whereas auto‐active NRG1A exhibits autoimmunity. Importantly, NRG1s localize to the cytosol and endomembrane network regardless of the presence of effectors, suggesting a cytosolic activation mechanism. Taken together, different sensor TNLs differentially use two groups of helper NLRs, ADR1s and NRG1s, to transduce downstream defense signals.

Diverse NLR immune receptors activate defence via the RPW8‐NLR NRG1

“…However, the requirement of NRG1 by RPP1, RPP2 and RPP4 for downy mildew resistance, although significant, is weak. In addition, RPP4 function was not affected in an independent experiment (Wu et al ., ). Thus, other helpers, such as ADR1 family proteins, already reported to contribute to RPP4 function (Bonardi et al ., ), also probably contribute to RPP1, RPP2 and RPP4 function.…”

“…Here, we found that CHS3‐induced HR requires NbNRG1 . Moreover, the chs3‐2D autoimmune phenotype is completely lost in an nrg1a‐nrg1b‐nrg1c mutant of Arabidopsis (Wu et al ., ). Thus, CHS3 signals only via NRG1s.…”

An EDS1-SAG101 complex functions in TNL-mediated immunity in Solanaceae

“…In Arabidopsis, there are three ADR1 homologs (ADR1-L1, -L2, -L3) and two NRG1 homologs (NRG1.1, NRG1.2) (Bonardi et al, 2011;Collier et al, 2011). Indeed, NRG1 homologs were recently reported to function redundantly in TNL-mediated immunity in Arabidopsis, and also ADR1s are required for several TNL-mediated immune responses (Dong et al, 2016;Castel et al, 2018;Wu et al, 2018). Helper CNLs of the NRG1 class are critical for function of most TNLs, but others require ADR1 class helpers or can signal via both pathways (Castel et al, 2018;Wu et al, 2018).…”

“…Indeed, NRG1 homologs were recently reported to function redundantly in TNL-mediated immunity in Arabidopsis, and also ADR1s are required for several TNL-mediated immune responses (Dong et al, 2016;Castel et al, 2018;Wu et al, 2018). Helper CNLs of the NRG1 class are critical for function of most TNLs, but others require ADR1 class helpers or can signal via both pathways (Castel et al, 2018;Wu et al, 2018). While genetic redundancy explains failure to isolate respective mutant alleles by forward genetics, a physical association of NRG1 proteins with EDS1 as reported by Qi et al (2018) will require further analysis.…”

An rpw8 quadruple mutant of Arabidopsis Col-0 is partially compromised in bacterial and fungal resistance

“…This sub-family of NLRs often have only a few members but exists in almost all plants (Zhong & Cheng, 2016). At least in angiosperms, these RPW8-NLRs are helper NLRs required for signalling of multiple sensor NLRs (Peart et al, 2005;Bonardi et al, 2011;Dong et al, 2016;Qi et al, 2018;Adachi et al, 2019;Castel et al, 2019a;Wu et al, 2019).…”