Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors

Abstract

Plants and animals deploy intracellular immune receptors that perceive specific pathogen effector proteins and microbial products delivered into the host cell. We demonstrate that the ADR1 family of Arabidopsis nucleotide-binding leucine-rich repeat (NB-LRR) receptors regulates accumulation of the defense hormone salicylic acid during three different types of immune response: (i) ADRs are required as "helper NB-LRRs" to transduce signals downstream of specific NB-LRR receptor activation during effector-triggered immunity; (ii) ADRs are required for basal defense against virulent pathogens; and (iii) ADRs regulate microbial-associated molecular pattern-dependent salicylic acid accumulation induced by infection with a disarmed pathogen. Remarkably, these functions do not require an intact P-loop motif for at least one ADR1 family member. Our results suggest that some NB-LRR proteins can serve additional functions beyond canonical, P-loop-dependent activation by specific virulence effectors, extending analogies between intracellular innate immune receptor function from plants and animals.nucleotide-binding domain and leucine-rich repeat-containing protein receptors | plant immune system | effector-triggered immunity | microbial-associated molecular pattern-triggered immunity P lants respond to attempted microbial infection with a twotiered immune system. In the first tier, extracellular pattern recognition receptors (PRRs) bind conserved microbial-associated molecular pattern (MAMP) ligands, activating a complex host response that results in MAMP-triggered immunity (MTI). Successful pathogens deploy suites of virulence effectors that delay or suppress MTI, allowing infection. In the second tier, plant intracellular immune receptors of the nucleotide-binding leucinerich repeat (NB-LRR) protein family can be activated either by direct binding of effectors or, alternatively, by effector action on an associated target protein that generates a "modified-self" molecule (1, 2). Effector-mediated NB-LRR activation results in effectortriggered immunity (ETI), a rapid and high-amplitude output significantly overlapping with MTI (1). ETI is typically accompanied by the hypersensitive cell death response (HR), limited to the site of pathogen attack. Both MTI and some cases of NB-LRRmediated ETI require the salicylic acid (SA)-signaling molecule as a downstream mediator of transcriptional output responses (3, 4).Plant NB-LRR proteins belong to the STAND (signal transduction ATPases with numerous domains) superfamily, which includes the animal apoptotic proteins Apaf-1/CED4 and innate immune receptors of the nucleotide-binding domain and leucinerich repeat-containing proteins (NLR) family (5). Animal NLRs are activated by MAMPs and by modified-self molecules in the form of danger-associated molecular patterns (6) and regulate inflammasome activation, autophagy, and cell death (7). STAND protein functions require an intact P-loop motif (GxxxxGKT/S) that coordinates ATP binding. STAND proteins are molecular switches that toggle fr...

Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4

“…6c). To generate RPS4B (D3829)RLD , a nucleotide deletion was performed at 3,829 bp in RPS4B RLD using the QuickChange II XL Site-Directed mutagenesis kit (Agilent 20,000 g at 4°C and aliquots of filtered supernatants were used as input samples. Immunoprecipitations were conducted on 1.5 ml of filtered extract incubated for 2 h at 4°C under gentle agitation in the presence of 20 ml anti-FLAG M2 affinity Gel (A2220 Sigma-Aldrich) or GFP-Trap_A (gtm-20 ChromoTek).…”

“…19), and multiple genes of the ADR1 class are required for function of RPS2, RPP4 and RPP2 (ref. 20).…”

The wheat NB‐LRR gene TaRCR1 is required for host defence response to the necrotrophic fungal pathogen Rhizoctonia cerealis

“…Several dozens of NB‐LRR genes, acting as intracellular immune receptors to effectors of bacterial, viral and fungal pathogens, have been cloned from diverse plant species (Anderson et al ., 1997; Cloutier et al ., 2007; Deslandes et al ., 1998; Ellis et al ., 1999; Feuillet et al ., 2003; Hinsch and Staskawicz, 1996; Huang et al ., 2003, 2004; Inoue et al ., 2013; Periyannan et al ., 2013; Saintenac et al ., 2013; Shen et al ., 2007; Whitham et al ., 1994). Recently, an emerging model is that NB‐LRR proteins often function in pairs, with ‘helper’ proteins required for the activity of ‘sensors’ that mediate pathogen recognition (Bonardi et al ., 2011; Wu et al ., 2016). Certain NB‐LRR proteins contribute to signal transduction and/or amplification (Bonardi et al ., 2011; Césari et al ., 2014; Gabriëls et al ., 2007).…”

“…Recently, an emerging model is that NB‐LRR proteins often function in pairs, with ‘helper’ proteins required for the activity of ‘sensors’ that mediate pathogen recognition (Bonardi et al ., 2011; Wu et al ., 2016). Certain NB‐LRR proteins contribute to signal transduction and/or amplification (Bonardi et al ., 2011; Césari et al ., 2014; Gabriëls et al ., 2007). The above‐mentioned NB‐LRRs play a pivotal role in plant resistance responses to biotrophic pathogens.…”

Tracking ancestral lineages and recent expansions of NBS-LRR genes in angiosperms

“…5,7,12 This group of RPW8-NBS-LRR (RNL) genes has not been found to be involved in detecting specific pathogens as most known TNL or CNL type R genes, but functions in signal transductions of disease resistances. 12,13 A controversy was then raised by comparing independent phylogenetic analysis, referring to whether RNL genes are derived from a CNL lineage recently or represent another ancient NBS-LRR class that sister to CNL and TNL genes. 2,5,7 To clarify this basic concept for NBS-LRR gene classification, our recent study 6 performed large-scale phylogenetic analysis of NBS-LRR genes from 22 genomes across major angiosperm lineages.…”