RPS5-Mediated Disease Resistance: Fundamental Insights and Translational Applications

Abstract

Focusing on the discovery and characterization of the Arabidopsis disease resistance protein RPS5 and its guardee PBS1, this review discusses work done in the Innes laboratory from the initial identification of the RPS5 gene in 1995 to the recent deployment of the PBS1 decoy system in crops. This is done through discussion of the structure, function, and signaling environment of RPS5 and PBS1, highlighting collaborations and influential ideas along the way. RPS5, a nucleotide-binding leucine-rich repeat (NLR) protein, is activated by the proteolytic cleavage of PBS1. We have shown that the cleavage site within PBS1 can be altered to contain cleavage sites for other proteases, enabling RPS5 activation by these proteases, thereby conferring resistance to different pathogens. This decoy approach has since been translated into crop species using endogenous PBS1 orthologs and holds strong potential for GMO-free development of new genetic resistance against important crop pathogens. Expected final online publication date for the Annual Review of Phytopathology, Volume 58 is August 25, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

An atypical class of non-coding small RNAs produced in rice leaves upon bacterial infection

“…Still on Figure 4A, in the BIK1/PBL1 (13) clade, OsRLCK107, OsRLCK118 and OsRLCK176 have been previously shown to contribute to PTI or resistance to Xoo downstream of the OsCERK1, SDS2 or Xa21 receptors (48–50) and their transcript has a xisRNA duplex. Second, Figure 4B indicates that RLCK-VIIa proteins encoded by the loci overlapping with xisRNA007 (OsRLCK28) and xisRNA044 (OsRLCK55) closely cluster with the Arabidopsis decoy PBS1 (51). A Xoo type III effector interact with OsRLCK55 and OsRLCK185 (also in this clade) and OsRLCK185 acts as an essential phosphorelay of its binding partner OsCERK1 in mediating chitin- and peptidoglycan-induced rice immunity signaling (52).…”

Precision Breeding Made Real with CRISPR: Illustration through Genetic Resistance to Pathogens

“…Transforming RPS5 plants with a PBS1 mutant carrying the cleavage sites of other bacterial or viral proteases resulted in the recognition of these proteases and novel bacterial or virus resistance ( Kim et al., 2016 ) ( Figure 6 A). Using genome-editing tools, such as CRISPR-mediated GT or prime editing, the endogenous locus encoding the seven-residue cleavage site of PBS1 could be readily modified into the cleavage sites of other pathogen proteases ( Figure 6 B), resulting in RPS5-mediated surveillance of these novel effectors ( Pottinger and Innes, 2020 ). PBS1 is highly conserved among flowering plants and NLR-mediated surveillance of its cleavage emerged repeatedly in evolution, making it a versatile decoy system in corresponding crops ( Carter et al., 2019 ; Pottinger and Innes, 2020 ).…”

“…Using genome-editing tools, such as CRISPR-mediated GT or prime editing, the endogenous locus encoding the seven-residue cleavage site of PBS1 could be readily modified into the cleavage sites of other pathogen proteases ( Figure 6 B), resulting in RPS5-mediated surveillance of these novel effectors ( Pottinger and Innes, 2020 ). PBS1 is highly conserved among flowering plants and NLR-mediated surveillance of its cleavage emerged repeatedly in evolution, making it a versatile decoy system in corresponding crops ( Carter et al., 2019 ; Pottinger and Innes, 2020 ). More generally, similar trap systems for proteases or other effectors can probably be engineered with other decoys or guardess in a large spectrum of crops even if they do not possess a PBS1 surveillance system ( Giannakopoulou et al., 2016 ; Kim et al., 2016 ; Pottinger et al., 2020 ).…”

Outcome of the public consultation on the draft Scientific Opinion on the evaluation of existing guidelines for their adequacy for the molecular characterisation and environmental risk assessment of genetically modified plants obtained through synthetic biology

“…-We propose to add another reference of interest for engineered resistance to biotic stress: the paper by Pottinger and Innes (2020), which describes the PBS1 decoy…”