The Arabidopsis thaliana N‐recognin E3 ligase PROTEOLYSIS1 influences the immune response

Abstract

N‐degron pathways of ubiquitin‐mediated proteolysis (formerly known as the N‐end rule pathway) control the stability of substrate proteins dependent on the amino‐terminal (Nt) residue. Unlike yeast or mammalian N‐recognin E3 ligases, which each recognize several different classes of Nt residues, in Arabidopsis thaliana, N‐recognin functions of different N‐degron pathways are carried out independently by PROTEOLYSIS (PRT)1, PRT6, and other unknown proteins. PRT1 recognizes type 2 aromatic Nt‐destabilizing residues and PRT6 recognizes type 1 basic residues. These two N‐recognin functions diverged as separate proteins early in the evolution of plants, before the conquest of the land. We demonstrate that loss of PRT1 function promotes the plant immune system, as mutant prt1‐1 plants showed greater apoplastic resistance than WT to infection by the bacterial hemi‐biotroph Pseudomonas syringae pv tomato (Pst) DC3000. Quantitative proteomics revealed increased accumulation of proteins associated with specific components of plant defense in the prt1‐1 mutant, concomitant with increased accumulation of salicylic acid. The effects of the prt1 mutation were additional to known effects of prt6 in influencing the immune system, in particular, an observed over‐accumulation of pipecolic acid (Pip) in the double‐mutant prt1‐1 prt6‐1. These results demonstrate a potential role for PRT1 in controlling aspects of the plant immune system and suggest that PRT1 limits the onset of the defense response via degradation of substrates with type 2 Nt‐destabilizing residues.

Identification of nitric oxide (NO)-responsive genes under hypoxia in tomato (Solanum lycopersicum L.) root

“…In a recent study in Arabidopsis, it was demonstrated that loss of function of PRT1, involved in N-degron pathways of ubiquitin-mediated proteolysis, improves the plant immune system. DMR6 and DLO1 proteins were accumulated in the former study indicating their importance in regulating the basal defense system 77 .…”

The ubiquitin system affects agronomic plant traits

“…Plants with a prt6 loss-of-function allele exhibit increased resistance to bacterial pathogens in both barley and Arabidopsis (109). Similarly, a prt1 loss-offunction allele shows enhanced bacterial resistance in Arabidopsis (110). Loss of either E3 results in a constitutive increase in defense proteins, creation of a "primed" defense state normally only observed in wild-type leaves after infection of other leaves, and increased synthesis of other defense metabolites (110,109).…”

“…Similarly, a prt1 loss-offunction allele shows enhanced bacterial resistance in Arabidopsis (110). Loss of either E3 results in a constitutive increase in defense proteins, creation of a "primed" defense state normally only observed in wild-type leaves after infection of other leaves, and increased synthesis of other defense metabolites (110,109). PRT6 modulates the stability of a family of transcription factors that regulate the hypoxic responses to pathogens that induce undifferentiated cell growth, such as cysts or galls (111).…”

Nitric oxide function during oxygen deprivation in physiological and stress processes

“…ERFVII group was the first substrate of the PCO branch of the PRT6 N-degron pathway described in plants ( Gibbs et al , 2011 ; Licausi et al , 2011 ) followed by the transcriptional regulators polycomb repressive complex 2 subunit VERNALIZATION 2 (VRN2) ( Gibbs et al , 2018 ) and LITTLE ZIPPER 2 (ZPR2) ( Weits et al , 2019 ). N-degron pathway substrates regulate important aspects of plant development such as seed storage mobilization ( Zhang et al ., 2018 a , b ), germination ( Holman et al , 2009 ; Gibbs et al , 2014 ), photomorphogenesis ( Abbas et al , 2015 ), stomatal closure ( Gibbs et al , 2014 ), shoot and leaf development ( Graciet et al , 2009 ), root architecture ( Shukla et al , 2019 ), SAM function ( Weits et al , 2019 ), vernalization ( Gibbs et al , 2018 ; Labandera et al , 2020 ), flowering ( Vicente et al , 2017 ), or leaf senescence ( Yoshida et al , 2002 ), and also regulates stress responses such as flooding ( Hartman et al , 2019 ) or pathogen attack ( de Marchi et al , 2016 ; Vicente et al , 2019 ; Till et al , 2019 ).…”