The N-end rule pathway regulates pathogen responses in plants

Marchi, Rémi de; Sorel, Maud; Mooney, Brian; Fudal, Isabelle; Goslin, Kevin; Kwaśniewska, Kamila; Ryan, Patrick T.; Pfalz, Marina; Kroymann, Juergen; Pollmann, Stephan; Feechan, Angela; Wellmer, Frank; Rivas, Susana; Graciet, Emmanuelle

doi:10.1038/srep26020

Cited by 40 publications

(66 citation statements)

References 67 publications

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“…In this paper, we report the effects of loss of PRT1 function on the immune system. A previous report showed that the prt1 mutant was more susceptible to the hemi‐biotroph bacterium Pseudomonas syringae pv tomato in short‐day plants (de Marchi et al, ); however, using an assembly of different approaches, we show that removal of the activity of the PRT1 E3 ligase enhances resistance of arabidopsis to this pathogen, and that this is associated with constitutive alteration of the proteome including the enhanced accumulation of many pathogenesis‐associated proteins. In addition, we show an altered metabolome profile in the mutant including SA, camalexin, and, together with prt6 mutant, Pip.…”

Section: Introductioncontrasting

confidence: 59%

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

et al. 2019

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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.

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Section: Introductioncontrasting

confidence: 59%

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

et al. 2019

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“…Another upregulated protein, GSTF7 was hypothesized to play a role in camalexin synthesis based on its induction in the constitutively active MKK9 mutant (Su et al ., ). Our analysis of previously published transcriptome data (de Marchi et al ., ) comparing gene expression in ate1 ate2 with WT, and comparing gene expression during Pst infection in Col‐0 and ate1 ate2 also showed increased expression of RNAs encoding camalexin synthesis genes (Tables S3, S4). Analysis of transcript expression indicated greater accumulation for most genes of camalexin synthesis in mature uninfected leaves of ntaq1 and prt6 compared to WT (Figs , S7), including PAD3 (CYP71B15), that catalyzes the final two steps of camalexin synthesis.…”

Section: Resultsmentioning

confidence: 99%

“…These results are opposite to those obtained by de Marchi et al . (), who found enhanced sensitivity to Pst DC3000 of N‐end rule mutants prt6 and ate1 ate2 (which removes ATE Nt‐arginylation activity, Fig. a).…”

Section: Resultsmentioning

confidence: 99%

“…In our experiments, there were no differences in responses of WT and prt6 to B. cinerea suggesting that independently of other mechanisms activated, an increase in camalexin in prt6 may not reach a level necessary for reduction in fungal growth. A recent report showed N‐end rule mutants, including alleles of prt6 , ate1 ate2 and ntaq1 to be in general equal or more sensitive than WT Arabidopsis to a wide range of bacterial and fungal pathogens with diverse infection strategies and lifestyles (de Marchi et al ., ). Our results, in which plants were grown under either neutral days or under the short‐day condition used by de Marchi et al .…”

Section: Discussionmentioning

confidence: 99%

“…Induction of components of the hypoxia response, controlled by Group VII ETHYLENE RESPONSE FACTOR (ERFVII) transcription factor substrates (ERFVIIs), enhanced clubroot development, indicating that the protist hijacks the N‐end rule ERFVII regulation system to enhance infection. In another study, inactivation of different components of the Arg/N‐end rule pathway was shown to result in greater susceptibility of Arabidopsis to necrotrophic pathogens and altered timing and amplitude of response to the hemibiotroph Pseudomonas syringae pathovar tomato ( Pst ) AvrRpm1 (de Marchi et al ., ). A correlation between Nt‐Acetylation and the stability of a Nod‐like receptor, Suppressor of NPR1, Constitutive 1 (SNC1) was also reported (Xu et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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Distinct branches of the N‐end rule pathway modulate the plant immune response

et al. 2018

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The N-end rule pathway is a highly conserved constituent of the ubiquitin proteasome system, yet little is known about its biological roles. Here we explored the role of the N-end rule pathway in the plant immune response. We investigated the genetic influences of components of the pathway and known protein substrates on physiological, biochemical and metabolic responses to pathogen infection. We show that the glutamine (Gln) deamidation and cysteine (Cys) oxidation branches are both components of the plant immune system, through the E3 ligase PROTEOLYSIS (PRT)6. In Arabidopsis thaliana Gln-specific amino-terminal (Nt)-amidase (NTAQ1) controls the expression of specific defence-response genes, activates the synthesis pathway for the phytoalexin camalexin and influences basal resistance to the hemibiotroph pathogen Pseudomonas syringae pv tomato (Pst). The Nt-Cys ETHYLENE RESPONSE FACTOR VII transcription factor substrates enhance pathogen-induced stomatal closure. Transgenic barley with reduced HvPRT6 expression showed enhanced resistance to Ps. japonica and Blumeria graminis f. sp. hordei, indicating a conserved role of the pathway. We propose that that separate branches of the N-end rule pathway act as distinct components of the plant immune response in flowering plants.

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A simple and efficient Agrobacterium‐mediated transient expression system to dissect molecular processes in Brassica rapa and Brassica napus

Mooney

Graciet

2020

Plant Direct

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The family Brassicaceae is a source of important crop species, including Brassica napus (oilseed rape), Brassica oleracea , and B. rapa , that is used globally for oil production or as a food source ( e.g., pak choi or turnip). However, despite advances in recent years, including genome sequencing, a lack of established tools tailored to the study of Brassica crop species has impeded efforts to understand their molecular processes in greater detail. Here, we describe the use of a simple Agrobacterium ‐mediated transient expression system adapted to B. rapa and B. napus that could facilitate study of molecular and biochemical events in these species. We also demonstrate the use of this method to characterize the N‐degron pathway of protein degradation in B. rapa . The N‐degron pathway is a subset of the ubiquitin‐proteasome system and represents a mechanism through which proteins may be targeted for degradation based on the identity of their N‐terminal amino acid residue. Interestingly, N‐degron‐mediated processes in plants have been implicated in the regulation of traits with potential agronomic importance, including the responses to pathogens and to abiotic stresses such as flooding tolerance. The stability of transiently expressed N‐degron reporter proteins in B. rapa indicates that its N‐degron pathway is highly conserved with that of Arabidopsis thaliana . These findings highlight the utility of Agrobacterium ‐mediated transient expression in B. rapa and B. napus and establish a framework to investigate the N‐degron pathway and its roles in regulating agronomical traits in these species. Significance statement We describe an Agrobacterium‐ mediated transient expression system applicable to Brassica crops and demonstrate its utility by identifying the destabilizing residues of the N‐degron pathway in B. rapa . As the N‐degron pathway functions as an integrator of environmental signals, this study could facilitate efforts to improve the robustness of Brassica crops.

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The N-end rule pathway regulates pathogen responses in plants

Cited by 40 publications

References 67 publications

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

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

Distinct branches of the N‐end rule pathway modulate the plant immune response

A simple and efficient Agrobacterium‐mediated transient expression system to dissect molecular processes in Brassica rapa and Brassica napus

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