NADPH-dependent thioredoxin reductase C plays a role in nonhost disease resistance against Pseudomonas syringae pathogens by regulating chloroplast-generated reactive oxygen species.

Yasuhiro Ishiga,Kirankumar S Mysore,Takako Ishiga,Takakazu Matsuura,Yoko Ikeda

doi:10.7717/peerj.1938

Yasuhiro Ishiga, Kirankumar S Mysore + Show 3 more

Open Access

https://doi.org/10.7717/peerj.1938

Copy DOI

Abstract

Chloroplasts are cytoplasmic organelles for photosynthesis in eukaryotic cells. In addition, recent studies have shown that chloroplasts have a critical role in plant innate immunity against invading pathogens. Hydrogen peroxide is a toxic by-product from photosynthesis, which also functions as a signaling compound in plant innate immunity. Therefore, it is important to regulate the level of hydrogen peroxide in response to pathogens. Chloroplasts maintain components of the redox detoxification system including enzymes such as 2-Cys peroxiredoxins (2-Cys Prxs), and NADPH-dependent thioredoxin reductase C (NTRC). However, the significance of 2-Cys Prxs and NTRC in the molecular basis of nonhost disease resistance is largely unknown. We evaluated the roles of Prxs and NTRC using knock-out mutants of Arabidopsis in response to nonhost Pseudomonas syringae pathogens. Plants lacking functional NTRC showed localized cell death (LCD) accompanied by the elevated accumulation of hydrogen peroxide in response to nonhost pathogens. Interestingly, the Arabidopsis ntrc mutant showed enhanced bacterial growth and disease susceptibility of nonhost pathogens. Furthermore, the expression profiles of the salicylic acid (SA) and jasmonic acid (JA)-mediated signaling pathways and phytohormone analyses including SA and JA revealed that the Arabidopsis ntrc mutant shows elevated JA-mediated signaling pathways in response to nonhost pathogen. These results suggest the critical role of NTRC in plant innate immunity against nonhost P. syringae pathogens.

Highlights

Plants are surrounded by a large number of microbes, including potential pathogens, in their natural habitat
We have previously shown that loss-of-function analysis of Prx and NADPHdependent thioredoxin reductase C (NTRC) resulted in accelerated Pseudomonas syringae pv. tomato DC3000 (Pto DC3000) disease-associated cell death with enhanced reactive oxygen species (ROS) accumulation in tomatoes and Arabidopsis (Ishiga et al, 2012)
These results indicate that pv. tabaci (Pta) 6605 involves the Type I nonhost resistance, whereas pv. glycinea (Pgl) race 4 and Pto T1 involve the Type II nonhost resistance in Arabidopsis

Summary

Introduction

Plants are surrounded by a large number of microbes, including potential pathogens, in their natural habitat. In addition to constitutive defenses, plants have developed multiple layers of advanced surveillance systems against invading pathogens to activate a wide array of inducible defense responses including rapid oxidative burst, callose (β-1,3-glucan) deposition in the cell wall, the induction of hormone-mediated signaling pathways leading to the expression of defense-related genes, and the production of antimicrobial compounds (Hok, Attard & Keller, 2010). To date, these surveillance systems are known to include two layers of plant immune responses against invading pathogens. In addition to apoplastic ROS, chloroplastderived ROS have been shown to function in LCD (Ishiga et al, 2009; Zurbriggen et al, 2009; Ishiga et al, 2012). Zurbriggen et al (2009) reported the requirement of chloroplastgenerated ROS for LCD, based on tobacco plants over-expressing a chloroplast-targeted cyanobacterial flavodoxin. Lim et al (2010) demonstrated that loss-of-function analysis of SlFTR-c (ferredoxin:thioredoxin reductase-c) resulted in spontaneous necrosis development associated with elevated accumulation of ROS without pathogen inoculation

Methods

Results

Conclusion