Abstract
BackgroundNonhost resistance is a generalized, durable, broad-spectrum resistance exhibited by plant species to a wide variety of microbial pathogens. Although nonhost resistance is an attractive breeding strategy, the molecular basis of this form of resistance remains unclear for many plant-microbe pathosystems, including interactions with the bacterial pathogen of rice, Xanthomonas oryzae pv. oryzae (Xoo).Methods and FindingsVirus-induced gene silencing (VIGS) and an assay to detect the hypersensitive response (HR) were used to screen for genes required for nonhost resistance to Xoo in N. benthamiana. When infiltrated with Xoo strain YN-1, N. benthamiana plants exhibited a strong necrosis within 24 h and produced a large amount of H2O2 in the infiltrated area. Expression of HR- and defense-related genes was induced, whereas bacterial numbers dramatically decreased during necrosis. VIGS of 45 ACE (Avr/Cf-elicited) genes revealed identified seven genes required for nonhost resistance to Xoo in N. benthamiana. The seven genes encoded a calreticulin protein (ACE35), an ERF transcriptional factor (ACE43), a novel Solanaceous protein (ACE80), a hydrolase (ACE117), a peroxidase (ACE175) and two proteins with unknown function (ACE95 and ACE112). The results indicate that oxidative burst and calcium-dependent signaling pathways play an important role in nonhost resistance to Xoo. VIGS analysis further revealed that ACE35, ACE80, ACE95 and ACE175, but not the other three ACE genes, interfered with the Cf-4/Avr4-dependent HR.Conclusions/Significance N. benthamiana plants inoculated with Xoo respond by rapidly eliciting an HR and nonhost resistance. The oxidative burst and other signaling pathways are pivotal in Xoo-N. benthamiana nonhost resistance, and genes involved in this response partially overlap with those involved in Cf/Avr4-dependent HR. The seven genes required for N. benthamiana-mediated resistance to Xoo provide a basis for further dissecting the molecular mechanism of nonhost resistance.
Highlights
It is a general phenomenon that microbial pathogens can successfully infect only a limited number of plant species
Xanthomonas oryzae pv. oryzae (Xoo) is considered a non-adaptive pathogen with respect to N. benthamiana; its ability to induce an hypersensitive response (HR) in this plant species is strain-dependent [29]
Results showed that silencing of ACE35, ACE80, ACE95 and ACE175, but not ACE43, ACE112 and ACE117, compromised Cf-4/Avr4-dependent HR, and led to either complete suppression of the HR or a partial HR in 70% of the silenced plants (Table 3; Figure 5B). These results demonstrated that ACE35, ACE80, ACE95 and ACE175 were required for the HR in both the Xoo/N. benthaminana and Cf-4/Avr4 interactions, indicating that the regulatory pathways for the HR in both interactions partially overlapped
Summary
It is a general phenomenon that microbial pathogens can successfully infect only a limited number of plant species. When non-adapted pathogens attempt to colonize plant species outside of the normal host range, nonhost disease resistance is triggered. Nonhost resistance is durable and broad-spectrum, which makes it highly desirable for mediating resistance to plant diseases [1]. It is apparent that nonhost resistance to non-adapted pathogens includes defense mechanisms similar to those utilized for adapted pathogens, including pathogen-associated molecular pattern (PAMP)- and effector-triggered immunity (PTI and ETI, respectively) [8,9,10]. Nonhost resistance is a generalized, durable, broad-spectrum resistance exhibited by plant species to a wide variety of microbial pathogens. Nonhost resistance is an attractive breeding strategy, the molecular basis of this form of resistance remains unclear for many plant-microbe pathosystems, including interactions with the bacterial pathogen of rice, Xanthomonas oryzae pv. Nonhost resistance is an attractive breeding strategy, the molecular basis of this form of resistance remains unclear for many plant-microbe pathosystems, including interactions with the bacterial pathogen of rice, Xanthomonas oryzae pv. oryzae (Xoo)
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