Potato NPH3/RPT2-Like Protein StNRL1, Targeted by a Phytophthora infestans RXLR Effector, Is a Susceptibility Factor

Abstract

Plant pathogens deliver effectors to manipulate host processes. We know little about how fungal and oomycete effectors target host proteins to promote susceptibility, yet such knowledge is vital to understand crop disease. We show that either transient expression in Nicotiana benthamiana, or stable transgenic expression in potato (Solanum tuberosum), of the Phytophthora infestans RXLR effector Pi02860 enhances leaf colonization by the pathogen. Expression of Pi02860 also attenuates cell death triggered by the P. infestans microbeassociated molecular pattern INF1, indicating that the effector suppresses pattern-triggered immunity. However, the effector does not attenuate cell death triggered by Cf4/Avr4 coexpression, showing that it does not suppress all cell death activated by cell surface receptors. Pi02860 interacts in yeast two-hybrid assays with potato NPH3/RPT2-LIKE1 (NRL1), a predicted CULLIN3-associated ubiquitin E3 ligase. Interaction of Pi02860 in planta was confirmed by coimmunoprecipitation and bimolecular fluorescence complementation assays. Virus-induced gene silencing of NRL1 in N. benthamiana resulted in reduced P. infestans colonization and accelerated INF1-mediated cell death, indicating that this host protein acts as a negative regulator of immunity. Moreover, whereas NRL1 virus-induced gene silencing had no effect on the ability of the P. infestans effector Avr3a to suppress INF1-mediated cell death, such suppression by Pi02860 was significantly attenuated, indicating that this activity of Pi02860 is mediated by NRL1. Transient overexpression of NRL1 resulted in the suppression of INF1-mediated cell death and enhanced P. infestans leaf colonization, demonstrating that NRL1 acts as a susceptibility factor to promote late blight disease.

Shining Light on the Function of NPH3/RPT2-Like Proteins in Phototropin Signaling

“…Consequently, sr1ip1 mutants are more susceptible to Pseudomonas syringae infection, indicating that SR1IP1 serves as a positive regulator of plant immunity (Zhang et al, 2014). By contrast, virus-induced gene silencing of SR1IP1 orthologs in N. benthamiana reduces susceptibility to Phytophthora infestans infection, suggesting that SR1IP1 also can act as a negative regulator of plant defense (Yang et al, 2016). Clearly, more work is needed to elucidate the role of SR1IP1 (NCH1) in plant immunity and how this function integrates with its role in regulating chloroplast accumulation movement .…”

Evidence for intragenic recombination and selective sweep in an effector gene of Phytophthora infestans

“…This theory suggests that effector genes may reduce pathogen fitness and therefore are selected against during pathogen evolution. However, recent molecular and functional analyses indicate that many effector proteins are essential components of infection and may manipulate plant cellular processes to increase host susceptibility and suppress host immune systems (Boevink et al., 2016; Wang et al., 2015; Yang, McLellan, et al., 2016). Consequently, effector genes are expected to evolve differently to other parts of pathogen genomes in reflecting this antagonistic coevolution between the pathogen and host and the trade‐off of the advantages and disadvantages any effector change may cause to the pathogen population.…”

“…However, this RXLR effector repertoire is likely expanding, contributing to the enormous size of the P. infestans genome (Haas et al., 2009; Raffaele & Kamoun, 2012). Biochemical and virulent functions of some RXLR effectors in P. infestans have been characterized recently (Bozkurt et al., 2011; King et al., 2014; McLellan et al., 2013; Wang et al., 2015; Yang, McLellan, et al., 2016). …”

RXLR Effector AVR2 Up-Regulates a Brassinosteroid-Responsive bHLH Transcription Factor to Suppress Immunity

“…A number of examples highlight that the presence and activity of host effector targets can be required for host susceptibility (Yang et al, 2016;Boevink et al, 2016a;Wang et al, 2015;Cui et al, 2010;Chen et al, 2010). Plant genes that are required to support infection, often acting as negative regulators of immunity, are known as susceptibility (S) factors (van Schie and Takken, 2014;Boevink et al, 2016b).…”

“…Many effectors act on positive regulators of immunity to inhibit their activity (Whisson et al, 2016;Deslandes and Rivas, 2012;Dou and Zhou, 2012;Feng et al, 2012;Block and Alfano, 2011). In contrast, a number of pathogen effectors have been found to target host proteins that negatively regulate immunity (Yang et al, 2016;Boevink et al, 2016a;Wang et al, 2015;Cui et al, 2010;Chen et al, 2010). Negative regulators in the host that are required by pathogens to aid disease progression, and are thus manipulated by effectors to promote or use their activity, have been designated as susceptibility (S) factors (van Schie and Takken, 2014;Boevink et al, 2016b).…”