A Phytophthora infestans RXLR effector targets plant PP1c isoforms that promote late blight disease

Boevink, Petra C.; Wang, Xiaodan; McLellan, Hazel; He, Qiaojun; Naqvi, Shaista; Armstrong, Miles; Zhang, Wei; Hein, Ingo; Gilroy, Eleanor M.; Tian, Zhendong; Birch, Paul R. J.

doi:10.1038/ncomms10311

Cited by 126 publications

(165 citation statements)

References 48 publications

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“…1C). The enhancement of P. infestans leaf colonization promoted by Pi02860 expression inside host cells is similar to that of other recently described RXLR effectors (McLellan et al, 2013;King et al, 2014;Zheng et al, 2014;Wang et al, 2015;Boevink et al, 2016) and consistent with it modifying the host to promote susceptibility.…”

Section: Pi02860 Promotes P Infestans Virulence and Suppresses Ptisupporting

confidence: 86%

“…More recently, an RXLR effector from P. infestans was shown to target host PP1c isoforms. Rather than inhibiting these phosphatases, the effector forms unique holoenzymes with them to presumably dephosphorylate key substrates in the plant nucleus, leading to enhanced susceptibility (Boevink et al, 2016). Thus, the PP1c isoforms also can be regarded as susceptibility factors.…”

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confidence: 99%

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

et al. 2016

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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.

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Section: Pi02860 Promotes P Infestans Virulence and Suppresses Ptisupporting

confidence: 86%

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confidence: 99%

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

et al. 2016

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“…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).…”

Section: Avr2 Transgenic Plants Are More Susceptible To P Infestansmentioning

confidence: 99%

“…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).…”

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confidence: 99%

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

Turnbull

Yang²,

Naqvi³

et al. 2017

Plant Physiol.

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An emerging area in plant research focuses on antagonism between regulatory systems governing growth and immunity. Such cross talk represents a point of vulnerability for pathogens to exploit. AVR2, an RXLR effector secreted by the potato blight pathogen Phytophthora infestans, interacts with potato BSL1, a putative phosphatase implicated in growthpromoting brassinosteroid (BR) hormone signaling. Transgenic potato (Solanum tuberosum) plants expressing the effector exhibit transcriptional and phenotypic hallmarks of overactive BR signaling and show enhanced susceptibility to P. infestans. Microarray analysis was used to identify a set of BR-responsive marker genes in potato, all of which are constitutively expressed to BR-induced levels in AVR2 transgenic lines. One of these genes was a bHLH transcription factor, designated StCHL1, homologous to AtCIB1 and AtHBI1, which are known to facilitate antagonism between BR and immune responses. Transient expression of either AVR2 or CHL1 enhanced leaf colonization by P. infestans and compromised immune cell death activated by perception of the elicitin Infestin1 (INF1). Knockdown of CHL1 transcript using Virus-Induced Gene Silencing (VIGS) reduced colonization of P. infestans on Nicotiana benthamiana. Moreover, the ability of AVR2 to suppress INF1-triggered cell death was attenuated in NbCHL1-silenced plants, indicating that NbCHL1 was important for this effector activity. Thus, AVR2 exploits cross talk between BR signaling and innate immunity in Solanum species, representing a novel, indirect mode of innate immune suppression by a filamentous pathogen effector.

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“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Yang

Ouyang

Fang

et al. 2018

Evolutionary Applications

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Effectors, a group of small proteins secreted by pathogens, play a critical role in the antagonistic interaction between plant hosts and pathogens through their dual functions in regulating host immune systems and pathogen infection capability. In this study, evolution in effector genes was investigated through population genetic analysis of Avr3a sequences generated from 96 Phytophthora infestans isolates collected from six locations representing a range of thermal variation and cropping systems in China. We found high genetic variation in the Avr3a gene resulting from diverse mechanisms extending beyond point mutations, frameshift, and defeated start and stop codons to intragenic recombination. A total of 51 nucleotide haplotypes encoding 38 amino acid isoforms were detected in the 96 full sequences with nucleotide diversity in the pathogen populations ranging from 0.007 to 0.023 (mean = 0.017). Although haplotype and nucleotide diversity were high, the effector gene was dominated by only three haplotypes. Evidence for a selective sweep was provided by (i) the population genetic differentiation (G ST) of haplotypes being lower than the population differentiation (F ST ) of SSR marker loci; and (ii) negative values of Tajima's D and Fu's FS. Annual mean temperature in the collection sites was negatively correlated with the frequency of the virulent form (Avr3aEM), indicating Avr3a may be regulated by temperature. These results suggest that elevated air temperature due to global warming may hamper the development of pathogenicity traits in P. infestans and further study under confined thermal regimes may be required to confirm the hypothesis.

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A Phytophthora infestans RXLR effector targets plant PP1c isoforms that promote late blight disease

Cited by 126 publications

References 48 publications

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

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

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

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

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