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Sophien Kamoun - One of the best experts on this subject based on the ideXlab platform.
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cross reactivity of a rice nlr immune receptor to distinct Effectors from the rice blast pathogen magnaporthe oryzae provides partial disease resistance
Journal of Biological Chemistry, 2019Co-Authors: Freya A Varden, Sophien Kamoun, Ryohei Terauchi, Hiromasa Saitoh, Kae Yoshino, Marina Franceschetti, Mark J. BanfieldAbstract:Unconventional integrated domains in plant intracellular immune receptors of the nucleotide-binding leucine-rich repeat (NLRs) type can directly bind translocated Effector proteins from pathogens and thereby initiate an immune response. The rice (Oryza sativa) immune receptor pairs Pik-1/Pik-2 and RGA5/RGA4 both use integrated heavy metal-associated (HMA) domains to bind the Effectors AVR-Pik and AVR-Pia, respectively, from the rice blast fungal pathogen Magnaporthe oryzae These Effectors both belong to the MAX Effector family and share a core structural fold, despite being divergent in sequence. How integrated domains in NLRs maintain specificity of Effector recognition, even of structurally similar Effectors, has implications for understanding plant immune receptor evolution and function. Here, using plant cell death and pathogenicity assays and protein-protein interaction analyses, we show that the rice NLR pair Pikp-1/Pikp-2 triggers an immune response leading to partial disease resistance toward the "mis-matched" Effector AVR-Pia in planta and that the Pikp-HMA domain binds AVR-Pia in vitro We observed that the HMA domain from another Pik-1 allele, Pikm, cannot bind AVR-Pia, and it does not trigger a plant response. The crystal structure of Pikp-HMA bound to AVR-Pia at 1.9 A resolution revealed a binding interface different from those formed with AVR-Pik Effectors, suggesting plasticity in integrated domain-Effector interactions. The results of our work indicate that a single NLR immune receptor can bait multiple pathogen Effectors via an integrated domain, insights that may enable engineering plant immune receptors with extended disease resistance profiles.
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Candidate Effector Proteins of the Rust Pathogen Melampsora larici-populina Target Diverse Plant Cell Compartments
Molecular Plant-Microbe Interactions, 2015Co-Authors: Benjamin Petre, Diane G O Saunders, Jan Sklenar, Cécile Lorrain, Joe Win, Sébastien Duplessis, Sophien KamounAbstract:Rust fungi are devastating crop pathogens that deliver Effector proteins into infected tissues to modulate plant functions and promote parasitic growth. The genome of the poplar leaf rust fungus Melampsora larici-populina revealed a large catalog of secreted proteins, some of which have been considered candidate Effectors. Unraveling how these proteins function in host cells is a key to understanding pathogenicity mechanisms and developing resistant plants. In this study, we used an Effectoromics pipeline to select, clone, and express 20 candidate Effectors in Nicotiana benthamiana leaf cells to determine their subcellular localization and identify the plant proteins they interact with. Confocal microscopy revealed that six candidate Effectors target the nucleus, nucleoli, chloroplasts, mitochondria, and discrete cellular bodies. We also used coimmunoprecipitation (coIP) and mass spectrometry to identify 606 N. benthamiana proteins that associate with the candidate Effectors. Five candidate Effectors specifically associated with a small set of plant proteins that may represent biologically relevant interactors. We confirmed the interaction between the candidate Effector MLP124017 and TOPLESS-related protein 4 from poplar by in planta coIP. Altogether, our data enable us to validate Effector proteins from M. larici-populina and reveal that these proteins may target multiple compartments and processes in plant cells. It also shows that N. benthamiana can be a powerful heterologous system to study Effectors of obligate biotrophic pathogens.
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deployment of the burkholderia glumae type iii secretion system as an efficient tool for translocating pathogen Effectors to monocot cells
Plant Journal, 2013Co-Authors: Shailendra Sharma, Akiko Hirabuchi, Shiveta Sharma, Kee Hoon Sohn, Aiko Uemura, Sophien Kamoun, Kentaro Yoshida, Ryohei Terauchi, Koki Fujisaki, Jonathan D G JonesAbstract:†SUMMARY Genome sequences of plant fungal pathogens have enabled the identification of Effectors that cooperatively modulate the cellular environment for successful fungal growth and suppress host defense. Identification and characterization of novel Effector proteins are crucial for understanding pathogen virulence and host-plant defense mechanisms. Previous reports indicate that the Pseudomonas syringae pv. tomato DC3000 type III secretion system (T3SS) can be used to study how non-bacterial Effectors manipulate dicot plant cell function using the Effector detector vector (pEDV) system. Here we report a pEDV-based Effector delivery system in which the T3SS of Burkholderia glumae, an emerging rice pathogen, is used to translocate the AVR-Pik and AVR-Pii Effectors of the fungal pathogen Magnaporthe oryzae to rice cytoplasm. The translocated AVR-Pik and AVR-Pii showed avirulence activity when tested in rice cultivars containing the cognate R genes. AVR-Pik reduced and delayed the hypersensitive response triggered byB. glumaein the non-host plant Nicotiana benthamiana, indicativeof an immunosuppressive virulenceactivity. AVR proteins fused withfluorescent protein and nuclear localization signal were delivered by B. glumae T3SS and observed in the nuclei of infected cells in rice, wheat, barley and N. benthamiana. Our bacterial T3SS-enabled eukaryotic Effector delivery and subcellular localizationassaysprovidea usefulmethodforidentifyingandstudyingEffector functionsin monocotplants.
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host protein bsl1 associates with phytophthora infestans rxlr Effector avr2 and the solanum demissum immune receptor r2 to mediate disease resistance
The Plant Cell, 2012Co-Authors: Diane G O Saunders, Sebastian Schornack, Tolga O. Bozkurt, Susan Breen, Ingo Hein, Nicolas Champouret, Vivianne G A A Vleeshouwers, Paul R J Birch, Eleanor M Gilroy, Sophien KamounAbstract:Plant pathogens secrete Effector proteins to modulate plant immunity and promote host colonization. Plant nucleotide binding leucine-rich repeat (NB-LRR) immunoreceptors recognize specific pathogen Effectors directly or indirectly. Little is known about how NB-LRR proteins recognize Effectors of filamentous plant pathogens, such as Phytophthora infestans. AVR2 belongs to a family of 13 sequence-divergent P. infestans RXLR Effectors that are differentially recognized by members of the R2 NB-LRR family in Solanum demissum. We report that the putative plant phosphatase BSU-LIKE PROTEIN1 (BSL1) is required for R2-mediated perception of AVR2 and resistance to P. infestans. AVR2 associates with BSL1 and mediates the interaction of BSL1 with R2 in planta, possibly through the formation of a ternary complex. Strains of P. infestans that are virulent on R2 potatoes express an unrecognized form, Avr2-like (referred to as A2l). A2L can still interact with BSL1 but does not promote the association of BSL1 with R2. Our findings show that recognition of the P. infestans AVR2 Effector by the NB-LRR protein R2 requires the putative phosphatase BSL1. This reveals that, similar to Effectors of phytopathogenic bacteria, recognition of filamentous pathogen Effectors can be mediated via a host protein that interacts with both the Effector and the NB-LRR immunoreceptor.
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Oomycetes, Effectors, and all that jazz
Current opinion in plant biology, 2012Co-Authors: Tolga O. Bozkurt, Sebastian Schornack, Mark J. Banfield, Sophien KamounAbstract:Plant pathogenic oomycetes secrete a diverse repertoire of Effector proteins that modulate host innate immunity and enable parasitic infection. Understanding how Effectors evolve, translocate and traffic inside host cells, and perturb host processes are major themes in the study of oomycete-plant interactions. The last year has seen important progress in the study of oomycete Effectors with, notably, the elucidation of the 3D structures of five RXLR Effectors, and novel insights into how cytoplasmic Effectors subvert host cells. In this review, we discuss these and other recent advances and highlight the most important open questions in oomycete Effector biology.
Peter D Nagy - One of the best experts on this subject based on the ideXlab platform.
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screening legionella Effectors for antiviral effects reveals rab1 gtpase as a proviral factor coopted for tombusvirus replication
Proceedings of the National Academy of Sciences of the United States of America, 2019Co-Authors: Junichi Inaba, Kai Xu, Nikolay Kovalev, Harish N Ramanathan, Brett D Lindenbach, Peter D NagyAbstract:Bacterial virulence factors or Effectors are proteins targeted into host cells to coopt or interfere with cellular proteins and pathways. Viruses often coopt the same cellular proteins and pathways to support their replication in infected cells. Therefore, we screened the Legionella pneumophila Effectors to probe virus–host interactions and identify factors that modulate tomato bushy stunt virus (TBSV) replication in yeast surrogate host. Among 302 Legionella Effectors tested, 28 Effectors affected TBSV replication. To unravel a coopted cellular pathway in TBSV replication, the identified DrrA Effector from Legionella was further exploited. We find that expression of DrrA in yeast or plants blocks TBSV replication through inhibiting the recruitment of Rab1 small GTPase and endoplasmic reticulum-derived COPII vesicles into the viral replication compartment. TBSV hijacks Rab1 and COPII vesicles to create enlarged membrane surfaces and optimal lipid composition within the viral replication compartment. To further validate our Legionella Effector screen, we used the Legionella Effector LepB lipid kinase to confirm the critical proviral function of PI(3)P phosphoinositide and the early endosomal compartment in TBSV replication. We demonstrate the direct inhibitory activity of LegC8 Effector on TBSV replication using a cell-free replicase reconstitution assay. LegC8 inhibits the function of eEF1A, a coopted proviral host factor. Altogether, the identified bacterial Effectors with anti-TBSV activity could be powerful reagents in cell biology and virus–host interaction studies. This study provides important proof of concept that bacterial Effector proteins can be a useful toolbox to identify host factors and cellular pathways coopted by (+)RNA viruses.
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screening legionella Effectors for antiviral effects reveals rab1 gtpase as a proviral factor coopted for tombusvirus replication
Proceedings of the National Academy of Sciences of the United States of America, 2019Co-Authors: Junichi Inaba, Nikolay Kovalev, Harish N Ramanathan, Brett D Lindenbach, Craig R Roy, Peter D NagyAbstract:Bacterial virulence factors or Effectors are proteins targeted into host cells to coopt or interfere with cellular proteins and pathways. Viruses often coopt the same cellular proteins and pathways to support their replication in infected cells. Therefore, we screened the Legionella pneumophila Effectors to probe virus-host interactions and identify factors that modulate tomato bushy stunt virus (TBSV) replication in yeast surrogate host. Among 302 Legionella Effectors tested, 28 Effectors affected TBSV replication. To unravel a coopted cellular pathway in TBSV replication, the identified DrrA Effector from Legionella was further exploited. We find that expression of DrrA in yeast or plants blocks TBSV replication through inhibiting the recruitment of Rab1 small GTPase and endoplasmic reticulum-derived COPII vesicles into the viral replication compartment. TBSV hijacks Rab1 and COPII vesicles to create enlarged membrane surfaces and optimal lipid composition within the viral replication compartment. To further validate our Legionella Effector screen, we used the Legionella Effector LepB lipid kinase to confirm the critical proviral function of PI(3)P phosphoinositide and the early endosomal compartment in TBSV replication. We demonstrate the direct inhibitory activity of LegC8 Effector on TBSV replication using a cell-free replicase reconstitution assay. LegC8 inhibits the function of eEF1A, a coopted proviral host factor. Altogether, the identified bacterial Effectors with anti-TBSV activity could be powerful reagents in cell biology and virus-host interaction studies. This study provides important proof of concept that bacterial Effector proteins can be a useful toolbox to identify host factors and cellular pathways coopted by (+)RNA viruses.
Ziding Zhang - One of the best experts on this subject based on the ideXlab platform.
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network analysis reveals a common host pathogen interaction pattern in arabidopsis immune responses
Frontiers in Plant Science, 2017Co-Authors: Yuan Zhou, Ziding ZhangAbstract:Many plant pathogens secrete virulence Effectors into host cells to target important proteins in host cellular network. However, the dynamic interactions between Effectors and host cellular network have not been fully understood. Here, an integrative network analysis was conducted by combining Arabidopsis thaliana protein-protein interaction network, known targets of Pseudomonas syringae and Hyaloperonospora arabidopsidis Effectors, and gene expression profiles in the immune response. In particular, we focused on the characteristic network topology of the Effector targets and differentially expressed genes (DEGs). We found that Effectors tended to manipulate key network positions with higher betweenness centrality. The Effector targets, especially those that are common targets of an individual Effector, tended to be clustered together in the network. Moreover, the distances between the Effector targets and DEGs increased over time during infection. In line with this observation, pathogen-susceptible mutants tended to have more DEGs surrounding the Effector targets compared with resistant mutants. Our results suggest a common plant-pathogen interaction pattern at the cellular network level, where pathogens employ potent local impact mode to interfere with key positions in the host network, and plant organizes an in-depth defense by sequentially activating genes distal to the Effector targets.
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Network Analysis Reveals a Common Host–Pathogen Interaction Pattern in Arabidopsis Immune Responses
Frontiers in Plant Science, 2017Co-Authors: Hong Li, Yuan Zhou, Ziding ZhangAbstract:Many plant pathogens secrete virulence Effectors into host cells to target important proteins in host cellular network. However, the dynamic interactions between Effectors and host cellular network have not been fully understood. Here, an integrative network analysis was conducted by combining Arabidopsis thaliana protein-protein interaction network, known targets of Pseudomonas syringae and Hyaloperonospora arabidopsidis Effectors, and gene expression profiles in the immune response. In particular, we focused on the characteristic network topology of the Effector targets and differentially expressed genes (DEGs). We found that Effectors tended to manipulate key network positions with higher betweenness centrality. The Effector targets, especially those that are common targets of an individual Effector, tended to be clustered together in the network. Moreover, the distances between the Effector targets and DEGs increased over time during infection. In line with this observation, pathogen-susceptible mutants tended to have more DEGs surrounding the Effector targets compared with resistant mutants. Our results suggest a common plant-pathogen interaction pattern at the cellular network level, where pathogens employ potent local impact mode to interfere with key positions in the host network, and plant organizes an in-depth defense by sequentially activating genes distal to the Effector targets.
Junichi Inaba - One of the best experts on this subject based on the ideXlab platform.
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screening legionella Effectors for antiviral effects reveals rab1 gtpase as a proviral factor coopted for tombusvirus replication
Proceedings of the National Academy of Sciences of the United States of America, 2019Co-Authors: Junichi Inaba, Kai Xu, Nikolay Kovalev, Harish N Ramanathan, Brett D Lindenbach, Peter D NagyAbstract:Bacterial virulence factors or Effectors are proteins targeted into host cells to coopt or interfere with cellular proteins and pathways. Viruses often coopt the same cellular proteins and pathways to support their replication in infected cells. Therefore, we screened the Legionella pneumophila Effectors to probe virus–host interactions and identify factors that modulate tomato bushy stunt virus (TBSV) replication in yeast surrogate host. Among 302 Legionella Effectors tested, 28 Effectors affected TBSV replication. To unravel a coopted cellular pathway in TBSV replication, the identified DrrA Effector from Legionella was further exploited. We find that expression of DrrA in yeast or plants blocks TBSV replication through inhibiting the recruitment of Rab1 small GTPase and endoplasmic reticulum-derived COPII vesicles into the viral replication compartment. TBSV hijacks Rab1 and COPII vesicles to create enlarged membrane surfaces and optimal lipid composition within the viral replication compartment. To further validate our Legionella Effector screen, we used the Legionella Effector LepB lipid kinase to confirm the critical proviral function of PI(3)P phosphoinositide and the early endosomal compartment in TBSV replication. We demonstrate the direct inhibitory activity of LegC8 Effector on TBSV replication using a cell-free replicase reconstitution assay. LegC8 inhibits the function of eEF1A, a coopted proviral host factor. Altogether, the identified bacterial Effectors with anti-TBSV activity could be powerful reagents in cell biology and virus–host interaction studies. This study provides important proof of concept that bacterial Effector proteins can be a useful toolbox to identify host factors and cellular pathways coopted by (+)RNA viruses.
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screening legionella Effectors for antiviral effects reveals rab1 gtpase as a proviral factor coopted for tombusvirus replication
Proceedings of the National Academy of Sciences of the United States of America, 2019Co-Authors: Junichi Inaba, Nikolay Kovalev, Harish N Ramanathan, Brett D Lindenbach, Craig R Roy, Peter D NagyAbstract:Bacterial virulence factors or Effectors are proteins targeted into host cells to coopt or interfere with cellular proteins and pathways. Viruses often coopt the same cellular proteins and pathways to support their replication in infected cells. Therefore, we screened the Legionella pneumophila Effectors to probe virus-host interactions and identify factors that modulate tomato bushy stunt virus (TBSV) replication in yeast surrogate host. Among 302 Legionella Effectors tested, 28 Effectors affected TBSV replication. To unravel a coopted cellular pathway in TBSV replication, the identified DrrA Effector from Legionella was further exploited. We find that expression of DrrA in yeast or plants blocks TBSV replication through inhibiting the recruitment of Rab1 small GTPase and endoplasmic reticulum-derived COPII vesicles into the viral replication compartment. TBSV hijacks Rab1 and COPII vesicles to create enlarged membrane surfaces and optimal lipid composition within the viral replication compartment. To further validate our Legionella Effector screen, we used the Legionella Effector LepB lipid kinase to confirm the critical proviral function of PI(3)P phosphoinositide and the early endosomal compartment in TBSV replication. We demonstrate the direct inhibitory activity of LegC8 Effector on TBSV replication using a cell-free replicase reconstitution assay. LegC8 inhibits the function of eEF1A, a coopted proviral host factor. Altogether, the identified bacterial Effectors with anti-TBSV activity could be powerful reagents in cell biology and virus-host interaction studies. This study provides important proof of concept that bacterial Effector proteins can be a useful toolbox to identify host factors and cellular pathways coopted by (+)RNA viruses.
Adam J Bogdanove - One of the best experts on this subject based on the ideXlab platform.
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functional analysis of african xanthomonas oryzae pv oryzae talomes reveals a new susceptibility gene in bacterial leaf blight of rice
PLOS Pathogens, 2018Co-Authors: Tuan Tu Tran, Valérie Verdier, Alvaro L Perezquintero, Issa Wonni, Sara C D Carpenter, Yanhua Yu, Li Wang, Jan E Leach, Sebastien Cunnac, Adam J BogdanoveAbstract:Most Xanthomonas species translocate Transcription Activator-Like (TAL) Effectors into plant cells where they function like plant transcription factors via a programmable DNA-binding domain. Characterized strains of rice pathogenic X. oryzae pv. oryzae harbor 9–16 different tal Effector genes, but the function of only a few of them has been decoded. Using sequencing of entire genomes, we first performed comparative analyses of the complete repertoires of TAL Effectors, herein referred to as TALomes, in three Xoo strains forming an African genetic lineage different from Asian Xoo. A phylogenetic analysis of the three TALomes combined with in silico predictions of TAL Effector targets showed that African Xoo TALomes are highly conserved, genetically distant from Asian ones, and closely related to TAL Effectors from the bacterial leaf streak pathogen Xanthomonas oryzae pv. oryzicola (Xoc). Nine clusters of TAL Effectors could be identified among the three TALomes, including three showing higher levels of variation in their repeat variable diresidues (RVDs). Detailed analyses of these groups revealed recombination events as a possible source of variation among TAL Effector genes. Next, to address contribution to virulence, nine TAL Effector genes from the Malian Xoo strain MAI1 and four allelic variants from the Burkinabe Xoo strain BAI3, thus representing most of the TAL Effector diversity in African Xoo strains, were expressed in the TAL Effector-deficient X. oryzae strain X11-5A for gain-of-function assays. Inoculation of the susceptible rice variety Azucena lead to the discovery of three TAL Effectors promoting virulence, including two TAL Effectors previously reported to target the susceptibility (S) gene OsSWEET14 and a novel major virulence contributor, TalB. RNA profiling experiments in rice and in silico prediction of EBEs were carried out to identify candidate targets of TalB, revealing OsTFX1, a bZIP transcription factor previously identified as a bacterial blight S gene, and OsERF#123, which encodes a subgroup IXc AP2/ERF transcription factor. Use of designer TAL Effectors demonstrated that induction of either gene resulted in greater susceptibility to strain X11-5A. The induction of OsERF#123 by BAI3Δ1, a talB knockout derivative of BAI3, carrying these designer TAL Effectors increased virulence of BAI3Δ1, validating OsERF#123 as a new, bacterial blight S gene.
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a resistance locus in the american heirloom rice variety carolina gold select is triggered by tal Effectors with diverse predicted targets and is effective against african strains of xanthomonas oryzae pv oryzicola
Plant Journal, 2016Co-Authors: Adam J Bogdanove, Valérie Verdier, Lindsay R Triplett, Stephen P Cohen, Christopher Heffelfinger, Clarice Schmidt, Alejandra I Huerta, Cheick TeketeAbstract:The rice pathogens Xanthomonas oryzae pathovar (pv.) oryzae and pv. oryzicola produce numerous transcription activator-like (TAL) Effectors that increase bacterial virulence by activating expression of host susceptibility genes. Rice resistance mechanisms against TAL Effectors include polymorphisms that prevent Effector binding to susceptibility gene promoters, or that allow Effector activation of resistance genes. This study identifies, in the heirloom variety Carolina Gold Select, a third mechanism of rice resistance involving TAL Effectors. This resistance manifests through strong suppression of disease development in response to diverse TAL Effectors from both X. oryzae pathovars. The resistance can be triggered by an Effector with only 3.5 central repeats, is independent of the composition of the repeat variable di-residues that determine TAL Effector binding specificity, and is independent of the transcriptional activation domain. We determined that the resistance is conferred by a single dominant locus, designated Xo1, that maps to a 1.09 Mbp fragment on chromosome 4. The Xo1 interval also confers complete resistance to the strains in the African clade of X. oryzae pv. oryzicola, representing the first dominant resistance locus against bacterial leaf streak in rice. The strong phenotypic similarity between the TAL Effector-triggered resistance conferred by Xo1 and that conferred by the tomato resistance gene Bs4 suggests that monocots and dicots share an ancient or convergently evolved mechanism to recognize analogous TAL Effector epitopes.
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principles and applications of tal Effectors for plant physiology and metabolism
Current Opinion in Plant Biology, 2014Co-Authors: Adam J BogdanoveAbstract:Recent advances in DNA targeting allow unprecedented control over gene function and expression. Targeting based on TAL Effectors is arguably the most promising for systems biology and metabolic engineering. Multiple, orthogonal TAL-Effector reagents of different types can be used in the same cell. Furthermore, variation in base preferences of the individual structural repeats that make up the TAL Effector DNA recognition domain makes targeting stringency tunable. Realized applications range from genome editing to epigenome modification to targeted gene regulation to chromatin labeling and capture. The principles that govern TAL Effector DNA recognition make TAL Effectors well suited for applications relevant to plant physiology and metabolism. TAL Effector targeting has merits that are distinct from those of the RNA-based DNA targeting CRISPR/Cas9 system.
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tal Effector nucleotide targeter tale nt 2 0 tools for tal Effector design and target prediction
Nucleic Acids Research, 2012Co-Authors: Erin L Doyle, Nicholas J Booher, Daniel S Standage, Daniel F Voytas, Volker Brendel, John K Vandyk, Adam J BogdanoveAbstract:Transcription activator-like (TAL) Effectors are repeat-containing proteins used by plant pathogenic bacteria to manipulate host gene expression. Repeats are polymorphic and individually specify single nucleotides in the DNA target, with some degeneracy. A TAL Effector-nucleotide binding code that links repeat type to specified nucleotide enables prediction of genomic binding sites for TAL Effectors and customization of TAL Effectors for use in DNA targeting, in particular as custom transcription factors for engineered gene regulation and as site-specific nucleases for genome editing. We have developed a suite of web-based tools called TAL Effector-Nucleotide Targeter 2.0 (TALE-NT 2.0; https://boglab.plp.iastate.edu/) that enables design of custom TAL Effector repeat arrays for desired targets and prediction of TAL Effector binding sites, ranked by likelihood, in a genome, promoterome or other sequence of interest. Search parameters can be set by the user to work with any TAL Effector or TAL Effector nuclease architecture. Applications range from designing highly specific DNA targeting tools and identifying potential off-target sites to predicting Effector targets important in plant disease.
