RefPlantNLR: a comprehensive collection of experimentally validated plant NLRs

Reference datasets are critical in computational biology. They help define canonical biological features and are essential for benchmarking studies. Here, we describe a comprehensive reference dataset of experimentally validated plant NLR immune receptors. RefPlantNLR consists of 415 NLRs from 31 genera belonging to 11 orders of flowering plants. We used RefPlantNLR to determine the canonical features of functionally validated plant NLRs. This reference dataset should prove useful for benchmarking NLR annotation tools, guiding comparative analyses of NLRs across the wide spectrum of plant diversity and identifying under-studied taxa. We hope that the RefPlantNLR resource will contribute to moving the field beyond a uniform view of NLR structure and function.

[1]  E. A. van der Biezen,et al.  Plant disease-resistance proteins and the gene-for-gene concept. , 1998, Trends in biochemical sciences.

[2]  Genome‐wide functional analysis of hot pepper immune receptors reveals an autonomous NLR clade in seed plants , 2020, The New phytologist.

[3]  R. V. D. van der Hoorn,et al.  Defended to the Nines: 25 Years of Resistance Gene Cloning Identifies Nine Mechanisms for R Protein Function[OPEN] , 2018, Plant Cell.

[4]  Jonathan D. G. Jones,et al.  NLR-parser: rapid annotation of plant NLR complements , 2015, Bioinform..

[5]  Stephen A. Smith,et al.  Constructing a broadly inclusive seed plant phylogeny. , 2018, American journal of botany.

[6]  R. Terauchi,et al.  The “sensor domains” of plant NLR proteins: more than decoys? , 2015, Front. Plant Sci..

[7]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[8]  Witold Dyrka,et al.  Identification of NLR-associated amyloid signaling motifs in filamentous bacteria , 2020, bioRxiv.

[9]  Jonathan D. G. Jones,et al.  Alien Domains Shaped the Modular Structure of Plant NLR Proteins , 2019, Genome biology and evolution.

[10]  A. Deslauriers,et al.  The large repertoire of conifer NLR resistance genes includes drought responsive and highly diversified RNLs , 2019, Scientific Reports.

[11]  A. Deveau,et al.  Do fungi have an innate immune response? An NLR-based comparison to plant and animal immune systems , 2017, PLoS pathogens.

[12]  S. Kamoun,et al.  Receptor networks underpin plant immunity , 2018, Science.

[13]  R. Terauchi,et al.  NLR network mediates immunity to diverse plant pathogens , 2017, Proceedings of the National Academy of Sciences.

[14]  C. Chothia,et al.  Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. , 2001, Journal of molecular biology.

[15]  S. Cloutier,et al.  RGAugury: a pipeline for genome-wide prediction of resistance gene analogs (RGAs) in plants , 2016, BMC Genomics.

[16]  F. Fonseca,et al.  Plant NLR receptor proteins and their potential in the development of durable genetic resistance to biotic stresses , 2019, Biotechnology Research and Innovation.

[17]  Yvan Saeys,et al.  Essential guidelines for computational method benchmarking , 2018, Genome Biology.

[18]  Jonathan D. G. Jones,et al.  Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens , 2016, BMC Biology.

[19]  Zhengwei Zhu,et al.  CD-HIT: accelerated for clustering the next-generation sequencing data , 2012, Bioinform..

[20]  Meng Li,et al.  Evolution of NLR resistance genes with non-canonical N-terminal domains in wild tomato species. , 2020, The New phytologist.

[21]  David A. Lee,et al.  CATH: an expanded resource to predict protein function through structure and sequence , 2016, Nucleic Acids Res..

[22]  D. Merdinoglu,et al.  NLGenomeSweeper: A Tool for Genome-Wide NBS-LRR Resistance Gene Identification , 2020, Genes.

[23]  B. Steuernagel,et al.  BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust , 2018, Nature Plants.

[24]  Terri K. Attwood,et al.  PRINTS-S: the database formerly known as PRINTS , 2000, Nucleic Acids Res..

[25]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v4: recent updates and new developments , 2019, Nucleic Acids Res..

[26]  J. Rougemont,et al.  A rapid bootstrap algorithm for the RAxML Web servers. , 2008, Systematic biology.

[27]  K. Krasileva,et al.  Evolution of Plant NLRs: From Natural History to Precise Modifications. , 2020, Annual review of plant biology.

[28]  D. Higgins,et al.  Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega , 2011, Molecular systems biology.

[29]  T. Kroj,et al.  Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread , 2016, The New phytologist.

[30]  W. Haerty,et al.  Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions , 2017, Genome Biology.

[31]  Silvio C. E. Tosatto,et al.  InterPro in 2017—beyond protein family and domain annotations , 2016, Nucleic Acids Res..

[32]  An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species , 2019, eLife.

[33]  Mauno Vihinen,et al.  Representativeness of variation benchmark datasets , 2018, BMC Bioinformatics.

[34]  Andreu Paytuví Gallart,et al.  PRGdb 3.0: a comprehensive platform for prediction and analysis of plant disease resistance genes , 2017, Nucleic Acids Res..

[35]  S. Kamoun,et al.  NLR singletons, pairs, and networks: evolution, assembly, and regulation of the intracellular immunoreceptor circuitry of plants. , 2019, Current opinion in plant biology.

[36]  Silvio C. E. Tosatto,et al.  The Pfam protein families database in 2019 , 2018, Nucleic Acids Res..

[37]  William R. Taylor,et al.  The rapid generation of mutation data matrices from protein sequences , 1992, Comput. Appl. Biosci..

[38]  F. Micheli,et al.  RRGPredictor, a set-theory-based tool for predicting pathogen-associated molecular pattern receptors (PRRs) and resistance (R) proteins from plants. , 2020, Genomics.

[39]  S. Kamoun,et al.  From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors , 2008, The Plant Cell Online.

[40]  T. Kroj,et al.  A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis , 2014, Front. Plant Sci..

[41]  Takaki Maekawa,et al.  Evolution and Conservation of Plant NLR Functions , 2013, Front. Immunol..

[42]  Peter Jeschke,et al.  Pivoting the Plant Immune System from Dissection to Deployment , 2013 .

[43]  R. Terauchi,et al.  Lessons in Effector and NLR Biology of Plant-Microbe Systems. , 2018, Molecular plant-microbe interactions : MPMI.

[44]  M. Yano,et al.  Durable panicle blast-resistance gene Pb1 encodes an atypical CC-NBS-LRR protein and was generated by acquiring a promoter through local genome duplication. , 2010, The Plant journal : for cell and molecular biology.

[45]  Jonathan D. G. Jones,et al.  The NLR-Annotator Tool Enables Annotation of the Intracellular Immune Receptor Repertoire1[OPEN] , 2020, Plant Physiology.

[46]  S. Kamoun,et al.  An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species , 2019, bioRxiv.

[47]  Jonathan D. G. Jones,et al.  Intracellular innate immune surveillance devices in plants and animals , 2016, Science.