TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes.

The Toll/interleukin-1 receptor (TIR) domain is found in one of the two large families of homologues of plant disease resistance proteins (R proteins) in Arabidopsis and other dicotyledonous plants. In addition to these TIR-NBS-LRR (TNL) R proteins, we identified two families of TIR-containing proteins encoded in the Arabidopsis Col-0 genome. The TIR-X (TX) family of proteins lacks both the nucleotide-binding site (NBS) and the leucine rich repeats (LRRs) that are characteristic of the R proteins, while the TIR-NBS (TN) proteins contain much of the NBS, but lack the LRR. In Col-0, the TX family is encoded by 27 genes and three pseudogenes; the TN family is encoded by 20 genes and one pseudogene. Using massively parallel signature sequencing (MPSS), expression was detected at low levels for approximately 85% of the TN-encoding genes. Expression was detected for only approximately 40% of the TX-encoding genes, again at low levels. Physical map data and phylogenetic analysis indicated that multiple genomic duplication events have increased the numbers of TX and TN genes in Arabidopsis. Genes encoding TX, TN and TNL proteins were demonstrated in conifers; TX and TN genes are present in very low numbers in grass genomes. The expression, prevalence, and diversity of TX and TN genes suggests that these genes encode functional proteins rather than resulting from degradation or deletions of TNL genes. These TX and TN proteins could be plant analogues of small TIR-adapter proteins that function in mammalian innate immune responses such as MyD88 and Mal.

[1]  Zhonghe Zhou,et al.  The smallest known non-avian theropod dinosaur , 2000, Nature.

[2]  A. Mantovani,et al.  The Toll receptor family , 2001, Allergy.

[3]  Dirk E. Smith,et al.  Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction , 2001, Nature.

[4]  R. Medzhitov,et al.  Drosophila MyD88 is an adapter in the Toll signaling pathway , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[5]  B. Barrell,et al.  Prevalence of small inversions in yeast gene order evolution. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[6]  P. Singh,et al.  Sequence architecture downstream of the initiator codon enhances gene expression and protein stability in plants. , 2001, Plant physiology.

[7]  S. Dinesh-Kumar,et al.  Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[8]  M. Coleman,et al.  Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. , 2001, Science.

[9]  J. Leach,et al.  Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. , 2002, Genome research.

[10]  E V Koonin,et al.  Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. , 2001, Science.

[11]  R. Medzhitov,et al.  The Toll-receptor family and control of innate immunity. , 1999, Current opinion in immunology.

[12]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[13]  E. Koonin,et al.  The domains of death: evolution of the apoptosis machinery. , 1999, Trends in biochemical sciences.

[14]  J Schultz,et al.  SMART, a simple modular architecture research tool: identification of signaling domains. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  E. Vermaas,et al.  In vitro cloning of complex mixtures of DNA on microbeads: physical separation of differentially expressed cDNAs. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[16]  P. Ricciardi-Castagnoli,et al.  Physical contact between lipopolysaccharide and toll-like receptor 4 revealed by genetic complementation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Rithy K. Roth,et al.  Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays , 2000, Nature Biotechnology.

[18]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[19]  D. Lipman,et al.  Improved tools for biological sequence comparison. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Jonathan D. G. Jones,et al.  Plant pathogens and integrated defence responses to infection , 2001, Nature.

[21]  E. A. van der Biezen,et al.  The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. , 1997, The Plant cell.

[22]  B. Beutler,et al.  Three novel mammalian toll-like receptors: gene structure, expression, and evolution. , 2000, European cytokine network.

[23]  S. Srinivasula,et al.  Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. , 1998, Molecular cell.

[24]  Nevin D. Young,et al.  Diversity, Distribution, and Ancient Taxonomic Relationships Within the TIR and Non-TIR NBS-LRR Resistance Gene Subfamilies , 2002, Journal of Molecular Evolution.

[25]  D. Eisenberg,et al.  Detecting protein function and protein-protein interactions from genome sequences. , 1999, Science.

[26]  M. Timko,et al.  NRSA-1: a resistance gene homolog expressed in roots of non-host plants following parasitism by Striga asiatica (witchweed). , 1999, The Plant journal : for cell and molecular biology.

[27]  M. Chase,et al.  Chloroplast and nuclear gene sequences indicate late Pennsylvanian time for the last common ancestor of extant seed plants. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[28]  N. Franklin-Tong Receptor-ligand interaction demonstrated in Brassica self-incompatibility. , 2002, Trends in genetics : TIG.

[29]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[30]  D. Leister,et al.  Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. , 2002, Molecular biology and evolution.

[31]  S. Dower,et al.  Identification of Two Major Sites in the Type I Interleukin-1 Receptor Cytoplasmic Region Responsible for Coupling to Pro-inflammatory Signaling Pathways* , 2000, The Journal of Biological Chemistry.

[32]  S. Kruglyak,et al.  Regulation of adjacent yeast genes. , 2000, Trends in genetics : TIG.

[33]  T. Kaisho,et al.  Dendritic-cell function in Toll-like receptor- and MyD88-knockout mice. , 2001, Trends in immunology.

[34]  B. Staskawicz,et al.  The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes , 1999 .

[35]  E. Finnegan,et al.  Analysis of alternative transcripts of the flax L6 rust resistance gene. , 1999, The Plant journal : for cell and molecular biology.

[36]  Charles Elkan,et al.  The Value of Prior Knowledge in Discovering Motifs with MEME , 1995, ISMB.

[37]  R. Fluhr,et al.  Divergent Evolution of Plant NBS-LRR Resistance Gene Homologues in Dicot and Cereal Genomes , 2000, Journal of Molecular Evolution.

[38]  E. Finnegan,et al.  The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. , 1995, The Plant cell.

[39]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[40]  Daniel T. Lavelle,et al.  Tomato Prf Is a Member of the Leucine-Rich Repeat Class of Plant Disease Resistance Genes and Lies Embedded within the Pto Kinase Gene Cluster , 1996, Cell.

[41]  M. C. Heath Hypersensitive response-related death , 2000, Plant Molecular Biology.

[42]  S. Dinesh-Kumar,et al.  The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor , 1994, Cell.

[43]  B. Sobral,et al.  Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide‐binding superfamily , 1999 .

[44]  J. Glazebrook,et al.  Genes controlling expression of defense responses in Arabidopsis--2001 status. , 2001, Current opinion in plant biology.

[45]  G. Núñez,et al.  WD-40 Repeat Region Regulates Apaf-1 Self-association and Procaspase-9 Activation* , 1998, The Journal of Biological Chemistry.

[46]  A. D. McLachlan,et al.  Profile analysis: detection of distantly related proteins. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[47]  R. Fluhr Sentinels of disease. Plant resistance genes. , 2001, Plant physiology.

[48]  M. Nasrallah,et al.  The male determinant of self-incompatibility in Brassica. , 1999, Science.

[49]  L. Tong,et al.  Structural basis for signal transduction by the Toll/interleukin-1 receptor domains , 2000, Nature.

[50]  E. A. van der Biezen,et al.  Pronounced Intraspecific Haplotype Divergence at the RPP5 Complex Disease Resistance Locus of Arabidopsis , 1999, Plant Cell.

[51]  C. Janeway,et al.  MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. , 1998, Molecular cell.