First published online March 13, 2003; 10.1105/tpc.009308
The Plant Cell, Vol. 15, 809-834,
April 2003, Copyright © 2003,
American Society of Plant Biologists
Genome-Wide Analysis of NBS-LRREncoding Genes in Arabidopsis
Blake C. Meyersa,b,
Alexander Kozika,
Alyssa Griegoa,
Hanhui Kuanga and
Richard W. Michelmore1,a
a Department of Vegetable Crops, University of California, Davis, California 95616
b Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware 19711
1 To whom correspondence should be addressed. E-mail rwmichelmore{at}ucdavis.edu; fax 530-752-9659
The Arabidopsis genome contains 200 genes that encode proteins with similarity to the nucleotide binding site and other domains characteristic of plant resistance proteins. Through a reiterative process of sequence analysis and reannotation, we identified 149 NBS-LRRencoding genes in the Arabidopsis (ecotype Columbia) genomic sequence. Fifty-six of these genes were corrected from earlier annotations. At least 12 are predicted to be pseudogenes. As described previously, two distinct groups of sequences were identified: those that encoded an N-terminal domain with Toll/Interleukin-1 Receptor homology (TIR-NBS-LRR, or TNL), and those that encoded an N-terminal coiled-coil motif (CC-NBS-LRR, or CNL). The encoded proteins are distinct from the 58 predicted adapter proteins in the previously described TIR-X, TIR-NBS, and CC-NBS groups. Classification based on protein domains, intron positions, sequence conservation, and genome distribution defined four subgroups of CNL proteins, eight subgroups of TNL proteins, and a pair of divergent NL proteins that lack a defined N-terminal motif. CNL proteins generally were encoded in single exons, although two subclasses were identified that contained introns in unique positions. TNL proteins were encoded in modular exons, with conserved intron positions separating distinct protein domains. Conserved motifs were identified in the LRRs of both CNL and TNL proteins. In contrast to CNL proteins, TNL proteins contained large and variable C-terminal domains. The extant distribution and diversity of the NBS-LRR sequences has been generated by extensive duplication and ectopic rearrangements that involved segmental duplications as well as microscale events. The observed diversity of these NBS-LRR proteins indicates the variety of recognition molecules available in an individual genotype to detect diverse biotic challenges.
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Y. Zhang and X. Li
A Putative Nucleoporin 96 Is Required for Both Basal Defense and Constitutive Resistance Responses Mediated by suppressor of npr1-1,constitutive 1
PLANT CELL,
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A. Al-Daoude, M. de Torres Zabala, J.-H. Ko, and M. Grant
RIN13 Is a Positive Regulator of the Plant Disease Resistance Protein RPM1
PLANT CELL,
March 1, 2005;
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Z. Xie, Z.-L. Zhang, X. Zou, J. Huang, P. Ruas, D. Thompson, and Q. J. Shen
Annotations and Functional Analyses of the Rice WRKY Gene Superfamily Reveal Positive and Negative Regulators of Abscisic Acid Signaling in Aleurone Cells
Plant Physiology,
January 1, 2005;
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M. A. AYLIFFE and E. S. LAGUDAH
Molecular Genetics of Disease Resistance in Cereals
Ann. Bot.,
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A. J. Heidel, J. D. Clarke, J. Antonovics, and X. Dong
Fitness Costs of Mutations Affecting the Systemic Acquired Resistance Pathway in Arabidopsis thaliana
Genetics,
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S. Bieri, S. Mauch, Q.-H. Shen, J. Peart, A. Devoto, C. Casais, F. Ceron, S. Schulze, H.-H. Steinbiss, K. Shirasu, et al.
RAR1 Positively Controls Steady State Levels of Barley MLA Resistance Proteins and Enables Sufficient MLA6 Accumulation for Effective Resistance
PLANT CELL,
December 1, 2004;
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[Abstract]
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H. Kuang, S.-S. Woo, B. C. Meyers, E. Nevo, and R. W. Michelmore
Multiple Genetic Processes Result in Heterogeneous Rates of Evolution within the Major Cluster Disease Resistance Genes in Lettuce
PLANT CELL,
November 1, 2004;
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[Abstract]
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D. E. Hill, M. A. Brasch, A. A. del Campo, L. Doucette-Stamm, J. I. Garrels, J. Glaven, J. L. Hartley, J. R. Hudson Jr., T. Moore, and M. Vidal
Academia-Industry Collaboration: An Integral Element for Building "Omic" Resources
Genome Res.,
October 1, 2004;
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S. Xiao, B. Emerson, K. Ratanasut, E. Patrick, C. O'Neill, I. Bancroft, and J. G. Turner
Origin and Maintenance of a Broad-Spectrum Disease Resistance Locus in Arabidopsis
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C. Lurin, C. Andres, S. Aubourg, M. Bellaoui, F. Bitton, C. Bruyere, M. Caboche, C. Debast, J. Gualberto, B. Hoffmann, et al.
Genome-Wide Analysis of Arabidopsis Pentatricopeptide Repeat Proteins Reveals Their Essential Role in Organelle Biogenesis
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August 1, 2004;
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J. R. Bretz and S. W. Hutcheson
Role of Type III Effector Secretion during Bacterial Pathogenesis in Another Kingdom
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July 1, 2004;
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M. A. Graham, K. A.T. Silverstein, S. B. Cannon, and K. A. VandenBosch
Computational Identification and Characterization of Novel Genes from Legumes
Plant Physiology,
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R. W. Innes
Guarding the Goods. New Insights into the Central Alarm System of Plants
Plant Physiology,
June 1, 2004;
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M. Tor, D. Brown, A. Cooper, A. Woods-Tor, K. Sjolander, J. D.G. Jones, and E. B. Holub
Arabidopsis Downy Mildew Resistance Gene RPP27 Encodes a Receptor-Like Protein Similar to CLAVATA2 and Tomato Cf-9
Plant Physiology,
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S.-H. Shiu, W. M. Karlowski, R. Pan, Y.-H. Tzeng, K. F. X. Mayer, and W.-H. Li
Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice
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May 1, 2004;
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S. Yang and J. Hua
A Haplotype-Specific Resistance Gene Regulated by BONZAI1 Mediates Temperature-Dependent Growth Control in Arabidopsis
PLANT CELL,
April 1, 2004;
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X. Dong
The Role of Membrane-Bound Ankyrin-Repeat Protein ACD6 in Programmed Cell Death and Plant Defense
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M. Zhu, F. Shao, R. W. Innes, J. E. Dixon, and Z. Xu
The crystal structure of Pseudomonas avirulence protein AvrPphB: A papain-like fold with a distinct substrate-binding site
PNAS,
January 6, 2004;
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[Abstract]
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U. Kolukisaoglu, S. Weinl, D. Blazevic, O. Batistic, and J. Kudla
Calcium Sensors and Their Interacting Protein Kinases: Genomics of the Arabidopsis and Rice CBL-CIPK Signaling Networks
Plant Physiology,
January 1, 2004;
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C. Feuillet, S. Travella, N. Stein, L. Albar, A. Nublat, and B. Keller
Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome
PNAS,
December 9, 2003;
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[Abstract]
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Y. Zhang, S. Goritschnig, X. Dong, and X. Li
A Gain-of-Function Mutation in a Plant Disease Resistance Gene Leads to Constitutive Activation of Downstream Signal Transduction Pathways in suppressor of npr1-1, constitutive 1
PLANT CELL,
November 1, 2003;
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B. Boisson, C. Giglione, and T. Meinnel
Unexpected Protein Families Including Cell Defense Components Feature in the N-Myristoylome of a Higher Eukaryote
J. Biol. Chem.,
October 31, 2003;
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N. A. Eckardt and R. Innes
Resistance Rodeo: Rounding up the Full Complement of Arabidopsis NBS-LRR Genes
PLANT CELL,
April 1, 2003;
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