Phylogeny and genomic organization of the TIR and non-tIR NBS-LRR resistance gene family in Medicago truncatula.

Sequences homologous to the nucleotide binding site (NBS) domain of NBS-leucine-rich repeat (LRR) resistance genes were retrieved from the model legume M. truncatula through several methods. Phylogenetic analysis classified these sequences into TIR (toll and interleukin-1 receptor) and non-TIR NBS subfamilies and further subclassified them into several well-defined clades within each subfamily. Comparison of M. truncatula NBS sequences with those from several closely related legumes, including members of the tribes Trifoleae, Viceae, and Phaseoleae, reveals that most clades contain sequences from multiple legume species. Moreover, sequences from species within the closely related Trifoleae and Viceae tribes (e.g., Medicago and Pisum spp.) tended to be cophyletic and distinct from sequences of Phaseoleae species (e.g., soybean and bean). These results suggest that the origin of major clades within the NBS-LRR family predate radiation of these Papilionoid legumes, while continued diversification of these sequences mirrors speciation within this legume subfamily. Detailed genetic and physical mapping of both TIR and non-TIR NBS sequences in M. truncatula reveals that most NBS sequences are organized into clusters, and few, if any, clusters contain both TIR and non-TIR sequences. Examples were found, however, of physical clusters that contain sequences from distinct phylogenetic clades within the TIR or non-TIR subfamilies. Comparative mapping reveals several blocks of resistance gene loci that are syntenic between M. truncatula and soybean and between M. truncatula and pea.

[1]  E. Radwanski,et al.  Comparative genetics of disease resistance within the solanaceae. , 2000, Genetics.

[2]  B C Meyers,et al.  Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. , 1998, Genome research.

[3]  D. Cook,et al.  Production and characterization of diverse developmental mutants of Medicago truncatula. , 2000, Plant physiology.

[4]  J. Dangl,et al.  La Dolce Vita: A Molecular Feast in Plant–Pathogen Interactions , 1997, Cell.

[5]  R. Wilson,et al.  High throughput fingerprint analysis of large-insert clones. , 1997, Genome research.

[6]  P. Keim,et al.  Rpg1, a soybean gene effective against races of bacterial blight, maps to a cluster of previously identified disease resistance genes , 1998, Theoretical and Applied Genetics.

[7]  C. D. Nickell,et al.  Integration of Rps2, Rmd, and Rj2 Into Linkage Group J of the Soybean Molecular Map , 1994 .

[8]  C. Vallejos,et al.  Disease-resistance related sequences in common bean. , 1999, Genome.

[9]  Jonathan D. G. Jones,et al.  PLANT DISEASE RESISTANCE GENES. , 1997, Annual review of plant physiology and plant molecular biology.

[10]  P. Repetti,et al.  NDR1, a pathogen-induced component required for Arabidopsis disease resistance. , 1997, Science.

[11]  D. Baulcombe,et al.  Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. , 2000, The Plant journal : for cell and molecular biology.

[12]  R. Shoemaker,et al.  Resistance gene analogs are conserved and clustered in soybean. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Grant,et al.  Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[14]  B. Staskawicz,et al.  Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Jonathan D. G. Jones,et al.  Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[16]  T. Bisseling,et al.  Integration of the FISH pachytene and genetic maps of Medicago truncatula. , 2001, The Plant journal : for cell and molecular biology.

[17]  A. Bent,et al.  Plant Disease Resistance Genes: Function Meets Structure. , 1996, The Plant cell.

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

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

[20]  D. Cook,et al.  Construction of a bacterial artificial chromosome library of Medicago truncatula and identification of clones containing ethylene-response genes , 1999, Theoretical and Applied Genetics.

[21]  L. Mao,et al.  The Mla (powdery mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley. , 1999, Genetics.

[22]  D. Leister,et al.  A PCR–based approach for isolating pathogen resistance genes from potato with potential for wide application in plants , 1996, Nature Genetics.

[23]  Y. G. Yu,et al.  Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[25]  D. Cook,et al.  Medicago truncatula--a model in the making! , 1999, Current opinion in plant biology.

[26]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[27]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[28]  R. Michelmore,et al.  The Major Resistance Gene Cluster in Lettuce Is Highly Duplicated and Spans Several Megabases , 1998, Plant Cell.

[29]  R. Michelmore Genomic approaches to plant disease resistance. , 2000, Current opinion in plant biology.

[30]  P. Dodds,et al.  Structure, function and evolution of plant disease resistance genes. , 2000, Current opinion in plant biology.

[31]  S. Dinesh-Kumar,et al.  Signaling in plant-microbe interactions. , 1997, Science.

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

[33]  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.

[34]  P. Ronald,et al.  The evolution of disease resistance genes , 2004, Plant Molecular Biology.

[35]  N. Weeden,et al.  Characterization and linkage mapping of R-gene analogous DNA sequences in pea (Pisum sativum L.) , 2000, Theoretical and Applied Genetics.

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

[37]  N. Young The genetic architecture of resistance. , 2000, Current opinion in plant biology.

[38]  J. Doyle Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria , 1998 .

[39]  J. Parker,et al.  Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  E. Stahl,et al.  Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis , 1999, Nature.

[41]  J. Parker,et al.  Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. , 1996, The Plant cell.

[42]  M. Yano,et al.  Rapid reorganization of resistance gene homologues in cereal genomes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.