Solanaceae Evolutionary Dynamics of the I2-NBS Domain


In Solanaceae family several plant resistant genes to pathogen (R-genes) have been mapped and cloned. Most of them encode Nucleotide Binding Site Leucine Rich Repeat domain (NBS-LRR) protein. However, little is known about the resistance genes variability pattern and the evolutionary process acting on different species belonging to the same family. The aims of the present work, was to genotype and study the evolutionary relationship of fifty wild tomato accessions using the I2 resistance gene sequences. Thirty-three new candidate homologues I2 resistance gene nucleotide sequence were obtained from wild tomato species. Nucleotide polymorphisms in I2-NBS domain was detected in wild tomato species: diversity could have accumulated over a long time and species sorting could have produced new variants. In order to study the NBS-LRR domain variability we analyzed the evolution process acting on the amino acid sequence. The FEL method (codon Model) based on dN/dS, was used to estimate the presence of positive, negative and neutral selection acting on each codon. The I2-NBS domain sequence data studied seems to be under a general purification process of evolution. However, intermittent bouts of positive selection sites were detected in high variable regions. Phylogenetic analysis conducted within the Solanaceae family shows that the Solanum genus is under a rapid adaptative divergence process and Nicotiana and Capsicum clustered separately; Solanum peruvianum, in particular, displayed to be the most polymorphic specie. These results might be important for the identification of new sources of resistance genes to tomato pathogens.

Share and Cite:

Melito S., Sanseverino W., Carli P., Monti L., Frusciante L., Ercolano MR., "Solanaceae Evolutionary Dynamics of the I2-NBS Domain," American Journal of Plant Sciences, Vol. 3 No. 2, 2012, pp. 283-294. doi: 10.4236/ajps.2012.32034.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] H. H. Flor “Current Status of the Gene-for-Gene Concept,” Annual Review of Phytopathology, Vol. 9, No. 1, 1971, pp. 275-276. doi:10.1146/
[2] J. L. Dangl and J. D. G. Jones, “Plant Pathogens and Integrated Defense Responses to Infection,” Nature, Vol. 411, No. 6839, 2001, pp. 826-833. doi:10.1038/35081161
[3] I. R. Crute, “Gene-for-Gene Recognition in Plant-Pathogen Interactions,” Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, Vol. 346, 1994, pp. 345-49. doi:10.1098/rstb.1994.0151
[4] E. A. Van der Vossen, J. N. Van der Voort, K. Kanyuka, A. Bendahmane, H. Sandbrink, D. C. Baulcombe, J. Bakker, W. J. Stiekema and R. M. Klein-Lankhors, “Homologs of a Single Resistance Gene Cluster in Potato Confer Resistance to Distinct Pathogens: A Virus and a Nematode,” Plant Journal, Vol. 23, No. 5, 2000, pp. 567-76. doi:10.1046/j.1365-313x.2000.00814.x
[5] J. Bai , L. A. Pennill, J. Ning, S. W. Lee, J. Ramalingam, C. A. Webb, B. Zhao, Q. Sun, C. Nelson, J. E. Leach and S. Hulbert, “Diversity in Nucleotide Binding Site-Leucine Rich Repeat Genes in Cereals,” Genome Research, Vol. 12, No. 12, 2002, pp. 1871-1884. doi:10.1101/gr.454902
[6] S. B. Cannon, H. Zhu, A. M. Baumgarten, R. Spangler, G. May, D. R. Cook and N. D. Young, “Diversity, Distribution, and Ancient Taxonomic Relationships within the TIR and Non-TIR NBSLRR Resistance Gene Subfamilies,” Journal of Molecular Evolution, Vol. 54, No. 4, 2002, pp. 548-562. doi:10.1007/s00239-001-0057-2
[7] R. W. Michelmore and B. C. Meyers, “Clusters of Resistance Genes in Plants Evolve by Divergent Selection and a Birth-and-Death Process,” Genome Research, Vol. 8, 1998, pp. 1113-1130.
[8] V. Kanazin, L. F. Marek and R. C. Shoemaker, “Resistance Gene Analogs Are Conserved and Clustered in Soybean,” Proceeding of the National Academy Science of United State of America, Vol. 93, No. 21, 1996, pp. 11746-11750.
[9] B. C. Meyers, A. W. Dickerman, R. W. Michelmore, S. Sivaramakrishnan, B. W. Sobral and N. D. Young, “Plant Disease Resistance Genes Encode Members of an Ancient and Diverse Protein Family within the Nucleotide-Binding Superfamily,” Plant Journal, Vol. 20, No. 3, 1999, pp. 317-332. doi:10.1046/j.1365-313X.1999.t01-1-00606.x
[10] Q. Pan, Y. S. Liu, O. Budai-Hadrian, M. Sela, L. Carmel-Goren, D. Zamir and R. Fluhr, “Comparative Genetics of Nucleotide Binding Site-Leucine Rich Repeat Resistance Gene Homologs in the Genomes of Two Dicotyledons: Tomato and Arabidopsis,” Genetics, Vol. 155, No. 1, 2000, pp. 309-322.
[11] B. Mieslerova, A. Lebeda, Y. S. Chetelat, “Variation in Response of Wild Lycopersicon and Solanum spp. against Tomato Powdery Mildew (Oidium lycopersici),” Journal Phytopathology, Vol. 148, No. 5, 2000, pp. 303-311. doi:10.1046/j.1439-0434.2000.00492.x
[12] H. Laterrot, “Breeding Strategies for Disease Resistance in Tomatoes with Emphasis to the Tropics: Current Status and Research Challenges,” 1st International Symposium Tropical Tomato disease, Recife, 21-22 November 1996, pp. 126-132.
[13] N. Ori, Y. Eshed, I. Paran, G Presting, D. Aviv, S. Tanksley, D. Zamir and R Fluhr, “The I2C Family from the Wilt Disease Resistance Locus I2 Belongs to the Nucleotide Binding, Leucine-Rich Repeat Superfamily of Plant Resistance Genes,” Plant Cell, Vol. 9, No. 4, 1997, pp. 521-32.
[14] G. Simons, J. Groenendijk, J. Wijbrand, M. Reijans, J. Groenen, P. Diergaarde, T. Van der Lee, M. Bleeker, J. Onstenk, M. Both, M. Haring, J. Mes, B. Cornelissen, M. Zabeau and P. Vos, “Dissection of the Fusarium I2 Gene Cluster in Tomato Reveals Six Homologs and One Active Gene Copy,” Plant Cell, Vol. 10, No. 6, 1998, pp. 1055-1068.
[15] S. Huang , V. G. Vleeshouwers, J. S. Werij, R. C. Hutten, H.J. van Eck, R. G. Visser and E. Jacobsen, “The R3 Resistance to Phytophthora infestans in Potato Is Conferred by Two Closely Linked R Genes with Distinct Specificities,” Molecular Plant Microbe Interaction, Vol. 17, No. 4, 2004, pp. 428-435. doi:10.1094/MPMI.2004.17.4.428
[16] I. E. Peralta and D. M. Spooner, “Morphological Characterization and Relationships of Wild Tomatoes (Solanum L. Section Lycopersicon),” Monographs in Systematic Botany from the Missouri Botanical Garden, Vol. 104, 2005, pp. 227-257.
[17] M. T. Fulton, J. Chunwongse and S. D. Tanksley, “Microprep Protocol for Extraction of DNA from Tomato and Other Herbaceous Plants,” Plant Molecular Biology Reporter, Vol. 13, No. 3, 1995, pp. 207-209. doi:10.1007/BF02670897
[18] J. Rozas and R. Rozas, “DNASP Version 3: An Integrated Program for Molecular Population Genetics and Molecular Evolution Analysis,” Bioinformatics, Vol. 15, No. 2, 1999, pp. 174-175. doi:10.1093/bioinformatics/15.2.174
[19] J. D. Thompson, D. G. Higgins and T. J. Gibson, “CLUSTAL W: Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting, Position-Specific Gap Penalties and Weight Matrix Choice,” Nucleic Acid Research, Vol. 22, No. 22, 1994, pp. 4673-4680. doi:10.1093/nar/22.22.4673
[20] T. A. Hall, “BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT,” Nucleic Acids Symposium Series, Vol. 41, 1999, pp. 95-98.
[21] S. Kumar, K. Tamura and M. Nei, “MEGA3: Integrated Software for Molecular Evolutionary Genetics Analysis and Sequence Alignment,” Briefings in Bioinformatics, Vol. 5, No. 2, 2004, pp. 150-163. doi:10.1093/bib/5.2.150
[22] J. Rozas, J. C. Sanchez-DelBarrio, X. Messeguer and R. Rozas, “DnaSP, DNA Polymorphism Analyses by the Coalescent and Other Methods,” Bioinformatics, Vol. 19, No. 18, 2003, pp. 2496-2497. doi:10.1093/bioinformatics/btg359
[23] J. Felsenstein, “Phylip (Phylogeny Inference Package) Version 3.6. Distributed by the Author,” Department of Genomic Sciences, University of Washington, Seattle, 2004.
[24] S. Guindon, F. Lethiec, P. Duroux and O. Gascuel, “Phyml Online—A Web Server for Fast Maximum Likelihood-Based Phylogenetic Inference,” Nucleic Acid Re-search, Vol. 33, 2005, pp. W557-W559. doi:10.1093/nar/gki352
[25] J. A. Cuff, E. Birney, M. E. Clamp and G. J. Barton, “ProtEST: Protein Multiple Sequence Alignments from Expressed Sequence Tags,” Bioinformatics, Vol. 16, No. 2, 2000, pp. 111-116. doi:10.1093/bioinformatics/16.2.111
[26] P. Yang, K. N. Liou, M. I. Mishchenko and B. C. Gao, “Efficient Finite-Difference Time-Domain Scheme for Light Scattering by Dielectric Particles: Application to Aerosols,” Applied Optics, Vol. 39, No. 21, 2000, pp. 3727-3737. doi:10.1364/AO.39.003727
[27] Z. Yang and J. P. Bielawski, “Statistical Methods for Detecting Molecular Evolution,” Trends in Ecology & Evolution, Vol. 15, No. 12, 2000, pp. 496-503. doi:10.1016/S0169-5347(00)01994-7
[28] S. L. Pond and S. D. Frost, “Datamonkey: Rapid Detec-tion of Selective Pressure on Individual Sites of Codon Alignments,” Bioinformatics, Vol. 21, No. 10, 2005, pp. 2531-2533. doi:10.1093/bioinformatics/bti320
[29] K. E. Hammond-Kosack and J. D. G. Jones, “Plant Dis-ease Resistance Genes,” Annual Review of Plant Physi-ology and Plant Molecular Biology, Vol. 48, 1997, pp. 573-605. doi:10.1146/annurev.arplant.48.1.575
[30] W. Sanseverino, G. Roma, M. De Simone, L. Faino, S. Melito, E. Stupka, L. Frusciante and M. R. Ercolano, “PRGdb: A Bioinformatics Platform for Plant Resistance Gene Analysis,” Nucleic Acids Research, Vol. 38, No. 1, 2010, pp. D814-D821. doi:10.1093/nar/gkp978
[31] A. R. Friedman, “The Evolution of Resistance Genes in Multi-Protein Plant Resistance Systems,” Current Opinion in Genetics & Development, Vol. 17, No. 6, 2007, pp. 1-7. doi:10.1016/j.gde.2007.08.014
[32] P. Tiffin and D. A. Moeller, “Molecular Evolution of Plant Immune System Genes,” Trends in Genetics, Vol. 22, No. 12, 2006, pp. 662-670. doi:10.1016/j.tig.2006.09.011
[33] Y. Belkhadir, R. Subramaniam and J. L. Dangl, “Plant Disease Resistance Protein Signaling: NBS–LRR Proteins and Their Partners”, Current Opinion in Plant Biology, Vol. 7, No. 4, 2004, pp. 391-399. doi:10.1016/j.pbi.2004.05.009
[34] B. C. Couch, R. Spangler, C. Ramos and G. May, “Perva-sive Purifying Selection Characterizes the Evolution of I2 Homologs,” Molecular Plant Microbe Interaction, Vol. 19, No. 3, 2006, pp. 288-303. doi:10.1094/MPMI-19-0288
[35] I. E. Peralta and D. M. Spooner, “Classification of Wild Tomatoes: A Review,” Kurtziana, Vol. 28, No. 1, 2000, pp. 45-54.
[36] C. M. Rick, J. F. Fobes and S. D. Tanksley, “Evolution of Mating Systems in Lycopersicon hirsutum as Deduced from Genetic Variation in Electrophoretic and Morphological Characters,” Plant Systematic and Evolution, Vol. 132, 1979, pp. 279-298. doi:10.1007/BF00982390
[37] A. L. Caicedo and B. A Schaal, “Population Structure and Phylogeography of Solanum pimpinellifolium Inferred from a Nuclear Gene,” Molecular Ecology, Vol. 13, No. 7, 2004, pp. 1871-1882. doi:10.1111/j.1365-294X.2004.02191.x
[38] G. Bonnema, D. Schipper, van S. Heusden, P. Lindhout and P. Zabel, “Tomato Chromosome 1: High Resolution Genetic and Physical Mapping of the Short Arm in an In-terspecific Lycopersicon esculentum x L. peruvianum Cross,” Molecular Genomics and Genetics, Vol. 253, 1997, pp. 455-462.
[39] M. B. Sela-Buurlage, O. Budai-Hadrian, Q. Pan, L. Car-mel-Goren, R. Vunsch, D. Zamir and R. Fluhr, “Ge-nome-Wide Dissection of Fusarium Resistance in To-mato Reveals Multiple Complex Loci,” Molecular Ge-netics and Genomics, Vol. 265, No. 6, 2001, pp. 1104-1111. doi:10.1007/s004380100509
[40] K. Roselius, W. Stephan and T. St?dler, “The Relation-ship of Nucleotide Polymorphism, Recombination Rate and Selection in Wild Tomato Species,” Genetics, Vol. 171, No. 2, 2005, pp. 753-763. doi:10.1534/genetics.105.043877
[41] M. Mazurek, E. T. Cirulli, S. M. Collier, L. G. Landry, B. C. Kang, E. A. Quirin, J. M. Bradeen, P. Moffett and M. M. Jahn, “The Fractionated Orthology of Bs2 and Rx/ Gpa2 Supports Shared Synteny of Disease Resistance in the Solanaceae,” Genetics, Vol. 182, 2009, pp. 1351-1364. doi:10.1534/genetics.109.101022
[42] S. Knapp, L. Bohs L., M. Nee and D. M. Spooner, “Comparative and Functional Genomics, Solanaceae a Model for Linking Genomics with Biodiversity,” Com-parative and Functional Genomics, Vol. 5, No. 3, 2004, pp. 285-291. doi:10.1002/cfg.393
[43] J. De Meaux and T. Mitchell-Olds, “Evolution of Plant Resistance at the Molecular Level: Ecological Context of Species Interactions,” Heredity, Vol. 91, No. 4, 2003, pp. 345-352. doi:10.1038/sj.hdy.6800342
[44] S. Kryazhimskiy and J. B. Plotkin, “The Population Ge-netics of dN/dS,” PLoS Genetics, Vol. 4, No. 12, 2008, Article ID: e1000304. doi:10.1371/journal.pgen.1000304
[45] M. Anisimova, J. P. Bielawski and Z. Yang, “Accuracy and Power of Bayes Prediction of Amino Acid Sites under Positive Selection,” Molecular Biology Evolution, Vol. 19, No. 6, 2002, pp. 950-958. doi:10.1093/oxfordjournals.molbev.a004152
[46] A. Devoto, H. A. Hartmann, P. Piffanelli, C. Elliott, C. Simmons, G. Taramino, C. S. Goh, F. E. Cohen, B. C. Emerson, P. Schulze-Lefert and R. Panstruga, “Molecular Phylogeny and Evolution of the Plant-Specific Seven-Transmembrane MLO Family,” Journal of Molecular Evolution, Vol. 56, No. 1, 2003, pp. 77-88. doi:10.1007/s00239-002-2382-5
[47] L. P. Martinez-Castilla and E. R. Alvarez-Buylla, “Adap-tive Evolution in the Arabidopsis MADS Box Gene Fam-ily Inferred from Its Complete Resolved Phylogeny,” Proceeding of the National Academy Science of United State of America, Vol. 100, No. 23, 2003, pp. 13407-13412.
[48] D. O. Niu-Liu, L. Zhang and M. R. Foolad, “Sequence Comparison and Characterization of DNA Fragments Amplified by Resistance Gene Primers in Tomato,” Acta Horticulturae, Vol. 625, 2003, pp. 49-58.
[49] F. Ch. Trognitz and B. R. Trognitz, “Survey of Resistance Gene Analogs in Solanum caripense, a Relative of Potato and Tomato, and Update on R Gene Genealogy,” Molecular Genetics and Genomics, Vol. 274, No. 6, 2005, pp. 595-605. doi:10.1007/s00438-005-0038-z

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.