Skip to main content
SpringerLink
Log in

Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Many plant disease resistance genes (R-genes) encode proteins characterized by the presence of a nucleotide-binding site (NBS) and a leucine-rich repeat (LRR) region and occur in clusters of related genes in plant genomes. One such gene, Mi-1, confers isolate-specific resistance against root-knot nematodes, aphids and whiteflies in cultivated tomato, Solanum lycopersicon. The DNA region carrying Mi-1 and six closely related sequences was introgressed into tomato from Solanum peruvianum in the 1940s. For both susceptible and resistant tomato, Mi-1 homologues are present in two clusters with 3 and 4 copies each on the short arm of chromosome 6. Two homologues from each source are pseudogenes, and one homologue from each source encodes a truncated product. DNA sequence identity among the homologues including the truncated genes, but excluding the pseudogenes, ranges from 92.9 to 96.7%. All the non-pseudogene homologues are transcribed. Comparison of homologues suggests that extensive sequence exchange has occurred. Regions of diversifying selection are present in the ARC2 domain of the NBS region and dispersed throughout the LRR region, suggesting that these regions are possible locations of specificity determinants. Other sequences in the introgressed region have similarity to the Arabidopsis auxin-receptor protein TIR1, a jumonji-like transcription factor and a Na+/H+ antiporter. Analysis of sequences flanking the Mi-1-homologues reveals blocks of homology, but complex differences in arrangement of these blocks when susceptible and resistant genotypes are compared indicating that the region has undergone considerable rearrangement during evolution, perhaps contributing to evolution of specificity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Albrecht M, Takken FLW (2005) Update on the domain architectures of NLRs and R proteins. Biochem Biophys Res Commun 339:459–462

    Article  PubMed  CAS  Google Scholar 

  • Ammiraju JSS, Veremis JC, Huang X, Roberts PA, Kaloshian I (2003) The heat-stable, root-knot nematode resistance gene Mi-9 from Lycopersicon peruvianum is localized on the short arm of chromosome 6. Theor Appl Genet 106:478–484

    PubMed  CAS  Google Scholar 

  • Ayliffe MA, Collins NC, Ellis JG, Pryor A. (2000) The maize rp1 rust resistance gene identifies homologues in barley that have been subject to diversifying selection. Theor Appl Genet 100:1144–1154

    Article  CAS  Google Scholar 

  • Bai Y, van der Hulst R, Bonnema G, Marcel TC, Meijer-Dekens F, Niks RE, Lindhout P (2005) Tomato defense to Oidium neolycopersici: dominant Ol genes confer isolate-dependent resistance via a different mechanism than recessive ol-2. Mol Plant Microbe Interact 18:354–362

    PubMed  CAS  Google Scholar 

  • Ballvora A, Ercolano MR, Weiss J, Meksem K, Bormann CA, Oberhagemann P, Salamini F, Gebhardt C (2002) The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J 30:361–371

    Article  PubMed  CAS  Google Scholar 

  • Banerjee D, Zhang X, Bent AF (2001) The leucine-rich repeat domain can determine effective interaction between RPS2 and other host factors in Arabidopsis RPS2-mediated diseases resistance. Genetics 158:439–450

    PubMed  CAS  Google Scholar 

  • Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 7:391–399

    Article  PubMed  CAS  Google Scholar 

  • Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292:2281–2285

    Article  PubMed  CAS  Google Scholar 

  • Bittner-Eddy PD, Crute IR, Holub EB Beynon JL (2000) RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J 21:177–188

    Article  PubMed  CAS  Google Scholar 

  • Bohs L, Olmstead RG (1997) Phylogenetic relationships in Solanum (Solanaceae) based on ndhF sequences. Syst Bot 22:5–17

    Article  Google Scholar 

  • Brommonschenkel SH, Frary A, Frary A, Tanksley SD (2000) The broad-spectrum tospovirus resistance gene Sw-5 of tomato is a homolog of the root-knot nematode resistance gene Mi. Mol Plant Microbe Interact 13:1130–1138

    PubMed  CAS  Google Scholar 

  • Cannon SB, Zhu HY, Baumgarten AM, Spangler R, May G, Cook DR, Young ND (2002) Diversity, distribution, and ancient taxanomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. J Mol Evol 54:548–562

    Article  PubMed  CAS  Google Scholar 

  • Chisholm S, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  PubMed  CAS  Google Scholar 

  • Collier R, Fuchs B, Walter N, Lutke WK, Taylor CG (2005) Ex vitro composite plants: an inexpensive, rapid method for root biology. Plant J 43:449–457

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dhamasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Dinesh-Kumar SP, Baker BJ (2000) Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc Natl Acad Sci USA 97:1908–13

    Article  PubMed  CAS  Google Scholar 

  • Dixon MS, Jones DA, Hatzixanthis K, Ganal MW, Tanksley SD, Jones JDG (1995) High resolution mapping of the physical location of the tomato Cf-2 gene. Mol Plant Microbe Interact 8:200–206

    PubMed  CAS  Google Scholar 

  • Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JDG (1998) The tomato Cf-5 disease resistance gene and six homologues show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10:1915–1925

    Article  PubMed  CAS  Google Scholar 

  • Dodds P, Lawrence G, Ellis J (2001) Six amino acid changes confined to the leucine-rich repeat beta-strand/beta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13:163–178

    Article  PubMed  CAS  Google Scholar 

  • Dodds PN, Lawrence GJ, Catanzariti A, Teh T, Wang CA, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103:8888–8893

    Article  PubMed  CAS  Google Scholar 

  • Ellis J, Dodds P, Prior T (2000) The generation of plant disease resistance gene specificities. Trends Plant Sci 5:373–379

    Article  PubMed  CAS  Google Scholar 

  • Ernst K, Kumar A, Krisleit D, Kloos DU, Phillips MS, Ganal MW (2002) Broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31:127–136

    Article  PubMed  CAS  Google Scholar 

  • Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci USA 99:11519–11524

    Article  PubMed  CAS  Google Scholar 

  • Ganal MW, Tanksley SD (1996) Recombination around the Tm2a and Mi resistance genes in different crosses of Lycopersicon peruvianum. Theor Appl Genet 92:101–108

    Article  CAS  Google Scholar 

  • Gebhardt C, Valkonen JPT (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102

    Article  PubMed  CAS  Google Scholar 

  • Goggin FL, Shah G, Williamso VM, Ullman DE (2004) Developmental regulation of Mi-mediated aphid resistance is independent of Mi-1.2 transcript levels. Mol Plant Microbe Interact 17:532–536

    PubMed  CAS  Google Scholar 

  • Ho J-Y, Weide R, Ma HM, Wordragen MF, Lambert KN, Koornneef M, Zabel P, Williamson VM (1992) The root-knot nematode resistance gene (Mi) in tomato: Construction of a molecular linkage map and identification of dominant cDNA markers in resistant genotypes. Plant J 2:971–982

    PubMed  CAS  Google Scholar 

  • Holt BF, Hubert DA Dangl JL (2003) Resistance gene signaling in plants—complex similarities to animal innate immunity. Curr Opin Immun 15:20–25

    Article  CAS  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Ann Rev Phytopathol 39:285–312

    Article  CAS  Google Scholar 

  • Hwang CF, Williamson VM (2003) Leucine-rich repeat mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi. Plant J 34:585–593

    Article  PubMed  CAS  Google Scholar 

  • Kaloshian I, Yaghoobi J, Liharska T, Hontelez J, Hanson D, Hogan P, Jesse T, Wijbrandi J, Simons G, Vos P, Zabel P, Williamson VM (1998) Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Mol Gen Genet 257:376–385

    Article  PubMed  CAS  Google Scholar 

  • Korber B (2000) HIV signature and sequence variation analysis. In: Rodrigo AG, Learn GH (eds) Computational analysis of HIV molecular sequences. Kluwer, Dordrecht, pp 55–72

    Google Scholar 

  • Kuang H, Woo S-S, Meyers BC, Nevo E, Michelmore RW (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–2894

    Article  PubMed  CAS  Google Scholar 

  • Kuang H, Wei F, Marano MR, Wirtz U, Wang X, Liu J, Shum WP, Zaborsky J, Tallon LJ, Rensink W, Lobst S, Zhang P, Tornqvst CE, Tek A, Bamberg J, Helgeson J, Fry W, You F, Luo M-C, Jiang J, Buell CR, Baker B (2005) The R1 resistance gene cluster contains three groups of independently evolving, type R1 homologues and shows substantial structural variation among haplotypes of Solanum demissum. Plant J 44:37–51

    Article  PubMed  CAS  Google Scholar 

  • Kuang H, Ochoa OE, Nevo E, Michelmore RW (2006) The disease resistance gene Dm3 is infrequent in natural populations of Lactuca serriola due to deletions and frequent gene conversions at the RGC2 locus. Plant J 47:38–48

    Article  PubMed  CAS  Google Scholar 

  • Leipe DD, Koonin EV, Aravind L (2004) STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 343:1–28

    Article  PubMed  CAS  Google Scholar 

  • Liharska TB, Koornneef M, van Wordragen M, van Kammen A, Zabel P (1996) Tomato chromosome 6: effect of alien chromosomal segments on recombinant frequencies. Genome 39:485–491

    CAS  PubMed  Google Scholar 

  • Martinez de Ilarduya O, Kaloshian I (2001) Mi-1.2 transcripts accumulate ubiquitously in resistant Lycopersicon esculentum. J Nematol 33:116–120

    Google Scholar 

  • Mestre P, Baulcombe DC (2006) Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:491–501

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW (1998) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 11:1833–1846

    Article  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    Article  PubMed  CAS  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    Article  PubMed  CAS  Google Scholar 

  • Moffett P, Farmham G, Peart JR, Baulcombe DC (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J 21:4511–4519

    Article  PubMed  CAS  Google Scholar 

  • Mondragon-Palomino M, Gaut BS (2005) Gene conversion and the evolution of three leucine-rich repeat gene families in Arabidopsis thaliana. Mol Biol Evol 22:2444–2456

    Article  PubMed  CAS  Google Scholar 

  • Mondragon-Palomino M, Meyers BC, Michelmore RW, Gaut BS (2002) Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res 12:1305–1315

    Article  PubMed  CAS  Google Scholar 

  • Moreau P, Thoquet P, Oivier J, Laterrot H, Grimsley N (1998) Genetic mapping of Ph-2, a single locus controlling partial resistance to Phythophtora infestans in tomato. Mol Plant Microbe Interact 11:259–269

    CAS  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    PubMed  CAS  Google Scholar 

  • Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW NEWS 4:14

    Google Scholar 

  • Nombela G, Williamson VM, Muniz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol Plant Microbe Interact 16:645–649

    PubMed  CAS  Google Scholar 

  • Parrella G, Moretti A, Gognalons P, Lesage M-L, Marchoux G, Gebre-Selassie K, Caranta C (2004) The Am gene controlling resistance to Alfalfa mosaic virus in tomato is located in the cluster of dominant resistance genes on chromosome 6. Phytopathol 94:345–350

    CAS  Google Scholar 

  • Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC (2005) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr Biol 15:968–973

    Article  PubMed  CAS  Google Scholar 

  • Rairdan GJ, Moffett P (2006) Distinct domains of the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18:2082–2093

    Article  PubMed  CAS  Google Scholar 

  • Rossi M, Goggin F, Milligan SB, Kaloshian I, Ullman D, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95:9750–9754

    Article  PubMed  CAS  Google Scholar 

  • Ruegger M, Dewe E, Grey WM, Hobbie L, Turner J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes Dev 12:198–207

    PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–25

    PubMed  CAS  Google Scholar 

  • Salmeron JM, Oldroyd GED, Rommens CMT, Scofield SR, Kim HS, Lavelle DT, Dahlbeck D, Staskawicz BJ (1996) 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. Cell 86:123–133

    Article  PubMed  CAS  Google Scholar 

  • Schulte D, Cai DG, Kleine M, Fan LJ, Wang S, Jung C (2006) A complete physical map of a wild beet (Beta procumbens) translocation in sugar beet. Mol Gen Genomics 275:504–511

    Article  CAS  Google Scholar 

  • Seah S, Yaghoobi J, Rossi M, Gleason CA, Williamson VM (2004) The nematode-resistance gene, Mi-1, is associated with an inverted chromosomal segment in susceptible compared to resistant tomato. Theor Appl Genet 108:1635–1642

    Article  PubMed  CAS  Google Scholar 

  • Smith PG (1944) Embryo culture of a tomato species hybrid. Proc Am Soc Hort Sci 44:413–416

    Google Scholar 

  • Sun XL, Cao YL, Wang SP (2006) Point mutations with positive selection were a major force during the evolution of a receptor-kinase resistance gene family of rice. Plant Physiol 140:998–1008

    Article  PubMed  CAS  Google Scholar 

  • Takken FLW, Albrecht M, Tameling WIL (2006) Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9:383–390

    Article  PubMed  CAS  Google Scholar 

  • Tameling WI., Elzinga SDJ, Darmin PS, Vossen JH, Takken FLW, Haring MA, Cornelissen BJC (2002) The tomato R gene products I-2 and Mi-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14:2929–2939

    Article  PubMed  CAS  Google Scholar 

  • Thoquet P, Oliver J, Sperisen C, Rogowsky P, Laterrot H, Grimsley N (1996) Quantitative trait loci determining resistance to bacterial wilt in tomato cultivar Hawaii. Mol Plant-Microbe Interact 9:826–836

    CAS  Google Scholar 

  • Valentine T, Shaw J, Blok VC, Phillips MS, Oparka KJ, Lacomme C (2004) Efficient virus-induced gene silencing in roots using a modified tobacco rattle virus vector. Plant Physiol 136:3999–4009

    Article  PubMed  CAS  Google Scholar 

  • van der Biezen E, Jones J (1998) The NB-ARC domain: a novel signaling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8:R226–R227

    Article  PubMed  Google Scholar 

  • Van der Vossen EAG, Gros J, Sikkema A, Muskens M, Wouters D, Wolters P, Pereira A, Allefs S (2005) The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homologue conferring broad-spectrum late blight resistance in potato. Plant J 44:208–222

    Article  PubMed  CAS  Google Scholar 

  • Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M, Fierens-Onstenk J, de Both M, Peleman J, Liharska T, Hontelez J, Zabeau M (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotech 16:1365–1369

    Article  CAS  Google Scholar 

  • Warren RF, Henk A, Mowery P, Holub E Innes RW (1998) A mutation within the leucine-rich-repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10:1439–1452

    Article  PubMed  CAS  Google Scholar 

  • Wei F, Wing RA, Wise RP (2002) Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14:1903–1917

    Article  PubMed  CAS  Google Scholar 

  • Witte CP, Le QH, Bureau T, Kumar A (2001) Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci USA 98:13778–13783

    Article  PubMed  CAS  Google Scholar 

  • Zamir D, Ekstein-Michelson I, Zakay Y, Navot N, Zeidan M, Sarfatti M, Eshed Y, Harel E, Pleban T, van-Oss H, Kedar N, Rabinowitch HD, Czosnek H (1994) Mapping and introgression of a tomato yellow leaf curl virus tolerance gene, TY-1. Theor Appl Genet 88:141–146

    Article  CAS  Google Scholar 

  • Zhong XB, Bodeau J, Fransz PF, Williamson VM, van Kammen A, de Jong JH, Zabel P (1999) FISH to meiotic pachytene chromosomes of tomato locates the root knot nematode resistance gene Mi-1 and the acid phosphatase gene Aps-1 near the junction of euchromatin and pericentromeric heterochromatin of chromosome arms 6S and 6L, respectively. Theor Appl Genet 98:365–370

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank John Gardner for sequencing carried out at CEPRAP. This research was supported by the US Department of Agriculture National Research Initiative Cooperative State Research, Education and Extension Service grant (# 2000–35300–9410), the National Science Foundation award (IBN-9723679) to V.M.W., and NSF Cooperative Agreement BIR-8920216 to CEPRAP, an NSF Science and Technology Center.

Author information

Authors and Affiliations

  1. CSIRO Entomology, Private Bag 5, Wembley, WA, 6913, Australia

    Stuart Seah

  2. Department of Nematology, University of California, One Shields Avenue, Davis, CA, 95616, USA

    Adam C. Telleen & Valerie M. Williamson

Authors
  1. Stuart Seah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam C. Telleen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valerie M. Williamson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valerie M. Williamson.

Additional information

Communicated by M. Xu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seah, S., Telleen, A.C. & Williamson, V.M. Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues. Theor Appl Genet 114, 1289–1302 (2007). https://doi.org/10.1007/s00122-007-0519-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-007-0519-z

Keywords

Search

Navigation