Two different CC-NBS-LRR genes are required for Lr10-mediated leaf rust resistance in tetraploid and hexaploid wheat

Plant Journal

Volumn 60, Issue 6, 2009, Pages 1043-1054

  Loutre, Caroline ^a   Wicker, Thomas ^a   Travella, Silvia ^a,f   Galli, Paolo ^a,d   Scofield, Steve ^b   Fahima, Tzion ^c   Feuillet, Catherine ^b,e   Keller, Beat ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF HAIFA   (Israel)

^d ETH ZURICH   (Switzerland)

^e Diversity and Ecophysiology of Cereals   (France)

^f European Platform for Rehabilitation   (Belgium)

Author keywords

Diversifying selection; Leucine zipper; Resistance gene analog; Resistance gene evolution; Tetraploid wheat; Virus induced gene silencing

Indexed keywords

PLANT DNA;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; DNA SEQUENCE; GENE SILENCING; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; INNATE IMMUNITY; METABOLISM; MOLECULAR GENETICS; PLANT DISEASE; PLANT GENE; POLYPLOIDY; SEQUENCE ALIGNMENT; WHEAT;

ALLELES; AMINO ACID SEQUENCE; DNA, PLANT; GENE SILENCING; GENES, PLANT; GENETIC VARIATION; IMMUNITY, INNATE; MOLECULAR SEQUENCE DATA; PLANT DISEASES; POLYPLOIDY; SELECTION, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TRITICUM;

TRITICUM AESTIVUM;

EID: 71749115155     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.04024.x     Document Type: Article

References (49)

1. Ade, J., DeYoung, B.J., Golstein, C. Innes, R.W. (2007) Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc. Natl Acad. Sci. USA, 104, 2531 2536.
2. Ashikawa, I., Hayashi, N., Yaman, H., Kanamori, H., Wu, J., Matsumoto, T., Ono, K. Yano, M. (2008) Two adjacent nucleotide-binding site-leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics, 180, 2267 2276.
3. Ayliffe, M.A., Frost, D.V., Finnegan, E.J., Lawrence, G.J., Anderson, P.A. Ellis, J.G. (1999) Analysis of alternative transcripts of the flax L6 rust resistance gene. Plant J. 17, 287 292.
4. Baum, M., Lagudah, E.S. Appels, R. (1992) Wide crosses in cereals. Annu. Rev. Plant Biol. 43, 117 143.
5. Bent, A.F. Mackey, D. (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399 436.
6. Bieri, S., Mauch, S., Shen, Q.H. et al. (2004) RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance. Plant Cell, 16, 3480 3495.
7. Burch-Smith, T.M., Schiff, M., Caplan, J.L., Tsao, J., Czymmek, K. Dinesh-Kumar, S.P. (2007) A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol. 5, e68.
8. Cloutier, S., McCallum, B.D., Loutre, C., Banks, T.W., Wicker, T., Feuillet, C., Keller, B. Jordan, M.C. (2007) Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol. Biol. 65, 93 106.
9. DeYoung, B.J. Innes, R.W. (2007) The rules of engagement. The XIII International Congress on Molecular Plant-Microbe Interactions, Sorrento, Italy, July 2007. New Phytol. 176, 506 510.
10. Dodds, P.N., Lawrence, G.J. Ellis, J.G. (2001) Six amino acid changes confined to the leucine-rich repeat beta-strandbeta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell, 13, 163 178.
11. Eitas, T.K., Nimchuk, Z.L. Dangl, J.L. (2008) Arabidopsis TAO1 is a TIR-NB-LRR protein that contributes to disease resistance induced by the Pseudomonas syringae effector AvrB. Proc. Natl Acad. Sci. USA, 105, 6475 6480.
12. Feuillet, C., Travella, S., Stein, N., Albar, L., Nublat, A. Keller, B. (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc. Natl Acad. Sci. USA, 100, 15253 15258.
13. Feuillet, C., Langridge, P. Waugh, R. (2008) Cereal breeding takes a walk on the wild side. Trends Genet. 24, 24 32.
14. Holzberg, S., Brosio, P., Gross, C. Pogue, G.P. (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J. 30, 315 327.
15. Isidore, E., Scherrer, B., Chalhoub, B., Feuillet, C. Keller, B. (2005) Ancient haplotypes resulting from extensive molecular rearrangements in the wheat A genome have been maintained in species of three different ploidy levels. Genome Res. 15, 526 536.
16. Jiang, H., Wang, C., Ping, L., Tian, D. Yang, S. (2007) Pattern of LRR nucleotide variation in plant resistance genes. Plant Science, 173, 253 261.
17. Jones, J.D. Dangl, J.L. (2006) The plant immune system. Nature, 444, 323 329.
18. Jones, D. Jones, J.D. (1997) The role of leucine-rich repeat proteins in plant defenses. Adv. Bot. Res. 24, 89 167.
19. Kuang, H., Woo, S.S., Meyers, B.C., Nevo, E. Michelmore, R.W. (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster Disease resistance genes in lettuce. Plant Cell, 16, 2870 2894.
20. Lee, S.-K., Song, M.-Y., Seo, Y.-S. et al. (2009) Rice Pi5-mediated resistance to Magnaporthe oryzae requires the presence of two coiled-coil-nucleotide-binding-leucine-rich repeat genes. Genetics, 181, 1627 1638.
21. Luck, J.E., Lawrence, G.J., Dodds, P.N., Shepherd, K.W. Ellis, J.G. (2000) Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell, 12, 1367 1378.
22. Lupas, A.N. Gruber, M. (2005) The structure of alpha-helical coiled coils. Adv. Protein Chem. 70, 37 78.
23. Mackey, D., Holt, B.F., Wiig, A. Dangl, J.L. (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell, 108, 743 754.
24. McDowell, J.M. Simon, S.A. (2008) Molecular diversity at the plant-pathogen interface. Dev. Comp. Immunol. 32, 736 744.
25. McIntosh, R.A., Wellings, C.R. Park, R.F. (1995) Wheat Rusts: An Atlas of Resistance Genes. Dordrecht: Kluwer Academic Publishers.
26. Michelmore, R.W. Meyers, B.C. (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8, 1113 1130.
27. Mondragón-Palomino, M., Meyers, B.C., Michelmore, R.W. Gaut, B.S. (2002) Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res. 12, 1305 1315.
28. Noël, L., Moores, T.L., van Der Biezen, E.A., Parniske, M., Daniels, M.J., Parker, J.E. Jones, J.D. (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell, 11, 2099 2112.
29. Parniske, M., Hammond-Kosack, K.E., Golstein, C., Thomas, C.M., Jones, D.A., Harrison, K., Wulff, B.B. Jones, J.D. (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-49 locus of tomato. Cell, 91, 821 832.
30. Peart, J.R., Mestre, J., P., Lu.R., Malcuit, I. Baulcombe, D. (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.
31. Peleg, Z., Fahima, T., Abbo, S., Krugman, T., Nevo, E., Yakir, D. Saranga, Y. (2005) Genetic diversity for drought resistance in wild emmer wheat and its ecogeographical associations. Plant Cell Environ. 28, 176 191.
32. Qiu, J.W., Schürch, A.C., Yahiaoui, N., Dong, L.L., Fan, H.J., Zhang, Z.J., Keller, B. Ling, H.Q. (2007) Physical mapping and identification of a candidate for the leaf rust resistance gene Lr1 of wheat. Theor. Appl. Genet. 115, 159 168.
33. Rairdan, G.J., Collier, S.M., Sacco, M.A., Baldwin, T.T., Boettrich, T. Moffett, P. (2008) The coiled-coil and nucleotide binding domains of the potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell, 20, 739 741.
34. Schachermayr, G.M., Messmer, M.M., Feuillet, C., Winzeler, H., Winzeler, M. Keller, B. (1995) Identification of molecular markers linked to the Agropyron elongatum-derived leaf rust resistance gene Lr24 in wheat. Theor. Appl. Genet. 90, 982 990.
35. Scherrer, B., Keller, B. Feuillet, C. (2002) Two haplotypes of resistance gene analogs have been conserved during evolution at the leaf rust resistance locus Lr10 in wild and cultivated wheat. Funct. Integr. Genomics, 2, 40 50.
36. Scofield, S.R., Huang, L., Brandt, A.S. Gill, B.S. (2005) Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol. 138, 2165 2173.
37. Shabab, M., Shindo, T., Gu, C., Kaschani, F., Pansuriya, T., Chintha, R., Harzen, A., Colby, T., Kamoun, S. van der Hoorn, R.A. (2008) Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell, 20, 1169 1183.
38. Shen, J., Araki, H., Chen, L., Chen, J.Q. Tian, D. (2006) Unique evolutionary mechanism in R-genes under the presenceabsence polymorphism in Arabidopsis thaliana. Genetics, 172, 1243 1250.
39. Shen, Q.-H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., Seki, H., Uelker, B., Somssich, I.E. Schulze-Lefert, P. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science, 315, 1098 1103.
40. Sinapidou, E., Williams, K., Nott, L., Bahkt, S., Tör, M., Crute, I., Bittner-Eddy, P. Beynon, J. (2004) Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J. 38, 898 909.
41. Smith, S.M. Hulbert, S.H. (2005) Recombination events generating a novel Rp1 race specificity. Mol. Plant Microbe Interact. 18, 220 228.
42. Staal, J., Kaliff, M., Bohman, S. Dixelius, C. (2006) Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J. 46, 218 230.
43. Tian, D., Araki, H., Stahl, E., Bergelson, J. Kreitman, M. (2002) Signature of balancing selection in Arabidopsis. Proc. Natl Acad. Sci. USA, 99, 11525 11530.
44. Van der Hoorn, R.A., Kruijt, M., Roth, R., Brandwagt, B.F., Joosten, M.H. De Wit, P.J. (2001) Intragenic recombination generated two distinct Cf genes that mediate AVR9 recognition in the natural population of Lycopersicon pimpinellifolium. Proc. Natl Acad. Sci. USA, 98, 10493 10498.
45. Wicker, T., Stein, N., Albar, L., Feuillet, C. Schlagenhauf E., Keller.B. (2001) Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J. 26, 307 316.
46. Wicker, T., Yahiaoui, N. Keller, B. (2007) Illegitimate recombination is a major evolutionary mechanism for initiating size variation in plant resistance genes. Plant J. 51, 631 641.
47. Xu, Y., Tao, X., Shen, B., Horng, T., Medzhitov, R., Manley, J.L. Tong, L. (2000) Structural basis for signal transduction by the Tollinterleukin-1 receptor domains. Nature, 408, 111 115.
48. Yahiaoui, N., Brunner, S. Keller, B. (2006) Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J. 47, 85 98.
49. Yahiaoui, N., Kaur, N. Keller, B. (2009) Independent evolution of functional Pm3 resistance genes in wild tetraploid wheat and domesticated bread wheat. Plant J. 57, 846 856.