Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease

Plant Journal

Volumn 46, Issue 2, 2006, Pages 218-230

  Staal, Jens ^a   Kaliff, Maria ^a   Bohman, Svante ^a,b   Dixelius, Christina ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Callose; Camalexin; Complex trait; Natural variation; QTL; R gene signalling

Indexed keywords

DISEASES; DNA; MAPPING; PLANTS (BOTANY);

CALLOSE; CAMALEXIN; COMPLEX TRAIT; NATURAL VARIATION; R GENE SIGNALING;

GENES;

PLANT DNA; PRIMER DNA;

ARABIDOPSIS; ARTICLE; CROSS BREEDING; FUNGUS; GENE; GENETIC PREDISPOSITION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INBREEDING; INNATE IMMUNITY; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; PATHOGENICITY; PLANT DISEASE; POLYMERASE CHAIN REACTION;

ARABIDOPSIS; CROSSES, GENETIC; DNA PRIMERS; DNA, PLANT; EVOLUTION, MOLECULAR; FUNGI; GENES, PLANT; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, NATURAL; INBREEDING; PLANT DISEASES; POLYMERASE CHAIN REACTION;

CHROMOSOMES; DISEASES; GENES; NUCLEIC ACIDS; PLANTS;

ARABIDOPSIS; LEPTOSPHAERIA MACULANS;

EID: 33646851736     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02688.x     Document Type: Article

References (61)

1. Aarts N. Metz M. Holub E. Staskawicz B.J. Daniels M.J. Parker J.E. 1998 Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl Acad. Sci. USA, 95, 10306 10311.
2. Alonso J.M. Stepanova A.N. Leisse T.J. et al. 2003 Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
3. Alonso-Blanco C. Peeters A.J. Koornneef M. Lister C. Dean C. van den Bosch N. Pot J. Kuiper M.T. 1998 Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant J. 14, 259 271.
4. Austin M.J. Muskett P. Kahn K. Feys B.J. Jones J.D.G. Parker J. 2002 Regulatory role of SGT1 in early R gene-mediated plant defenses. Science, 295, 2077 2080.
5. Azevedo C. Sadanandom A. Kitagawa K. Freialdenhoven A. Shirasu K. Schulze-Lefert P. 2002 The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science, 295, 2073 2076.
6. Balesdent M.H. Barbetti M. Li H. Sivasithamparam K. Gout L. Rouxel T. 2005 Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology, 95, 1061 1071.
7. Bergelson J. Stahl E. Dudek S. Kreitman M. 1998 Genetic variation within and among populations of Arabidopsis thaliana. Genetics, 148, 1311 1323.
8. Bieri S. Mauch S. Shen Q. 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.
9. Blanc G. Wolfe K.H. 2004 Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell, 16, 1679 1691.
10. Bohman S. 2001 Molecular studies of Arabidopsis and Brassica with focus on resistance to Leptosphaeria maculans. PhD Thesis. Agraria q33 305. SLU Press, Uppsala, Sweden.
11. Bohman S. Wang M. Dixelius C. 2002 Arabidopsis thaliana derived resistance against Leptosphaeria maculans in a Brassica napus genomic background. Theor. Appl. Genet. 105, 498 504.
12. Bohman S. Staal J. Thomma B.P.H.J. Wang M. Dixelius C. 2004 Characterisation of an Arabidopsis-Leptosphaeria maculans pathosystem: resistance partially requires camalexin biosynthesis and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J. 37, 9 20.
13. Borevitz J. Nordborg M. 2003 The impact of genomics on the study of natural variation in Arabidopsis. Plant Physiol. 132, 718 725.
14. Borhan H.M. Holub E.B. Beynon J. Rozwadowski K. Rimmer R. 2004 The Arabidopsis TIR-NB-LRR gene RAC1 confers resistance to Albugo candida (white rust) and is dependent on EDS1 but not on PAD4. Mol. Plant Microbe Interact. 7, 711 719.
15. Buell C. Sommerville S. 1997 Use of Arabidopsis recombinant inbred lines reveals a monogenic and a novel digenic resistance mechanism to Xanthomonascampestris pv. campestris. Plant J. 12, 21 29.
16. Collins N. Thordal-Christensen H. Lipka V. et al. 2003 SNARE-protein-mediated disease resistance at the plant cell wall. Nature, 425, 973 977.
17. Cooley M.B. Pothirana S. Wu H.-J. Kachroo P. Klessig D.F. 2000 Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell, 12, 663 676.
18. Delwiche P.A. Williams P.H. 1979 Screening for resistance to blackleg of crucifers in the seedling stage. Cruciferae Newsl. 4, 24.
19. Denby K. Kumar P. Kliebenstein D. 2004 Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. Plant J. 38, 473 486.
20. Desfeux C. Clough S.J. Bent A.F. 2000 Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol. 123, 895 904.
21. Du Q. Thonberg H. Wang J. Whalestedt C. Liang Z. 2005 A systematic analysis of the silencing effects of an active siRNA at all single-nucleotide mismatched target sites. Nucleic Acids Res. 33, 1671 1677.
22. Glazebrook J. Ausubel F.M. 1994 Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc. Natl Acad. Sci. USA, 91, 8955 8959.
23. Gray W.M. Muskett P.R. Chuang H.-W. Parker J. 2003 Arabidopsis SGT1b is required for SCFTIR1-mediated auxin response. Plant Cell, 15, 1310 1319.
24. Gressel J. Michaeli D. Kampel V. Amsellem Z. Warshawsky A. 2002 Ultralow calcium requirements of fungi facilitate use of calcium regulating agents to suppress host calcium-dependent defenses, synergizing infection by a mycoherbicide. J. Agric. Food. Chem. 50, 6353 6360.
25. Hahn J. 2005 Regulation of Nod1 by Hsp90 chaperone complex. FEBS Lett. 579, 4513 4519.
26. Hammond-Kosack K.E. Parker J.E. 2003 Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol. 14, 177 193 Waterhouse P.M. 2002 High-throughput vectors for efficient gene silencing in plants. Funct. Plant Biol. 29, 1217 1225.
27. Howlett B. 2004 Current knowledge of the interaction between Brassica napus and Leptosphaeria maculans. Can. J. Plant Pathol. 26, 245 252.
28. Howlett B. Idnurm A. Pedras M.S.C. 2001 Leptosphaeria maculans, the causal agent of blackleg disease of Brassicas. Fungal Genet. Biol. 33, 1 14.
29. Inohara N. Nuñez G. 2003 NODs: intracellular proteins involved in inflammation and apoptosis. Nat. Rev. Immunol. 3, 371 381 Last R. 2002 Arabidopsis map-based cloning in the post-genome era. Plant Physiol. 129, 440 450.
30. Janssens S. Beyaert R. 2002 A universal role for MyD88 in TLR/IL-1R-mediated signaling. Trends Biochem. Sci. 27, 474 482.
31. Jordan T. Schornack S. Lahaye T. 2002 Alternative splicing of transcripts encoding Toll-like plant resistance proteins - what's the functional relevance to innate immunity Trends Plant Sci. 7, 392 398.
32. Kagan I.A. Hammerschmidt R. 2002 Arabidopsis ecotype variability in camalexin production and reaction to infection by Alternaria brassicicola. J. Chem. Ecol. 28, 2121 2140.
33. Kaneko Y.H. Inukai T. Suehiro N. Natsuaki T. Masuta C. 2004 Fine genetic mapping of the TuNI locus causing systemic veinal necrosis by turnip mosaic virus infection in Arabidopsis thaliana. Theor. Appl. Genet. 110, 33 40.
34. Kitagawa K. Skowyra D. Elledge S.J. Harper J.W. Hieter P. 1999 SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol. Cell, 4, 21 23.
35. Koch E. Slusarenko A. 1990 Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell, 2, 437 445.
36. Koornneef M. Alonso-Blanco C. Vreugdenhil D. 2004 Naturally occurring genetic variation in Arabidopsis thaliana. Annu. Rev. Plant Biol. 55, 142 172 Dean C. 1993 Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J. 4, 745 750.
37. Liu Y. Schiff M. Serino G. Deng X.W. Dinesh-Kumar S.P. 2002 Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to tobacco mosaic virus. Plant Cell, 14, 1483 1496.
38. Manly K.F. Cudmore R.H. Meer J.M. 2001 Map Manager QTX, cross-platform software for genetic mapping. Mamm. Genome, 12, 930 932 Parkin I. 2005 Complexities of chromosome landing in a highly duplicated genome: towards map based cloning of a gene controlling blackleg resistance in Brassica napus. Genetics, 171, 1977 1988.
39. McDowell J.M. Dhandayham M. Long T. Aarts M. Goff S. Holub E.B. Dangl J.L. 1998 Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell, 10, 1861 1874.
40. Mert-Türk F. Bennett M.H. Mansfield J.W. Holub E.B. 2003 Camalexin accumulation in Arabidopsis following abiotic elicitation or inoculation with virulent or avirulent Hyaloperonospora parasitica. Physiol. Mol. Plant Pathol. 62, 137 145.
41. Meyers B.C. Morgante M. Michelmore R.W. 2002 TIR-X and TIR-NB proteins: two new families related to disease resistance TIR-NB-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J. 32, 77 92.
42. Meyers B.C. Kozik A. Griego A. Kuang H. Michelmore R.W. 2003 Genome-wide analysis of NB-LRR-encoding genes in Arabidopsis. Plant Cell, 15, 809 834.
43. Mondragon-Palomino M. Meyers B.C. Michelmore R.W. Gaut B.S. 2002 Patterns of positive selection in the NBS-LRR gene family of Arabidopsis thaliana. Genome Res. 12, 1305 1315.
44. Nimchuk Z. Eulgem T. Holt B.F., III. Dangl J.L. 2003 Recognition and response in the plant immune system. Annu. Rev. Genet. 37, 579 609 Jones J. 1993 Phenotypic characterization and molecular mapping of the Arabidopsis thaliana locus RPP5 determining resistance to Peronospora parasitica. Plant J. 4, 821 831.
45. Parker J.E. Coleman M.J. Szabò V. Frost L.N. Schmidt R. van der Biezen E.A. Moores T. Dean C. Daniels M.J. Jones J.D.G. 1997 The Arabidopsis downy mildew resistance gene RPP5 shares similarities to the Toll and Interleukin-1 receptors with N and L6. Plant Cell, 9, 879 894.
46. Richly E. Kurth J. Leister D. 2002 Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol. Biol. Evol. 19, 76 84.
47. Roetschi A. Azeddine S. Lassaâd B. Mauch F. Mauch-Mani B. 2001 Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signaling. Plant J. 28, 293 305.
48. Rouxel T. Balesdent M.H. 2005 The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol. Plant Pathol. 6, 225 241.
49. Schmid K. Rosleff Sörensen T. Stracke R. Törjék O. Altmann T. Mitchell-Olds T. Weisshaar B. 2003 Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res. 13, 1250 1257.
50. Shirasu K. Schulze-Lefert P. 2003 Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci. 8, 252 258.
51. Sinapidou E. Williams K. Nott L. Bahkt S. Tor 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.
52. Takahashi A. Casais C. Ichimura K. Shirasu K. 2003 HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl Acad. Sci. USA, 100, 11777 11782.
53. Thomma B. Eggermont K. Penninckx I. Mauch-Mani B. Vogelsang R. Cammue B.P.A. Broekaert W.F. 1998 Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl Acad. Sci. USA, 95, 15107 15111.
54. Tiryaki I. Staswick P. 2002 An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol. 130, 887 894.
55. Tör M. Gordon P. Cuzick A. Eulgem T. Inapidou E. Mert-Türk F. Can C. Dangl J.L. Holub E.B. 2002 Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes. Plant Cell, 14, 993 1003.
56. Veronese P. Chen X. Bluhm B. Salmeron J. Dietrich R. Mengiste T. 2004 The BOS loci of Arabidopsis are required for resistance to Botrytis cinerea infection. Plant J. 40, 558 574.
57. Vogel J. Somerville S.C. 2000 Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc. Natl Acad. Sci. USA, 97, 1897 1902.
58. Wang S. Basten C.J. Zeng Z.B. 2004 Windows QTL Cartographer 2.0. Raleigh, NC: Department of Statistics, North Carolina State University.
59. West J.S. Kharbanda P.D. Barbetti M.J. Fitt B.D.L. 2001 Epidemiology and management of Leptosphaeria maculans (Phoma stem canker) on oilseed rape in Australia, Canada and Europe. Plant Pathol. 50, 10 27.
60. Yu F. Lydiate D.J. Rimmer S.R. 2005 Identification of two novel genes for blackleg resistance in Brassica napus. Theor. Appl. Genet. 110, 969 979.
61. Zhang X. Gassmann W. 2003 RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames. Plant Cell, 15, 2333 2342.