Powdery mildew-induced Mla mRNAs are alternatively spliced and contain multiple upstream open reading frames

Plant Physiology

Volumn 131, Issue 2, 2003, Pages 558-567

  Halterman, Dennis A ^a   Wei, Fusheng ^a,b,c   Wise, Roger P ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b WESTERN REGIONAL RESEARCH CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; GENES; PROTEINS; RNA;

GENOMIC COPIES;

GENETIC ENGINEERING;

BLUMERIA GRAMINIS; BLUMERIA GRAMINIS F. SP. HORDEI; EMBRYOPHYTA; ERYSIPHALES; FUNGI; HORDEUM; HORDEUM VULGARE; HORDEUM VULGARE SUBSP. VULGARE;

EID: 0347297502     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.014407     Document Type: Article

References (57)

1. Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ, Ellis JG (1997) Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell 9: 641-651
2. Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JDG, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defense. Science 295: 2077-2080
3. Ayliffe MA, Frost DV, Finnegan EJ, Lawrence GJ, Anderson PA, Ellis JG (1999) Analysis of alternative transcripts of the flax L6 rust resistance gene. Plant J 17: 287-292
4. Azevedo C, Sadanandom A, Kitagawa K, Friealdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295: 2073-2076
5. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856-1860
6. Boyd LA, Smith PH, Foster EM, Brown JKM (1995) The effects of allelic variation at the Mla resistance locus in barley on the early development of Erysiphe graminis f. sp. hordei and host responses. Plant J 7: 959-968
7. Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963-1965
8. 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: 1908-1913
9. Ellingboe AH (1972) Genetics and physiology of primary infection by Erysiphe graminis. Phytopathology 62: 401-406
10. Feys BJ, Moisan LJ, Newman MA, Parker JE (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J 20: 5400-5411
11. Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9: 275-296
12. Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843-846
13. Haas BJ, Volfovsky N, Town CD, Troukhan M, Alexandrov N, Feldmann KA, Flavell RB, White O, Salzberg SL (2002) Full-length messenger RNA sequences greatly improve genome annotation. Genome Biol 3: RESEARCH0029
14. Halterman D, Zhou F, Wei F, Wise RP, Schulze-Lefert P (2001) The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. Plant J 25: 335-348
15. Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8: 1773-1791
16. 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 B: 392-398
17. Jørgensen JH (1994) Genetics of powdery mildew resistance in barley. Crit Rev Plant Sci 13: 97-119
18. Jørgensen JH (1996) Effect of three suppressors on the expression of powdery mildew resistance genes in barley. Genome 39: 492-498
19. Kochetov AV, Sirnik OA, Rogosin IB, Glazko GV, Komarova ML, Shumny VK (2002) Contextual features of higher plant mRNA 5′-untranslated regions. Mol Biol 36: 510-516
20. Lawrence G J, Finnegan EJ, Ayliffe MA, Ellis IG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7: 1195-1206
21. Liu Y, Schiff M, Serino G, Deng X-W, Dinesh-Kumar SP (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
22. Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein structures. Science 252: 1162-1164
23. Luukkonen BGM, Tan W, Schwartz S (1995) Efficiency of reinitiation of translation on human immunodeficiency virus type 1 mRNAs is determined by the length of the upstream open reading frame and by intercistronic distance. J Virol 69: 4086-4094
24. Martin GBM, Frary A, Wu T, Brommonschenkel S, Chunwongse J, Earle ED, Tanksley SD (1994) A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell 6: 1543-1552
25. Mignone F, Gissi C, Liuni S, Pesole G (2002) Untranslated regions of mRNAs. Genome Biol 3: REVIEWS0004
26. Morris DR, Geballe AP (2000) Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20: 8635-8642
27. Moseman JG (1972) Isogenic barley lines for reaction to Erysiphe graminis f. sp. hordei. Crop Sci 12: 681-682
28. Muradov A, Petrasovits L, Davidson A, Scott KJ (1993) A cDNA clone for a pathogenesis-related protein 1 from barley. Plant Mol Biol 23: 439-442
29. Muskett PR, Kahn K, Austin MJ, Moisan LJ, Sadanandom A, Shirasu K, Jones JD, Parker JE (2002) Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14: 979-992
30. Neuenschwander U, Lawton K, Ryals J (1996) Systemic acquired resistance In G Stacey and NT Keen, eds, Plant-Microbe Interactions, Vol 1. Chapman and Hall, New York, pp 81-106
31. Parker JE, Coleman MJ, Szabò V, Frost LN, Schmidt R, van der Biezen EA, Moores T, Dean C, Daniels MJ, Jones JDG (1997) The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 9: 879-894
32. Peart JR, Cook G, Feys BJ, Parker JE, Baulcombe DC (2002a) An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus. Plant J 29: 569-579
33. Peart JR, Liu R, Sadanandom A, Malcuit I, Moffett P, Brice DC, Schauser L, Jagard DAW, Xiao S, Coleman MJ et al. (2002b) Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc Natl Acad Sci USA 99: 10865-10869
34. Peterhänsel C, Freialdenhoven A, Kurth J, Kolsch R, Schulze-Lefert P (1997) Interaction analyses of genes required for resistance responses to powdery mildew in barely reveal distinct pathways leading to leaf cell death. Plant Cell 9: 1397-1409
35. Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129: 1076-1085
36. Procissi A, Piazza P, Tonelli C (2002) A maize r1 gene is regulated post-transcriptionally by differential splicing of its leader. Plant Mol Biol 49: 239-248
37. Schulze-Lefert P, Vogel J (2000) Closing the ranks to attack by powdery mildew. Trends Plant Sci 5: 343-348
38. Shen KA, Chin DB, Arroyo-Garcia R, Ochoa OE, Lavelle DO, Wroblewski T, Meyers BC, Michelmore RW (2002) Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol Plant-Microbe Interact 15: 251-261
39. Shirasu K, Lahaye T, Tan M, Zhou F, Azevedo C, Schulze-Lefert P (1999a) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99: 355-366
40. Shirasu K, Nielsen K, Piffanelli P, Oliver R, Schulze-Lefert P (1999b) Cell-autonomous complementation of mlo resistance using a biolistic transient expression system. Plant J 17: 293-299
41. Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JD (1995) Molecular genetics of plant disease resistance. Science 268: 661-667
42. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci USA 96: 14153-14158
43. Tör M, Gordon P, Cuzick A, Eulgem T, Sinapidou E, Mert-Turk F, Can C, Dangl JL, Holub EB (2002) Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes. Plant Cell 14: 993-1003
44. Tornero P, Merritt P, Sadanandom A, Shirasu K, Innes RW, Dangl JL (2002) RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14: 1005-1015
45. van der Biezen EA, Jones JDG (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23: 454-456
46. Varet A, Parker J, Tornero P, Nass N, Nürnberger T, Dangl JL, Scheel D, Lee J (2002) NHL25 and NHL3, two NDR1/HIN1-like genes in Arabidopsis thaliana with potential role(s) in plant defense. Mol Plant-Microbe Interact 15: 605-616
47. Wang G-L, Ruan D-L, Song W-Y, Sideris S, Chen L, Pi LY, Zhang S, Zhang Z, Fauquet C, Gaut BS et al. (1998) Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10: 765-780
48. Wang ZX, Yamanouchi U, Katayose Y, Sasaki T, Yano M (2001) Expression of the Pib rice-blast-resistance gene family is up-regulated by environmental conditions favouring infection and by chemical signals that trigger secondary plant defences. Plant Mol Biol 47: 653-661
49. Wang ZX, Yano M, Yamanouchi U, Iwamoto M, Monna L, Hayasaka H, Katayose Y, Sasaki T (1999) The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J 19: 55-64
50. Wei F, Gobelman-Werner K, Morroll SM, Kurth J, Mao L, Wing R, Leister D, Schulze-Lefert P, Wise RP (1999) 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. Genetics 153: 1929-1948
51. Wei F, Wing R, Wise RP (2002) Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14: 1903-1917
52. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus gene N: similarity to toll and interleukin-1 receptor. Cell 78: 1101-1115
53. Willis AE (1999) Translational control of growth factor and proto-oncogene expression. Int J Biochem Cell Biol 31: 73-86
54. Wise RP (2000) Disease resistance: What's brewing in barley genomics? Plant Dis 84: 1160-1170
55. Wise RP, Ellingboe AH (1983) Infection kinetics of Erysiphe graminis f. sp. hordei on barley with different alleles at the Mla locus. Phytopathology 73: 1220-1222
56. Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano M, Iwata N, Sasaki T (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA 95: 1663-1668
57. Zhou F, Kurth J, Wei F, Elliott C, Valé G, Yahiaoui N, Keller B, Somerville S, Wise R, Schulze-Lefert P (2001) Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1 independent signaling pathway. Plant Cell 13: 337-350