Differential expression of the TMV resistance gene N prevents a hypersensitive response in seeds and during germination

Planta

Volumn 237, Issue 3, 2013, Pages 909-915

  Niemeyer, Julia ^a   Ruhe, Jonas ^a   Machens, Fabian ^a   Hehl, Reinhard ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Developmental regulation; HR genes; Hypersensitive response; N gene; PR genes; TMV; Transgenic tobacco

Indexed keywords

NICOTIANA TABACUM; TOBACCO MOSAIC VIRUS;

EID: 84874306269     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-012-1832-6     Document Type: Article

References (33)

1. Abbink TEM, Tjernberg PA, Bol JF, Linthorst HJM (1998) Tobacco mosaic virus helicase domain induces necrosis in N gene-carrying tobacco in the absence of virus replication. Mol Plant Microbe Interact 11: 1242-1246.
2. Becker C, Shutov AD, Nong VH, Senyuk VI, Jung R, Horstmann C, Fischer J, Nielsen NC, Müntz K (1995) Purification, cDNA cloning and characterization of proteinase B, an asparagine-specific endopeptidase from germinating vetch (Vicia sativa L.) seeds. Eur J Biochem 228: 456-462.
3. Benfey PN, Ren L, Chua NH (1990) Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J 9: 1677-1684.
4. Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45: 399-436.
5. Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP (2007) A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol 5: e68.
6. Caplan J, Padmanabhan M, Dinesh-Kumar SP (2008a) Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3: 126-135.
7. Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP (2008b) Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132: 449-462.
8. Czernic P, Huang HC, Marco Y (1996) Characterization of hsr201 and hsr515, two tobacco genes preferentially expressed during the hypersensitive reaction provoked by phytopathogenic bacteria. Plant Mol Biol 31: 255-265.
9. Deblaere R, Bytebier B, De Greve H, Deboeck F, Schell J, van Montagu M, Leemans J (1985) Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Res 13: 4777-4788.
10. Dinesh-Kumar SP, Baker BJ (2000) Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc Nat Acad Sci USA 97: 1908-1913.
11. Dinesh-Kumar SP, Whitham S, Choi D, Hehl R, Corr C, Baker B (1995) Transposon tagging of tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway. Proc Nat Acad Sci USA 92: 4175-4180.
12. Dinesh-Kumar SP, Tham W-H, Baker BJ (2000) Structure-function analysis of the tobacco mosaic virus resistance gene N. Proc Nat Acad Sci USA 97: 14789-14794.
13. Erickson FL, Holzberg S, Calderon-Urrea A, Handley V, Axtell M, Corr C, Baker B (1999) The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. Plant J 18: 67-75.
14. Hammond-Kosack KE, Harrison K, Jones JD (1994) Developmentally regulated cell death on expression of the fungal avirulence gene Avr9 in tomato seedlings carrying the disease-resistance gene Cf-9. Proc Nat Acad Sci USA 91: 10445-10449.
15. Haque A, Sasaki N, Kanegae H, Mimori S, Gao J-S, Nyunoya H (2009) Identification of a Tobacco mosaic virus elicitor-responsive sequence in the resistance gene N. Physiol Mol Plant Pathol 73: 101-108.
16. Hehl R, Baker B (1989) Induced transposition of Ds by a stable Ac in crosses of transgenic tobacco plants. Mol Gen Genet 217: 53-59.
17. Hehl R, Faurie E, Hesselbach J, Salamini F, Whitham S, Baker B, Gebhardt C (1999) TMV resistance gene N homologues are linked to Synchytrium endobioticum resistance in potato. Theor Appl Genet 98: 379-386.
18. Honée G, Melchers LS, Vleeshouwers VG, van Roekel JS, de Wit PJ (1995) Production of the AVR9 elicitor from the fungal pathogen Cladosporium fulvum in transgenic tobacco and tomato plants. Plant Mol Biol 29: 909-920.
19. Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227: 1229-1231.
20. Koyama T, Okada T, Kitajima S, Ohme-Takagi M, Shinshi H, Sato F (2003) Isolation of tobacco ubiquitin-conjugating enzyme cDNA in a yeast two-hybrid system with tobacco ERF3 as bait and its characterization of specific interaction. J Exp Bot 54: 1175-1181.
21. Levy M, Edelbaum O, Sela I (2004) Tobacco mosaic virus regulates the expression of its own resistance gene N. Plant Physiol 135: 2392-2397.
22. Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B (2012) MicroRNA regulation of plant innate immune receptors. Proc Nat Acad Sci USA 109: 1790-1795.
23. Marathe R, Anandalakshmi R, Liu Y, Dinesh-Kumar SP (2002) The tobacco mosaic virus resistance gene, N. Mol Plant Pathol 3: 167-172.
24. Padgett HS, Watanabe Y, Beachy RN (1997) Identification of the TMV replicase sequence that activates the N gene-mediated hypersensitive response. Mol Plant Microbe Interact 10: 709-715.
25. + influx. Proc Natl Acad Sci USA 99: 4079-4084.
26. Schmidt GW, Delaney SK (2010) Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Mol Genet Genomics 283: 233-241.
27. Schornack S, Ballvora A, Gürlebeck D, Peart J, Baulcombe D, Ganal M, Baker B, Bonas U, Lahaye T (2004) The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 37: 46-60.
28. Sugimoto M, Yamaguchi Y, Nakamura K, Tatsumi Y, Sano H (2004) A hypersensitive response-induced ATPase associated with various cellular activities (AAA) protein from tobacco plants. Plant Mol Biol 56: 973-985.
29. Takabatake R, Seo S, Mitsuhara I, Tsuda S, Ohashi Y (2006) Accumulation of the two transcripts of the N gene, conferring resistance to tobacco mosaic virus, is probably important for N gene-dependent hypersensitive cell death. Plant Cell Physiol 47: 254-261.
30. Thangavelu M, Belostotsky D, Bevan MW, Flavell RB, Rogers HJ, Lonsdale DM (1993) Partial characterization of the Nicotiana tabacum actin gene family: evidence for pollen-specific expression of one of the gene family members. Mol Gen Genet 240: 290-295.
31. Ueda H, Yamaguchi Y, Sano H (2006) Direct interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol Biol 61: 31-45.
32. van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44: 135-162.
33. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78: 1101-1115.