Haplotype variability and identification of new functional alleles at the Rdg2a leaf stripe resistance gene locus

Theoretical and Applied Genetics

Volumn 126, Issue 6, 2013, Pages 1575-1586

  Biselli, Chiara ^a   Urso, Simona ^a   Tacconi, Gianni ^a   Steuernagel, Burkhard ^b,c   Schulte, Daniela ^b,d   Gianinetti, Alberto ^a   Bagnaresi, Paolo ^a   Stein, Nils ^b   Cattivelli, Luigi ^a   Valè, Giampiero ^a  

^a ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c SAINSBURY LABORATORY   (United Kingdom)

^d KWS SAAT SE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HAPLOTYPE VARIABILITY; INTERGENIC REGIONS; MOLECULAR MECHANISM; NUCLEOTIDE DIVERSITY; POLYMORPHIC SITES; POSITIVE SELECTION; RESISTANCE GENES; SEQUENCE CONSERVATION;

AMINO ACIDS; CULTIVATION; DNA SEQUENCES; ENCODING (SYMBOLS); LAKES; NUCLEOTIDES;

GENE ENCODING;

ARTICLE; ASCOMYCETES; CLUSTER ANALYSIS; DISEASE RESISTANCE; DNA SEQUENCE; GENE DELETION; GENE LOCUS; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; HORDEUM; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT DISEASE; POLYMERASE CHAIN REACTION;

ASCOMYCOTA; BASE SEQUENCE; CLUSTER ANALYSIS; DISEASE RESISTANCE; EVOLUTION, MOLECULAR; GENETIC LOCI; GENETIC VARIATION; HAPLOTYPES; HORDEUM; MOLECULAR SEQUENCE DATA; PLANT DISEASES; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION;

HORDEUM; HORDEUM VULGARE; PYRENOPHORA GRAMINEA;

EID: 84878350422     PISSN: 00405752     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00122-013-2075-z     Document Type: Article

References (55)

1. Arru L, Faccini N, Govoni C, Cattivelli L, Pecchioni N, Delogu G, Stanca AM, Valè G (2003a) The PCR-based marker MWG2018 linked to the RDG2A leaf stripe resistance gene is a useful tool for assessing barley resistance in breeding programs. Crop Sci 43: 1036-1042.
2. Arru L, Francia E, Pecchioni N (2003b) Isolate-specific QTLs of resistance to leaf stripe (Pyrenophora graminea) in the Steptoe × Morex spring barley cross. Theor Appl Genet 106: 668-675.
3. Bella J, Hindle KL, McEwan PA, Lovell SC (2008) The leucine-rich repeat structure. Cell Mol Life Sci 65: 2307-2333.
4. Bhullar NK, Streetb K, Mackayc M, Yahiaoui N, Keller B (2009) Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus. Proc Natl Acad Sci USA 106: 9519-9524.
5. Bhullar NK, Zhang Z, Wicker T, Keller B (2010) Wheat gene bank accessions as a source of new alleles of the powdery mildew resistance gene Pm3: a large scale allele mining project. BMC Plant Biol 10: 88.
6. Bieri S, Mauch S, Shen QH, Peart J, Devoto A, Casais C, Ceron F, Schulze S, Steinbiß HH, Shirasu K, Schulze-Lefert P (2004) RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumuation for effective resistance. Plant Cell 16: 3480-3495.
7. Biselli C, Urso S, Bernardo L, Tondelli A, Tacconi G, Martino V, Grando S, Valè G (2010) Identification and mapping of the leaf stripe resistance gene Rdg1a in Hordeum spontaneum. Theor Appl Genet 120: 1207-1218.
8. Bulgarelli D, Collins NC, Tacconi G, Dall'Aglio E, Brueggeman R, Kleinhofs A, Stanca AM, Valè G (2004) High-resolution genetic mapping of the leaf stripe resistance gene Rdg2a in barley. Theor Appl Genet 108: 1401-1408.
9. Bulgarelli D, Biselli C, Collins NC, Consonni G, Stanca AM, Schulze-Lefert P, Valè G (2010) The CC-NB-LRR-type Rdg2a resistance gene confers immunity to the seed-borne barley leaf stripe pathogen in the absence of hypersensitive cell death. PLoS One 5: e12599.
10. Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP (2008) Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132: 449-462.
11. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539-548.
12. Dodds PN, Lawrence GJ, Ellis JG (2001) Six amino acid changes confined to the leucine-rich repeat β-strand/β-turn motif determine the difference between P and P2 rust resistance specificities in flax. Plant Cell 13: 163-178.
13. Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11: 495-506.
14. Gatti A, Rizza F, Delogu G, Terzi V, Porta-Puglia A, Vannacci G (1992) Physical and biochemical variability in a population of Drechslera graminea. J Genet Breed 46: 179-186.
15. Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93: 10274-10279.
16. Glowacki S, Macioszek VK, Kononowicz AK (2011) R proteins as fundamental of plant innate immune system. Cell Mol Biol Lett 16: 1-24.
17. Golzar H (1995) Barley leaf blights in Iran. Rachis 14: 41.
18. Howles P, Lawrence G, Finnegan J, McFadden H, Ayliffe M, Dodds P, Ellis J (2005) Autoactive alleles of the flax L6 rust resistance gene induce nonrace-specific rust resistance associated with hypersensitive response. Mol Plant Microbe Interact 18: 570-582.
19. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19: 4004-4014.
20. Jones DA, Jones JDG (1997) The role of leucine-rich repeat proteins in plant defenses. Adv Bot Res 24: 89-167.
21. Jorgensen JH (1994) Genetics of powdery mildew resistance in barley. Crit Rev Plant Sci 13: 97-119.
22. Kruijt M, Brandwagt BF, de Wit PJM (2004) Rearrangements in the Cf-9 disease resistance gene cluster of wild tomato have resulted in three genes mediate Avr9 responsiveness. Genetics 168: 1655-1663.
23. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33: 479-532.
24. Kumar RG, Sakthivel K, Sundaram RM, Neeraja CN, Balachandran SM, Shobha Rani N, Viraktamath BC, Madhav MS (2010) Allele mining in crops: prospects and potentials. Biotechnol Adv 28: 451-461.
25. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20: 116-122.
26. Liu X, Lin F, Wang L, Pan Q (2007) The in silico map-based cloning of Pi36, a rice Coiled-Coil-Nucleotide-Binding Site-Leucine-Rich Repeat gene that confers race-specific resistance to the blast fungus. Genetics 176: 2541-2549.
27. Loutre C, Wicker T, Travella S, Galli P, Scofield S, Fahima T, Feuillet C, Keller B (2009) Two different CC-NBS-LRR genes are required for Lr10-mediated leaf rust resistance in tetraploid and hexaploid wheat. Plant J 60: 1043-1054.
28. Lukasik E, Takken FLW (2009) STANDing strong, resistance proteins instigators of plant defense. Curr Opin Plant Biol 12: 427-436.
29. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8: 1113-1130.
30. Mirlohi A, Brueggeman R, Drader T, Nirmal J, Steffenson BJ, Kleinhofs A (2008) Allele sequencing of the barley stem rust resistance gene Rpg1 identifies regions relevant to disease resistance. Genet Resist 98: 910-918.
31. Pecchioni N, Faccioli P, Toubia-Rahme H, Valè G, Terzi V (1996) Quantitative resistance to barley leaf stripe (Pyrenophora graminea) is dominated by one major locus. Theor Appl Genet 93: 97-101.
32. Qu S, Liu G, Zhou B, Bellizzi M, Zeng L, Han B, Wang GL (2006) The broad-spectrum blast resistance gene Pi9 encodes an NBS-LRR protein and is a member of the multiple family in rice. Genetics 172: 1901-1914.
33. Rafiqi M, Bernoux M, Ellis JG, Dodds PN (2009) In the trenches of plant pathogen recognition: role of NB-LRR proteins. Semin Cell Dev Biol 20: 1017-1024.
34. Rairdan GJ, Collier SM, Sacco MA, Baldwin TT, Boettrich T, Moffett P (2008) The coiled coil and nucleotide binding domains of the potato Rx disease resistance protein function in pathogen recognition and signalling. Plant Cell 20: 739-751.
35. Rose LE, Bittner-Eddy PD, Langley CH, Holub EB, Michelmore RW, Beynon JL (2004) The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166: 1517-1527.
36. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20: 43-45.
37. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20: 43-45.
38. Scherrer B, Isidore E, Klein P, Kim J, Bellec A, Chalhoub B, Keller B, Feuillet C (2005) Large intraspecific haplotype variability at the Rph7 locus results from rapid and recent divergence in the barley genome. Plant Cell 17: 361-374.
39. Seeholzer S, Tsuchimatsu T, Jordan T, Bieri S, Pajonk S, Yang W, Jahoor A, Shimizu KK, Keller B, Schulze-Lefert P (2010) Diversity at the Mla Powdery Mildew resistance locus from cultivated barley reveals sites of positive selection. Mol Plant Microbe Interact 23: 497-509.
40. Shen QH, Schulze-Lefert P (2007) Rumble in the nuclear Jungle: compartmentalization, trafficking, and nuclear action of plant immune receptors. EMBO J 26: 4239-4301.
41. Steuernagel B, Taudien S, Gundlach H, Seidel M, Ariyadasa R, Schulte D, Petzold A, Felder M, Graner A, Scholz U, Mayer KFX, Platzer M, Stein N (2009) De novo 454 sequencing of barcoded BAC pools for comprehensive gene survey and genome analysis in the complex genome of barley. BMC Genomics 10: 547.
42. Tameling WI, Vossen JH, Albrecht M, Lengauer T, Berden JA, Haring MA, Cornelissen BJ, Takken FL (2006) Mutations in the NB-ARC domain of I-2 that impair ATO hydrolysis cause autoactivation. Plant Physiol 4: 1233-1245.
43. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
44. The International Barley Genome Sequencing Consortium (IBSC) (2012) A physical, genetical and functional sequence assembly of the barley gene space. Nature (London). doi: 10. 1038/nature11543.
45. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25: 4876-4882.
46. Tunali B (1995) Reactions of Turkish barley cultivars to Pyrenophora graminea isolates. Rachis 14: 72-75.
47. 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.
48. Wang M, Allefs S, van den Berg RG, Vleeshouwers VGA, van den Vossen EAG, Vosman B (2008) Allele mining in Solanum: conserved homologues of Rpi-blb1 are identified in Solanum stoloniferum. Theor Appl Genet 116: 933-943.
49. 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.
50. Yahaiaoui N, Brunner S, Keller B (2006) Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J 47: 85-98.
51. Yahiaoui N, Srichumpa P, Dudler R, Keller B (2004) Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J 37: 528-538.
52. Yahyaoui AH (2004) Occurrence of barley leaf blight diseases in central-western Asia and North Africa. In: Yahyaoui AH, Brader L, Tekauz A, Wallwork H, Steffenson B (eds) Proceedings of the second international workshop on barley leaf blights. ICARDA, Aleppo, pp 13-18.
53. Yang Z (2007) PAML4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
54. Yang Z, Nielsen R, Goldman N, Pederson AMK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431-449.
55. Zhou B, Dolan M, Sakai H, Wang GL (2007) The genomic dynamics and evolutionary mechanism of the Pi2/9 locus in rice. Mol Plant Microbe Interact 20: 63-71.