Differential effects of lesion mimic mutants in barley on disease development by facultative pathogens

Journal of Experimental Botany

Volumn 66, Issue 11, 2015, Pages 3417-3428

  McGrann, Graham R D ^b   Steed, Andrew ^a   Burt, Christopher ^c   Nicholson, Paul ^a   Brown, James K M ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b SCOTTISH AGRICULTURAL COLLEGE   (United Kingdom)

^c RAGT Seeds Ltd   (United Kingdom)

Author keywords

Cell death; Disease resistance; Endophyte; Hemibiotroph; Hypersensitive response; Mlo; Necrotroph; Plant microbe interactions

Indexed keywords

PLANT PROTEIN;

ALLELE; ASCOMYCETES; CELL DEATH; DISEASE RESISTANCE; FUSARIUM; GENETICS; HORDEUM; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF;

ALLELES; ASCOMYCOTA; CELL DEATH; DISEASE RESISTANCE; FUSARIUM; HORDEUM; MUTATION; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS;

EID: 84938720409     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv154     Document Type: Article

References (59)

1. Abramoff MD, Magalhaes PJ, Ram SJ. 2004. Image Processing with ImageJ. Biophotonics International 11, 36-42.
2. Balague C, Lin B, Alcon C, Flottes G, Malmström S, Köhler C, Neuhaus G, Pelletier G, Gaymard F, Roby D. 2003. HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide gated channel ion channel family. The Plant Cell 15, 365-379.
3. Blein M, Levrel A, Lemoine J, Gautier V, Chevalier M, Barloy D. 2009. Oculimacula yallundae lifestyle revisited: relationships between the timing of eyespot symptom appearance, the development of the pathogen and the responses of infected partially resistant wheat plants. Plant Pathology 58, 1-11.
4. Brown JKM, Makepeace JC. 2009. The effect of genetic variation in barley on responses to Ramularia collo-cygni. Aspects of Applied Biology 92, 43-47.
5. Brown NA, Urban M, Van De Meene AML, Hammond-Kosack KE. 2010. The infection biology of Fusarium graminearum: defining the pathways of spikelet to spikelet colonisation in wheat ears. Fungal Biology 114, 555-571.
6. Büschges R, Hollricher K, Panstruga R, et al. 1997. The barley mlo gene: A novel control element of plant pathogen resistance. Cell 88, 695-705.
7. Chapman NH, Burt C, Dong H, Nicholson P. 2008. The development of PCR-based markers for the selection of eyespot resistance genes Pch1 and Pch2. Theoretical and Applied Genetics 117, 425-433.
8. Chen X, Steed A, Travella S, Keller B, Nicholson P. 2009. Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytologist 182, 975-983.
9. Colebrook EH, Creissen G, McGrann GRD, Dreos R, Lamb C, Boyd LA. 2012. Broad-spectrum acquired resistance in barley induced by the Pseudomonas pathosystem shares transcriptional components with Arabidopsis systemic acquired resistance. Molecular Plant-Microbe Interactions 25, 658-667.
10. Collins NC, Thordal-Christensen H, Lipka V, et al. 2003. SNAREprotein- mediated disease resistance at the plant cell wall. Nature 425, 973-977.
11. Dangl JL, Dietrich RA, Richberg MH. 1996. Death don't have no mercy: cell death programs in plant-microbe interactions. The Plant Cell 8, 1793-1807.
12. Freialdenhoven A, Peterhansel C, Kurth J, Kreuzaler F, Schulze- Lefert P. 1996. Identification of genes required for the function of nonrace- specific mlo resistance to powdery mildew in barley. Plant Cell 8, 5-14.
13. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205-227.
14. Hammond-Kosack KE, Parker JE. 2003. Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Current Opinion in Biotechnology 14, 177-193.
15. Havis, ND, Brown, JKM, Clemente, G, et al. 2015. Ramularia collocygni - an emerging pathogen of barley crops. Phytopathology doi 10.1094/PHYTO-11-14-0337-FI
16. Havis ND, Nyman N, Oxley SJP. 2014. Evidence for seed transmission and asymptomatic growth of Ramularia collo-cygni in barley (Hordeum vulgare). Plant Pathology 63, 929-936.
17. Heller J, Tudzynski P. 2011. Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annual Review of Phytopathology 49, 369-390.
18. Jansen C, von Wettstein D, Schafer W, Kogel KH, Felk A, Maier FJ. 2005. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proceedings of the National Academy of Sciences of the United States of America 102, 16892-16897.
19. Jarosch B, Kogel KH, Schaffrath U. 1999. The ambivalence of the barley Mlo locus: mutations conferring resistance against powdery mildew (Blumeria graminis f. sp, hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Molecular Plant-Microbe Interactions 12, 508-514.
20. Jones AM. 2001. Programmed cell death in development and defense. Plant Physiology 125, 94-97.
21. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444, 323-329.
22. Jörgensen JH. 1992. Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63, 141-152.
23. Kamlofski CA, Antonelli E, Bender C, Jaskelioff M, Danna CH, Ugalde R, Acevedo A. 2007. A lesion mimic mutant of wheat with enhanced resistance to leaf rust. Plant Pathology 56, 46-54.
24. Keisa A, Kanberga-Silina K, Nakurte I, Kunga L, Rostoks N. 2011. Differential disease resistance response in the barley necrotic mutant nec1. BMC Plant Biology 11, 66.
25. Keisa A, Nakurte I, Kunga L, Kale L, Rostoks N. 2013. Increased auxin content and altered auxin response in barley necrotic mutant nec1. In: Advance in Barley Sciences: Proceedings of 11th International Barley Genetics Symposium . Dordrecht: Springer, 229-241.
26. Kjaer B, Jensen HP, Jensen J, Jörgensen JH. 1990. Associations between 3 ml-o powdery mildew resistance genes and agronomic traits in barley. Euphytica 46, 185-193.
27. Kumar J, Huckelhoven R, Beckhove U, Nagarajan S, Kogel KH. 2001. A compromised Mlo pathway affects the response of barley to the necrotrophic fungus Bipolaris sorokiniana (Teleomorph: Cochliobolus sativus) and its toxins. Phytopathology 91, 127-133.
28. Lorrain S, Vailleau F, Balaque C, Roby D. 2003. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends in Plant Science 8, 263-271.
29. Ma W, Berkowitz GA. 2011. Ca2+ conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades. New Phytologist 190, 566-572.
30. Makepeace JC, Havis ND, Burke JI, Oxley SJP, Brown JKM. 2008. A method of inoculating barley seedlings with Ramularia collo-cygni. Plant Pathology 57, 991-999.
31. McGrann, GRD, Steed A, Burt C, Goddard R, LaChaux C, Bansal A, Corbitt M, Gorniak K, Nicholson P, Brown JKM. 2015. Contribution of the drought tolerance-related Stress-responsive NAC 1 transcription factor to resistance of barley to Ramularia leaf spot. Molecular Plant Pathology 16, 201-209.
32. McGrann GRD, Stavrinides A, Russell J, Corbitt MM, Booth A, Chartrain L, Thomas WT, Brown JKM. 2014. A trade off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, Ramularia leaf spot. Journal of Experimental Botany 65, 1025-1037.
33. McGrann GRD, Townsend BJ, Antoniw JF, Asher MJC, Mutasa- Göttgens ES. 2009. Barley elicits a similar early basal defence response during host and non-host interactions with Polymyxa root parasites. European Journal of Plant Pathology 123, 5-15.
34. Mengiste T. 2012. Plant immunity to necrotrophs. Annual Review of Phytopathology 50, 267-294.
35. Moeder W, Urquhart W, Ung H, Yoshioka K. 2011. The role of cyclic nucleotide-gated ion channels in plant immunity. Molecular Plant 4, 442-452.
36. Moeder W, Yoshioka K. 2008. Lesion mimic mutants: a classical, yet still fundamental approach to study programmed cell death. Plant Signaling & Behavior 3, 764-767.
37. Nurnberger T, Brunner F, Kemmerling B, Piater L. 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunological Reviews 198, 249-266.
38. Payne RW, Murray DA, Harding SA, Baird DB, Soutar DM. 2009. GenStat for Windows (12th Edition) Introduction . Hemel Hempstead: VSN International.
39. Peraldi A, Griffe LL, Burt C, McGrann GRD, Nicholson P. 2014. Brachypodium distachyon exhibits compatible interactions with Oculimacula spp. and Ramularia collo-cygni, providing the first pathosystem model to study eyespot and ramularia leaf spot diseases. Plant Pathology 63, 554-562.
40. Persson M, Falk A, Dixelius C. 2009. Studies on the mechanism of resistance to Bipolaris sorokiniana in the barley lesion mimic mutant bst1. Molecular Plant Pathology 10, 587-598.
41. Persson M, Rasmussen M, Falk A, Dixelius C. 2008. Barley mutants with enhanced level of resistance to Swedish isolates of Bipolaris sorokiniana, casual agent of spot blotch. Plant Breeding 127, 639-643.
42. Peterhänsel C, Freialdenhoven A, Kurth J, Kolsch R, Schulze-Lefert P. 1997. Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell 9, 1397-1409.
43. Petti C, Reiber K, Ali SS, Berney M, Doohan FM. 2012. Auxin as a player in the biocontrol of Fusarium head blight disease of barley and its potential as a disease control agent. BMC Plant Biology 12, 224.
44. Piffanelli P, Zhou FS, 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 Physiology 129, 1076-1085.
45. Rostoks N, Schmierer D, Kudrna D, Kleinhofs A. 2003. Barley putative hypersensitive induced reaction genes: genetic mapping, sequence analyses and differential expression in disease lesion mimic mutants. Theoretical and Applied Genetics 107, 1094-1101.
46. Rostoks N, Schmierer D, Mudie S, Drader T, Brueggeman R, Caldwell DG, Waugh R, Kleinhofs A. 2006. Barley necrotic locus nec1 encodes the cyclic nucleotide-gated ion channel 4 homologous to the Arabidopsis HLM1. Molecular Genetics and Genomics 275, 159-168.
47. Saville RJ, Gosman N, Burt CJ, Makepeace J, Steed A, Corbitt M, Chandler E, Brown JKM, Boulton MI, Nicholson P. 2012. The 'Green Revolution' dwarfing genes play a role in disease resistance in Triticum aestivum and Hordeum vulgare. Journal of Experimental Botany 63, 1271-1283.
48. Scherm B, Balmas V, Spanu F, Pani G, Delogu G, Pasquali M, Migheli Q. 2013. Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Molecular Plant Pathology 14, 323-341.
49. Schützendübel A, Stadler M, Wallner D, von Tiedemann A. 2008. A hypothesis on physiological alterations during plant ontogenesis governing susceptibility of winter barley to ramularia leaf spot. Plant Pathology 57, 518-526.
50. Scott PR. 1971. The effect of temperature on eyespot (Cercosporella herpotrichoides) in wheat seedlings. Annals of Applied Biology 68, 169-175.
51. Shagimardanova EI, Gusev OA, Sychev VN, Levinskikh MA, Sharipova MR, Il'inskaya ON, Bingham G, Sugimoto M. 2010. Expression of stress response genes in barley Hordeum vulgare in a spaceflight environment. Molecular Biology 44, 734-740.
52. Stabentheiner E, Minihofer T, Huss H. 2009. Infection of barley by Ramularia collo-cygni: scanning electron microscopic investigations. Mycopathologia 168, 135-143.
53. Taylor JMG, Paterson LJ, Havis ND. 2010. A quantitative real-time PCR assay for the detection of Ramularia collo-cygni from barley (Hordeum vulgare). Letters in Applied Microbiology 50, 493-499.
54. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research 0034.0031-0034.0011.
55. Walters DR, Havis ND, Oxley SJP. 2008. Ramularia collo-cygni: the biology of an emerging pathogen of barley. Fems Microbiology Letters 279, 1-7.
56. Wolter M, Hollricher K, Salamini F, Schulze-Lefert P. 1993. The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defense mimic phenotype. Molecular and General Genetics 239, 122-128.
57. Wright SA, Azarang M, Falk AB. 2013. Barley lesion mimics, supersusceptible or highly resistant to leaf rust and net blotch. Plant Pathology 62, 982-992.
58. Zadoks JC, Chang TT, Konzak CF. 1974. Decimal code for growth stages of cereals. Weed Research 14, 415-421.
59. Zhang L, Lavery L, Gill U, Gill K, Steffenson B, Yan GP, Chen XM, Kleinhofs A. 2009. A cation/proton-exchanging protein is a candidate for the barley NecS1 gene controlling necrosis and enhanced defense response to stem rust. Theoretical and Applied Genetics 118, 385-397.