Mechanisms of Snow Mold Resistance in Wheat

  • Denis GaudetEmail author
  • André Laroche
Conference paper


Snow molds can limit production of winter wheat in regions that are prone to deep persistent snow during the winter. There are two mechanisms involved in resistance to snow molds: (1) genetic resistance varieties and (2) age-related resistance varieties. Winter wheat varieties seeded early are substantially more resistant than those seeded on conventional seeding dates, regardless of their level of genetic resistance to snow molds. Both forms of resistance are induced at low temperatures during hardening. Also associated with snow mold resistance in wheat is fructan; resistant varieties accumulate higher levels of fructans in the autumn and metabolize them more slowly throughout the winter compared to susceptible varieties and early-seeded varieties always accumulate higher levels of fructans compared to later seeded varieties. The mechanism(s) of snow mold resistance remains unknown, although previous studies have demonstrated the upregulation of defense pathways and transcripts of defense-related proteins and transcription factors during prehardening growth and hardening, particularly those associated with the jasmonic acid defense pathway. A model for snow mold resistance that integrates upregulation of defense genes during hardening and early infection by snow molds and fructan-mediated homeostasis, which maintains defense gene expression during the winter, is presented. Gradual depletion of fructan reserves reduces the plant’s ability to maintain defense gene expression and eventually results in plant susceptibility if snow mold conditions persist. The involvement of common defense pathways in biotic and abiotic forms of resistance to snow molds is an important consideration for devising strategies for control of these pathogens.


Winter Wheat Cold Acclimation Freezing Tolerance Winter Cereal Systemic Acquire Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7:601–611PubMedCrossRefGoogle Scholar
  2. Amano Y, Osanai S-I (1983) Winter wheat breeding for resistance to snow mold and cold hardiness. III. Varietal differences of ecological characteristics on cold acclimation and relationships of them to resistance. Bull Hokkaido Natl Agric Exp Stn 50:83–95Google Scholar
  3. Årsvoll K (1976) Sclerotinia borealis. Sporulation, spore germination and pathogenesis. Meld Norg LandbrHogsk 55:1–11Google Scholar
  4. Årsvoll K (1977) Effects of hardening, plant age, and development in Phleum pratense and Festuca pratensis on resistance to snow mould fungi. Meld Norg LandbrHøgsk 56:1–14Google Scholar
  5. Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 7:391–399PubMedCrossRefGoogle Scholar
  6. Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Ann Rev Phytopathol 45:399–436CrossRefGoogle Scholar
  7. Bertrand A, Castonguay Y, Azaiez A, Hsiang T, Dionne J (2011) Cold-induced responses in annual bluegrass genotypes with differential resistance to pink snow mold (Microdochium nivale). Plant Sci 180:111–119PubMedCrossRefGoogle Scholar
  8. Bhuiyan NH, Selvaraj G, Wei Y, King J (2009) Role of lignification in plant defense. Plant Signal Behav 4:158–159PubMedCrossRefGoogle Scholar
  9. Bruehl GW (1982) Developing wheats resistant to snow mold. Plant Dis 66:1190–1093Google Scholar
  10. Bruehl GW, Cunfer B (1971) Physiologic and environmental factors that affect the severity of snow mold of wheat. Phytopathology 61:792–799CrossRefGoogle Scholar
  11. Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451PubMedCrossRefGoogle Scholar
  12. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedCrossRefGoogle Scholar
  13. Conrath U (2009) Priming of induced plant defense responses. Adv Bot Res 51:361–395CrossRefGoogle Scholar
  14. Cook RJ, Papendick RI (1972) Influence of water potential of soils and plants on root disease. Ann Rev Phytopathol 10:349–374CrossRefGoogle Scholar
  15. Dörffling K, Schulenburg S, Lesselich G, Dörffling H (1990) Abscisic acid and proline levels in cold hardened winter wheat leaves in relation to variety-specific differences in freezing resistance. J Agron Crop Sci 165:230–239CrossRefGoogle Scholar
  16. Durrant WE, Dong X (2004) Systemic acquired resistance. Ann Rev Phytopathol 42:185–209CrossRefGoogle Scholar
  17. Ergon Å, Klemsdal SS, Tronsmo AM (1998) Interactions between cold hardening and Microdochium nivale infection on expression of pathogenesis-related genes in winter wheat. Physiol Mol Plant Pathol 53:301–310CrossRefGoogle Scholar
  18. Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009) Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol 150:1750–1761PubMedCrossRefGoogle Scholar
  19. Fowler DB (1982) Date of seeding, fall growth, and winter survival of winter wheat and rye. Agron J 74:1060–1063CrossRefGoogle Scholar
  20. Fowler DB (2012) Wheat production in the high winter stress climate of the great plains of North America—An experiment in crop adaptation. Crop Sci 52:11–20CrossRefGoogle Scholar
  21. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690PubMedCrossRefGoogle Scholar
  22. Galiba G, Tuberosa R, Kocsy G, Sutka J (1993) Involvement of chromosomes 5 A and 5D in cold-induced abscisic acid accumulation in and frost tolerance of wheat calli. Plant Breed 110:237–242CrossRefGoogle Scholar
  23. Garcàa-Olmedo F, Molina A, Alamillo JM, Rodràguez-Palenzuéla P (1998) Plant defense peptides. Biopolymers 47:479–491CrossRefGoogle Scholar
  24. Gaudet DA (1986) Effect of temperature on pathogenicity of sclerotial and non-sclerotial isolates of Coprinus psychromorbidus under controlled conditions. Can J Plant Pathol 8:394–399CrossRefGoogle Scholar
  25. Gaudet DA (1994) Progress towards understanding interactions between cold hardiness and snow mold resistance and development of resistant cultivars. Can J Plant Pathol 16:241–246CrossRefGoogle Scholar
  26. Gaudet DA, Bhalla MK, Clayton GC, Chen THH (1989) Effect of cottony snow mold and low temperatures on winter wheat survival in central and northern Alberta. Can J Plant Pathol 11:291–296CrossRefGoogle Scholar
  27. Gaudet DA, Chen THH (1987) Effects of hardening and plant age on development of resistance to cottony snow mold (Coprinus psychromorbidus) in winter wheat under controlled conditions. Can J Bot 65:1152–1156CrossRefGoogle Scholar
  28. Gaudet DA, Chen THH (1988) The effect of freezing resistance and low temperature stress on development of cottony snow mold (Coprinus psychromorbidus) in winter wheat. Can J Bot 66:1610–1615CrossRefGoogle Scholar
  29. Gaudet DA, Kokko EG (1985) Penetration and infection of winter wheat leaves by Coprinus psychromorbidus under controlled conditions. Can J Bot 62:955–960Google Scholar
  30. Gaudet DA, Kozub GC (1991) Screening winter wheat for resistance to cottony snow mold under controlled conditions. Can J Plant Sci 71:957–965CrossRefGoogle Scholar
  31. Gaudet DA, Laroche A, Frick M, Huel R, Puchalski B (2003a) Cold induced expression of plant defensin and lipid transfer protein transcripts in winter wheat. Physiol Plant 117:195–205CrossRefGoogle Scholar
  32. Gaudet DA, Laroche A, Frick M, Huel R, Puchalski B (2003b) Plant development affects the cold-induced expression of plant defence-related transcripts in winter wheat. Physiol Mol Plant Pathol 62:175–184CrossRefGoogle Scholar
  33. Gaudet DA, Laroche A, Puchalski B (2001) Seeding date alters carbohydrate accumulation in winter wheat. Crop Sci 41:728–738CrossRefGoogle Scholar
  34. Gaudet DA, Laroche A, Yoshida M (1999) Low temperature-wheat-fungal interactions: a carbohydrate connection. Physiol Plant 106:437–444CrossRefGoogle Scholar
  35. Gaudet DA, Tronsmo AM, Laroche A (2012) Climate change and plant diseases. Temperature adaptation in a changing climate. Nature at risk. KB Story and KK Tanino. Wallingford, UK, CABI:144–159Google Scholar
  36. Gaudet DA, Wang Y, Frick M, Puchalski B, Penniket C, Ouellet T, Robert L, Singh J, Laroche A (2010) Low temperature induced defence gene expression in winter wheat in relation to resistance to snow moulds and other wheat diseases. Plant Sci 180:99–110PubMedCrossRefGoogle Scholar
  37. Grant MR, Jones JDG (2009) Hormone (dis)harmony moulds plant health and disease. Science 324:750–752PubMedCrossRefGoogle Scholar
  38. Heath MC (2000a) Hypersensitive response-related death. Plant Mol Biol 44:321–334CrossRefGoogle Scholar
  39. Heath MC (2000b) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319CrossRefGoogle Scholar
  40. Hématy K, Cherk C, Somerville S (2009) Host–pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12:406–413PubMedCrossRefGoogle Scholar
  41. Hincha DK, Livingston III DP, Premakumar R, Zuther E, Obel N, Cacela C, Heyer AG (2007) Fructans from oat and rye: Composition and effects on membrane stability during drying. Biochim Biophys Acta (BBA)—Biomembr 1768:1611–1619Google Scholar
  42. Hon WC, Griffith M, Mlynarz A, Kwok YC, Yang D (1995) Antifreeze proteins in winter rye sre similar to pathogenesis-related proteins. Plant Physiol 109:879–889PubMedCrossRefGoogle Scholar
  43. Houde M, Belcaid M, Ouellet F, Danyluk J, Monroy A, Dryanova A, Gulick P, Bergeron A, Laroche A, Links M, MacCarthy L, Crosby W, Sarhan F (2006) Wheat EST resources for functional genomics of abiotic stress. BMC Genomics 7:149PubMedCrossRefGoogle Scholar
  44. Houde M, Danyluk J, Laliberte J-F, Rassart E, Dhindsa RS, Sarhan F (1992) Cloning, characterization, and expression of a cDNA encoding a 50-Kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol 99:1381–1387PubMedCrossRefGoogle Scholar
  45. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230CrossRefGoogle Scholar
  46. Iriki N, Kuwabara T (1993) Half diallel analysis of field resistance of winter wheat to Typhula ishikariensis Biotype A in artificially infested plots. Japan J Breed 43:495–501CrossRefGoogle Scholar
  47. Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15:2503–2513PubMedCrossRefGoogle Scholar
  48. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  49. Kawakami A, Yoshida M (2002) Molecular characterization o fsucrose:sucrose 1-fructosyltransferase and sucrose:fructan 6-fructosyltransferase associated with fructan accumulation in winter wheat during cold hardening. Biosci Biotechnol Biochem 66:2297–2305PubMedCrossRefGoogle Scholar
  50. Kawakami A, Yoshida M (2005) Fructan:fructan 1-fructosyltransferase, a key enzyme for biosynthesis of graminan oligomers in hardened wheat. Planta 223:90–104PubMedCrossRefGoogle Scholar
  51. Kawakami A, Yoshida M (2012) Graminan breakdown by fructan exohydrolase induced in winter wheat inoculated with snow mold. J Plant Physiol 169:294–302PubMedCrossRefGoogle Scholar
  52. Kiyomoto RK, Bruehl GW (1977) Carbohydrate accumulation and depletion by winter cereals differing in resistance to Typhula idahoensis. Phytopathology 67:206–211CrossRefGoogle Scholar
  53. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844PubMedCrossRefGoogle Scholar
  54. Kuwabara C, Imai R (2009) Molecular basis of disease resistance acquired through cold acclimation in overwintering plants. J Plant Biol 52:19–26CrossRefGoogle Scholar
  55. Nissinen O (1996) Analysis of climatic factors affecting snow mould injury in first-year timothy (Phleum pratence L.) with special reference to Sclerotinia borealis. Acta Univ Oulu A 289:1–115Google Scholar
  56. Wingender R, Röhrig H, Höricke C, Wing D, Schell, J (1989) Differential regulation of soybean chalcone synthase genes in plant defence, symbiosis and upon environmental stimuli. Mol Gen Genet 218:315–322Google Scholar
  57. Orozco-Cardenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and system in via the octadecanoid pathway. Proc Nat Acad Sci 96:6553–6557Google Scholar
  58. Oshiman K, Kobayashi I, Shigemitsu H, Kunoh H (1995) Studies on turfgrass snow mold caused by Typhula ishikariensis. II. Microscopical observation of infected bentgrass leaves. Mycoscience 36:179–185CrossRefGoogle Scholar
  59. Østrem L, Rapacz M, Jørgensen M, Höglind M (2011) Effect of developmental stage on carbohydrate accumulation patterns during winter of timothy and perennial ryegrass. Acta Agric Scand, Section B – Soil Plant Sci 61:153–163Google Scholar
  60. Pääkkönen E, Seppänen S, Holopainen T, Kokko H, Kärenlampi S, Kärenlampi L, Kangasjärvi J (1998) Induction of genes for the stress proteins PR-10 and PAL in relation to growth, visible injuries and stomatal conductance in birch (Betula pendula) clones exposed to ozone and/or drought. New Phytol 138:295–305CrossRefGoogle Scholar
  61. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295PubMedCrossRefGoogle Scholar
  62. PŁażek A, Dubert F, Pociecha E, Janowiak F, Kolasińska I, Maciejewski M (2011) Resistance of winter rye (Secale cereale L.) to Microdochium nivale depends on soluble carbohydrate content but not on abscisic acid level. J Phytopathol 159:751–758CrossRefGoogle Scholar
  63. Pociecha E, Płażek A, Janowiak F, Janeczko A, Zwierzykowski Z (2008a) Physiological basis for differences in resistance to Microdochium nivale (Fr.) Samuels and Hallett in two androgenic genotypes of Festulolium derived from tetraploid F1 hybrids of Festuca pratensis and Lolium multiflorum (Festulolium). J Phytopath 156:155–163CrossRefGoogle Scholar
  64. Pociecha E, Płażek A, Janowiak F, Zwierzykowski Z (2008b) ABA level, proline and phenolic concentration, and PAL activity induced during cold acclimation in androgenic Festulolium forms with contrasting resistance to frost and pink snow mould (Microdochium nivale). Physiol Mol Plant Pathol 73:126–132CrossRefGoogle Scholar
  65. Pociecha E, Płażek A, Janowiak F, Waligórski P, Zwierzykowski Z (2009) Changes in abscisic acid, salicylic acid and phenylpropanoid concentrations during cold acclimation of androgenic forms of Festulolium (Festuca pratensis, Lolium multiflorum) in relation to resistance to pink snow mould (Microdochium nivale). Plant Breed 128:397–403CrossRefGoogle Scholar
  66. Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicytate antagonism. Ann Rev Phytopathol 49:317–343CrossRefGoogle Scholar
  67. Sun J-Y, Gaudet DA, Lu Z-X, Frick M, Puchalski B, Laroche A (2008) Characterization and antifungal properties of wheat nonspecific lipid transfer proteins. Mol Plant-Microbe Interact 21:346–360PubMedCrossRefGoogle Scholar
  68. Sung S, Amasino RM (2005) Remenbering winter: toward a molecular understanding of vernalization. Ann Rev Plant Biol 56:491–508CrossRefGoogle Scholar
  69. Thomashow MF (2003) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599CrossRefGoogle Scholar
  70. Thordal-Christensen H (2003) Fresh insights into processes of nonhost resistance. Curr Opin Plant Biol 6:351–357PubMedCrossRefGoogle Scholar
  71. Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317PubMedCrossRefGoogle Scholar
  72. Tronsmo A, Gregersen PL, Hjelsjord J, Sandal T, Bryngelsson T, Collinge DB (1993) Cold induced disease resistance. Mechanisms of plant defense responses. B Fritig and M Legrand, Kluwer Academic Publishers 369Google Scholar
  73. Tronsmo AM (1984a) Predisposing effects of low temperature on resistance to winter stress factors in grasses. Acta Agric Scand 34:210–220CrossRefGoogle Scholar
  74. Tronsmo AM (1984b) Resistance to the rust fungus Puccinia poae-nemoralis in Poa pratensis is induced by low-temperature hardening. Can J Bot 62:2891–2892CrossRefGoogle Scholar
  75. Tronsmo AM (1986) Host water potentials may restrict development of snow mold fungi in low temperature hardened grasses. Physiol Plant 68:175–179CrossRefGoogle Scholar
  76. Van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Ann Rev Phytopathol 44:135–162CrossRefGoogle Scholar
  77. Veisz O, Galiba G, Sutka J (1996) Effect of abscisic acid on the cold hardiness of wheat seedlings. J Plant Physiol 149:439–443CrossRefGoogle Scholar
  78. Wingender R, Röhrig H, Höricke C, Wing D, Schell, J (1989) Differential regulation of soybean chalcone synthase genes in plant defence, symbiosis and upon environmental stimuli. Mol Gen Genet 218:315–322Google Scholar
  79. Yoshida M, Abe J, Moriyama M, Kuwabara T (1998) Carbohydrate levels among winter wheat cultivars varying in freezing tolerance and snow mold resistance during autumn and winter. Physiol Plant 103:8–16CrossRefGoogle Scholar
  80. Yoshida M, Abe J, Moriyama M, Shimokawa S, Nakamura Y (1997) Seasonal changes in the physical state of crown water associated with freezing tolerance in winter wheat. Physiol Plant 99:363–370CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Agriculture and Agri-Food CanadaLethbridge Research CentreLethbridgeCanada

Personalised recommendations