European oak powdery mildew: Impact on trees, effects of environmental factors, and potential effects of climate change

Annals of Forest Science

Volumn 71, Issue 6, 2014, Pages 633-642

  Marçais, Benoit ^a   Desprez Loustau, Marie Laure ^b  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UMR 1202 BIOGECO   (France)

Author keywords

Erysiphe alphitoides; Quercus; Natural regeneration; Oak decline; Phenological synchrony

Indexed keywords

EID: 84906242269     PISSN: 12864560     EISSN: 1297966X     Source Type: Journal    
DOI: 10.1007/s13595-012-0252-x     Document Type: Review

References (81)

1. Anonymous (1956) Oak mildew. Forestry Commission Leaflet no. 38
2. Arnaud G (1921) Study on parasite fungi (Parodiellinaceae, including Erysiphaea (in French). Ann Epiphyt 7:1-115
3. Aubert CG (1919) Powdery mildew and forests of western France (in French). Rev Eaux Forêts 57:189-195
4. Aust HJ, Hoyningen-Huene J (1986) Microclimate in relation to powdery mildew epidemics. Annu Rev Phytopathol 24:491-510
5. Barbaroux C, Bréda N (2002) Contrasting distribution and seasonal dynamics of carbohydrate reserves in stem wood of adult ring-porous sessile oak and diffuse-porous beech trees. Tree Physiol 22:1201-1210
6. Basova SV (1987) Seasonal dynamics of powdery mildew of pedunculate oak in a seed grafting plantation (in Russian). Mikol Fitopatol 21:269-273
7. Bastiaan L (1991) Ratio between virtual and visual lesion size as a measure to describe reduction in leaf photosynthesis of rice due to leaf blast. Phytopathology 81:611-615
8. Battaglia M, Pinkard EA, Sands PJ, Bruce JL, Quentin A (2011) Modelling the impact of defoliation and leaf damage on forest plantation function and production. Ecol Modelling 222:3193-3202
9. Borchert R (1976) Differences in shoot growth patterns between juvenile and adult trees and their interpretation based on systems analysis of trees. Acta Hort 56:123-130
10. Both C, Van Ash M, Bijlsma RG, Van Den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J Animal Ecol 78:73-83
11. Brasier CM, Robredo F, Ferraz JFP (1993) Evidence for Phytophthora cinnamomi involvement in Iberian oak decline. Plant Pathol 42:140-145
12. Bréda N, Granier A, Aussenac G (1995) Effects of thinning on soil and tree water relations, transpiration and growth in an oak forest (Quercus petraea). Tree Physiol 15:295-306
13. Brüggemann N, Schnitzler JP (2001) Influence of powdery mildew (Microsphaera alphitoides) on isoprene biosynthesis and emission of pedunculate oak (Quercus robur L.) leaves. J Appl Bot 75:91-96
14. Bureau E (1908) Impact of Oidium quercinum on different oak species. CR Hebd Scéances Acad Sci 10:268 (in French)
15. Chuine I (2000) A unified model for tree phenology. J Theor Biol 707:337-347
16. Delatour C (1983) Oak declines in Europe (in French). Rev For Franc 35:265-282
17. Desprez-Loustau ML, Vitasse Y, Delzon S, Capdevielle X, Marçais B, Kremer A (2010a) Are plant pathogen populations adapted for encounter with their host? A case study of phenological synchrony between oak and an obligate fungal parasite along an altitudinal gradient. J Evol Biol 23:87-97
18. Desprez-Loustau ML, Robin C, Reynaud G, Déqué M, Badeau V, Piou D, Husson C, Marçais B (2010b) Simulating the effects of a climate change scenario on geographical range and activity of forest pathogenic fungi. In: Loustau D (ed) Response of temperate and Mediterranean forests to climate change: effects on carbon cycle, productivity and vulnerability. QUAE, Paris, pp 253-280
19. Desprez-Loustau M-L, Feau N, Mougou-Hamdane A, Dutech C (2011) Interspecific and intraspecific diversity in oak powdery mildews in Europe: coevolution history and adaptation to their hosts. Mycoscience 52:163-175
20. Divon HH, Fluhr R (2007) Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol Letters 266:65-74
21. Doé F (1919) [The conversion of coppice with standard into high forest and powdery mildew] (in French). Rev Eaux Forêts 57:53-59
22. Ducomet V (1913) Research on oak and chestnut diseases in Brittany (in French). Ann Epiphyt 1:87-105
23. Edwards MC, Ayres PG (1982) Seasonal changes in resistance of Quercus petraea (sessile oak) leaves to Microsphaera alphitoides. Trans Br Mycol Soc 78:569-571
24. Endler JA (1993) The color of light in forests and its implications. Ecol Monographs 63:1-27
25. Fabre B, Ioos R, Piou D, Marçais B (2011) Is emergence of pine Dothistroma needle blight in France caused by the cryptic species Dothistroma pini. Phytopathology 102:47-54
26. Falk R (1924) Oak dieback in the Straslund district and contribution to the biology of Armillaria and powdery mildew in German. Allg Forst Jagdz 100:298-317
27. Feau N, Lauron-Moreau A, Piou D, Marçais B, Dutech C, Desprez-Loustau ML (2011) Niche partitioning of genetic lineages involved in the oak powdery mildew complex. Fung Ecol 5:154-162
28. Foex ME (1941) Invasion of European oaks by the powdery mildew (in French). Rev Eaux Forêts 79:338-349
29. Gerard B, Caël O, Mandret X, Bréda N, Marçais B (2013) Disturbances in the leaf area index dynamics increases oak's vulnerability to powdery mildew and therefore the risk of decline. Ann For Sci (in press)
30. Giertych MJ, Suszka J (2010) Influence of cutting off distal ends of Quercus robur acorns on seedling growth and their infection by the fungus Erysiphe alphitoides in different light conditions. Dendrobiology 64:73-77
31. Glawe DA (2008) The powdery mildews:a review of the world's most familiar (yet poorly known) plant pathogens. Annu Rev Phytopathol 46:27-51
32. Grzebyta J, Karolewski P, Zytkowiak R, Giertych MJ, Werner A, Zadworny M, Oleksyn J (2005) Effects of elevated temperature and fluorine pollution on relations between the pedunculate oak (Quercus robur) and oak powdery mildew (Microsphaera alphitoides). Dendrobiology 53:27-33
33. Grzywacz A, Wazny J (1973) The impact of industrial air pollutants on the occurrence of several important pathogenic fungi of forest trees in Poland. Eur J For Pathol 3:129-141
34. Hajji M, Dreyer M, Marçais B (2009) Impact of Erysiphe alphitoides on transpiration and photosynthesis in Quercus robur leaves. Eur J Plant Pathol 125:63-72
35. Hewitt HG (1974) Conidial germination in Microsphaera alphitoides. Trans Br Mycol Soc 63:587-628
36. 2 and water vapour exchange rates in leaves of Quercus robur infected by Microspheara alphitoides (powdery mildew). Physiol Plant Pathol 7:127-137
37. Hewitt HG, Ayres PG (1976) Effect of infection by Microsphaera alphitoides (powdery mildew) on carbohydrate levels and translocation in seedlings of Quercus robur. New Phytolol 77:379-390
38. Jarvis PG (1964) The adaptability to light intensity of seedlings of Quercus petraea. J Ecol 52:545-571
39. Jarvis WR, Gubler WD, Grove GG (2002) Epidemiology of powdery mildews in agricultural pathosystems. In: Bélanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews. A comprehensive treatise. APS Press, St. Paul, pp 169-199
40. Jung T, Blaschke H, Oswald W (2000) Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease. Plant Pathol 49:706-718
41. Kelly DL (2002) The regeneration of Quercus petraea (sessile oak) in southweat Ireland: a 25-year experimental study. For Ecol Manag 166:207-226
42. Kerling L (1966) The hibernation of the oak mildew. Acta Bot Neerl 15:76-83
43. Kiss L, Pintye A, Kovács GM, Jankovics T, Fontaine MC, Harvey N, Xu X, Nicot PC, Bardin M, Shykoff JA, Giraud T (2011) Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi. Mol Ecol 20:1492-1507
44. Langhoffer A (1929) Oak decline in Yougoslavia, especially in Slavonia (in French). Rev Eaux Forêts 37:763-764
45. Landmann G, Becker M, Delatour C, Dreyer E, Dupouey JL (1993) Oak dieback in France: historical and recent records, possible causes, current investigations. In: Rundgespräche der Kommission für Ökologie, Bd. 5 'Zustand und Gefährdung der Laubwälder', pp. 97-114
46. Lanier L, Joly P, Bondoux P, Bellemère A (1976) Pathology of broadleaf trees species (in French). Mycologie et Pathologie forestière, Masson, In, pp 311-320
47. Marçais B, Caël O, Delatour C (2000) Relationship between above-ground signs and symptoms and root infection by Collybia fusipes in oaks. For Pathol 30:7-17
48. Marçais B, Bréda N (2006) Role of an opportunistic pathogen in the decline of stressed oak trees. J Ecol 94:1214-1223
49. Marçais B, Kavkova M, Desprez-Loustau ML (2009) Phenotypic variation in the phenology of ascospore production between European populations of oak powdery mildew. Ann For Sci 66:814-822
50. Mignucci JS, Boyer JS (1979) Inhibition of photosynthesis and transpiration in soybean infected by Microsphaera diffusa. Phytopathology 69:227-230
51. Minkevich II, Stoyanov SM (1987) Prevision of the development of oak powdery mildew based on the phenology of the host plant in Bulgaria. Izvestiya Vysshikh Zavedenij, Lesnoj Zhurnal 3:114-116 (in Bulgarian)
52. Molleveaux J (1926) [The demise of late oak in Vierzon] (in French). Rev Eaux Forêts 64:614-617
53. Mougou A, Dutech C, Desprez-Loustau ML (2008) New insights into the identity and origin of the causal agent of oak powdery mildew in Europe. For Pathol 38:275-287
54. Mougou-Hamdane A, Giresse X, Dutech C, Desprez-Loustau ML (2010) Spatial distribution of lineages of oak powdery mildew fungi in France, using quick molecular detection methods. Ann For Sci 67:212
55. Murray JS (1974) The fungal pathogens of oak. In: Morris MG, Perrin FH (eds) The British oak: its history and natural history. Botanical society of the British Isles & EW Classey, Faringdon, Berkshire
56. Newsham KK, Oxborough K, Greenslade PD, McLeod AR (2000) UV-B radiation constrains the photosynthesis of Quercus robur through impacts on the abundance of Microsphaera alphitoides. For Pathol 30:265-275
57. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637-669
58. Percival GC, Fraser GA (2002) The influence of powdery mildew infection on photosynthesis, chlorophyll fluorescence, leaf chlorophyll and carotenoid content of three woody plant species. Arboricultural Journal 26:333-346
59. Petercord R (2011) Damage on oak after insect infestation and mildew infection in Lower and Middle Franconia (in German). Forstschutz Aktuell 51:19-21
60. Pinkard EA, Battaglia M, Roxburgh S, O'Grady AP (2011) Estimating the net primary production under changing climate: adding pest into the equation. Tree Physiol 31:686-699
61. Raymond J (1927) Oak powdery mildew (in French). Ann Epiphyt 13:94-129
62. Roberts MR, Paul ND (2006) Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytol 170:677-699
63. Robinson RL (1927) Mortality among oaks. Quaterly J For 21:25-27
64. Roux C (1910) [Oak powdery mildew] (in French). Annales de la Société d'Agriculture, Science et Industrie IV:251-258
65. Schnathorst WC (1965) Environmental relationships in the powdery mildews. Annu Rev Phytopathol 3:343-366
66. Schuerger AC, Brown CS (1997) Spectral quality affects disease development of three pathogens on hydroponically grown plants. Hort Sci 32:96-100
67. Selochnik NN, Il'yushenko AF, Kondrashova NK (1994) Powdery mildew of oak and its distribution in the stand canopy (in Russian). Lesovedenie 4:61-70
68. Sivapalan A (1993) Effect of water on germination of powdery mildew conidia. Mycol Res 97:71-76
69. Shtienberg D (1992) Effects of foliar diseases on gas exchange processes: a comparative study. Phytopathology 82:760-765
70. Soutrenon A (1998) [A pluriannual experiment confirms the impact of powdery mildew on young seedlings] (in French). Les cahiers du DSF, 1-2000 (la santé des forets [France] en 1997), Min. Agri. Pêche (DERF), Paris, 93-94
71. Soutrenon A (2003) [Evaluation of the interest of a chemical treatment againt oak powdery mildew in natural regeneration] Document CEMAGREF, 19p (in French)
72. Sucharzewska E (2009) The development of Erysiphe alphitoides and E. hypophylla in the urban environment. Acta Mycol 44:109-123
73. Suthaparan A, Torre S, Stensvand A, Herrero ML, Pettersen RI, Gadoury DM, Gislerød HR (2010) Specific light-emitting diodes can suppress sporulation of Podosphaera pannosa on greenhouse roses. Plant Dis 94:1105-1110
74. Takamatsu S, Braun U, Limkaisang S, Kom-Un S, Sato Y, Cunnington JH (2007) Phylogeny and taxonomy of the oak powdery mildew Erysiphe alphitoides sensu lato. Mycol Res 111:809-826
75. Thomas FM, Blank R, Hartmann G (2002) Abiotic and biotic factors and their interactions as causes of oak decline in central Europe. For Pathol 32:277-307
76. Van Ash M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37-55
77. Weltzien HC (1978) Geographical distribution of powdery mildews. In: Spencer DM (ed) The powdery mildews. Academic, London, pp 39-49
78. Willocquet L, Colombet C, Rougier M, Fargues J, Clerjeau M (1996) Effects of radiation, especially ultraviolet B, on conidial germination and mycelial growth powdery mildew. Eur J Plant Pathol 102:441-449
79. Woodward RC, Waldie JSL, Steven HM (1929) Oak mildew and its control in forest nurseries. Forestry 3:38-56
80. Yarwood CE (1957) Powdery mildews. Bot Rev 23:235-300
81. Yossifovitch M (1926) [Oak decline (Q. pedunculata) in the forests of Slavonia (Yougoslavia)] (in Serbo-Croatian). Rev Eaux Forêts. pp 288-291