Interactive effects of drought and pathogens in forest trees

This review synthesizes the available knowledge on drought-disease interactions in forest trees with a focus on (1) evidence and patterns of drought-disease interactions, (2) current understanding of processes and mechanisms, and (3) three well documented cases studies. The first part is based on the analysis of a database of slightly more than one hundred studies, obtained by keyword searches combining drought, diseases or pathogens, and forest trees. A large majority of published studies referred to a positive association between drought and disease, i.e. disease favoured by drought or drought and disease acting synergistically on tree health status, with a predominance of canker/dieback diseases, caused by pathogens like Botryosphaeria, Sphaeropsis, Cytospora and Biscognauxia (Hypoxylon). The type of disease-related variables (incidence vs. severity) and the intensity and timing of water stress were shown to be significant factors affecting the drought- infection interaction. Interactions with other abiotic stresses and species-specific and genetic effects, related to host or pathogen, have also been reported. Direct effects of drought on pathogens are generally negative, although most fungal pathogens exhibit an important plasticity and can grow at water potentials well below the minimum for growth of their host plants. Studies on indirect effects of drought on pathogens through other community interactions are still relatively scarce. Positive drought-infection effects can mostly be explained by indirect effects of drought on host physiology. The predisposition and the multiple stress hypotheses are presented, as well as recent developments in the study of the molecular basis of abiotic and biotic stress, and their interactions. Sphaeropsis sapinea on pines, Biscognauxia mediterranea on oaks and root pathogens in declines associated with drought provide illustrative examples, treated as case studies, of pathogens of current significance associated with drought. The conclusion highlights some knowledge gaps, e.g. the role of latent parasites and the shift to a pathogenic stage, or the genetics of some fungal groups. The need for prevention of pathogen dispersal, especially crucial in the case of latent pathogens, is emphasized.

[1]  G. W. Peterson Infection, Epidemiology, and Control of Diplodia Blight of Austrian, Ponderosa, and Scots Pines , 1977 .

[2]  Brent R. Frey,et al.  Predicting landscape patterns of aspen dieback: mechanisms and knowledge gaps , 2004 .

[3]  Lynne Boddy,et al.  Effect of temperature and water potential on growth rate of wood-rotting basidiomycetes , 1983 .

[4]  Jonathan D. G. Jones,et al.  Plant pathogens and integrated defence responses to infection , 2001, Nature.

[5]  D. Tilman,et al.  Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease , 2002 .

[6]  A. Görg,et al.  Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. , 2003, Environmental microbiology.

[7]  F. Asiegbu,et al.  Pathogen-inducible cDNAs from the interaction of the root rot fungus Heterobasidion annosum with Scots pine (Pinus sylvestris L.) , 2005 .

[8]  L. Nageleisen,et al.  Le dépérissement actuel de feuillus divers : hêtre, merisier, alisier torminal, érable sycomore, peuplier, châtaignier, charme, aulne glutineux , 1994 .

[9]  E. Smalley,et al.  The development of Hypoxylon canker of Populus tremuloides: role of interacting environmental factors , 1974 .

[10]  D. Schoeneweiss Predisposition, Stress, and Plant Disease , 1975 .

[11]  T. Burgess,et al.  Multiple gene genealogies and microsatellite markers reflect relationships between morphotypes of Sphaeropsis sapinea and distinguish a new species of Diplodia. , 2003, Mycological research.

[12]  J. Pera,et al.  Pathogenicity of fungi isolated from Quercus suber in Catalonia (NE Spain) , 2000 .

[13]  J. Rogers,et al.  Biscogniauxia and Camillea in Mexico , 1993 .

[14]  A. Alves,et al.  Botryosphaeria corticola, sp. nov. on Quercus species, with notes and description of Botryosphaeria stevensii and its anamorph, Diplodia mutila , 2004 .

[15]  M. Windham,et al.  Light intensity and drought stress as predisposition factors for dogwood anthracnose , 1995 .

[16]  B. Clinton,et al.  CANOPY GAP CHARACTERISTICS AND DROUGHT INFLUENCES IN OAK FORESTS OF THE COWEETA BASIN , 1993 .

[17]  G. Stanosz,et al.  Persistence of Sphaeropsis sapinea on or in asymptomatic shoots of red and jack pines , 1997 .

[18]  T. Jung,et al.  Phytophthora quercina sp. nov., causing root rot of European oaks , 1999 .

[19]  M. Wingfield,et al.  Genotypic Diversity of Sphaeropsis sapinea from South Africa and Northern Sumatra. , 2000, Plant disease.

[20]  D. Eamus,et al.  Water, turgor and osmotic potentials of fungi. , 1986 .

[21]  J. S. Murray Death of bark in Acer pseudoplatanus associated with drought , 1978 .

[22]  B. Marçais,et al.  Soil factors associated with infection by Collybia fusipes and decline of oaks , 2003 .

[23]  A. Rayner DIAMOND‐BARK DISEASES OF SYCAMORE IN BRITAIN , 1980 .

[24]  G. S. Puritch,et al.  Effect of Water Stress on the Rate of Non-suberized Impervious Tissue Formation Following Wounding in Abies grandis , 1975 .

[25]  P. Manion,et al.  Antifungal compounds in aspen: effect of water stress , 1994 .

[26]  Y. Hadar,et al.  Variation among New Zealand isolates of Sphaeropsis sapinea , 2002 .

[27]  C. Chou Crown wilt of Pinus radiata associated with Diplodia pinea infection of woody stems. , 1987 .

[28]  M. Morelet,et al.  SPHAEROPSIS SAPINEA UN NOUVEAU PROBLÈME SANITAIRE DES PINS EN FRANCE , 1991 .

[29]  P. Vivin,et al.  Differences in drought resistance among 3 deciduous oak species grown in large boxes , 1993 .

[30]  Paoletti,et al.  Pre- and post-inoculation water stress affects Sphaeropsis sapinea canker length in Pinus halepensis seedlings , 2001 .

[31]  B. Marçais,et al.  Inoculation of Mature Pedunculate Oaks (Quercus robur) with the Root Rot Fungus Collybia fusipes: Relationships with Tree Vigour and Soil Factors , 2003, European Journal of Plant Pathology.

[32]  N. Blaker Predisposing Effects of Soil Moisture Extremes on the Susceptibility of Rhododendron to Phytophthora Root and Crown Rot , 1981 .

[33]  N. Paul,et al.  Effects of rust and post‐infection drought on photosynthesis, growth and water relations in groundsel , 1984 .

[34]  M. Wingfield,et al.  Circumscription of Botryosphaeria species associated with Proteaceae based on morphology and DNA sequence data. , 2003, Mycologia.

[35]  M. Ostry,et al.  Sphaeropsis sapinea cankers on stressed red and jack pines in Minnesota and Wisconsin. , 1990 .

[36]  E. Turco,et al.  Dendroclimatic analysis of "Quercus robur" infected with "Fusarium eumartii" , 2002 .

[37]  P. Manion,et al.  Tree Disease Concepts , 1981 .

[38]  M. Johansson,et al.  Resistance of Picea abies seedlings to infection by Heterobasidion annosum in relation to drought stress , 1992 .

[39]  R. Bruck Interacting environmental factors associated with the incidence of hypoxylon canker on trembling aspen , 1980 .

[40]  M. Wingfield,et al.  Conidial dispersal of Sphaeropsis sapinea in three climatic regions of South Africa. , 1987 .

[41]  J. Sutton,et al.  High temperature, darkness, and drought predispose black spruce seedlings to gray mold , 1994 .

[42]  K. Wahlstroem,et al.  Spread of Armillaria spp. and Heterobasidion annosum in Norway spruce exposed to drought, irrigation and fertilization , 1994 .

[43]  J. P. Grime,et al.  Biodiversity and Ecosystem Functioning: Current Knowledge and Future Challenges , 2001, Science.

[44]  A. Ragazzi,et al.  Water stress and the development of cankers by Diplodia mutila on Quercus robur , 1999 .

[45]  L. Vaillancourt,et al.  Detection of Latent Sphaeropsis sapinea Infections in Austrian Pine Tissues Using Nested-Polymerase Chain Reaction. , 2003, Phytopathology.

[46]  G. Stanosz,et al.  Sphaeropsis sapinea Morphotypes Differ in Aggressiveness, but Both Infect Nonwounded Red or Jack Pines. , 1997, Plant disease.

[47]  F. Podger,et al.  The Role of Phytophthora Cinnamomi in Australian and New Zealand Forests , 1972 .

[48]  R. Valentini,et al.  Influence of water relations on Quercus cerris-Hypoxylon mediterraneum interaction: a model of drought-induced susceptibility to a weakness parasite. , 1994, Tree physiology.

[49]  C. Crist,et al.  The influence of controlled stresses on susceptibility of European white birch stems to attack by Botryosphaeria dothidea. , 1975 .

[50]  A. R. Stage,et al.  Climate: A Factor in the Origin of the Pole Blight Disease of Pinus Monticola Dougl , 1971 .

[51]  E. Hansen,et al.  Phytophthora species in oak forests of north-east France , 1999 .

[52]  P. Schweizer,et al.  Heat-induced resistance in barley to powdery mildew (Blumeria graminisf.sp.hordei) is associated with a burst of active oxygen species , 1998 .

[53]  A. Vannini,et al.  Development of a Polymerase Chain Reaction (PCR) assay for the specific detection of Biscogniauxia mediterranea living as an endophyte in oak tissues , 2001 .

[54]  J. Boyer Biochemical and biophysical aspects of water deficits and the predisposition to disease. , 1995, Annual review of phytopathology.

[55]  W. Jacobi,et al.  Effects of water stress on Thyronectria canker of honeylocusts , 1989 .

[56]  P. Reich,et al.  Diversity and Productivity in a Long-Term Grassland Experiment , 2001, Science.

[57]  T. Jung,et al.  Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease , 2000 .

[58]  H. Smith,et al.  The role of latent Sphaeropsis sapinea infections in post-hail associated die-back of Pinus patula , 2002 .

[59]  M. A. Palmer Isolate types of Sphaeropsis sapinea associated with main stem cankers and top-kill of Pinus resinosa in Minnesota and Wisconsin , 1991 .

[60]  C. Delatour,et al.  Contribution à l'étude du dépérissement du chêne : pathologie racinaire en forêt de Tronçais , 1985 .

[61]  C. Brasier,et al.  Phytophthora cinnamomi and oak decline in southern Europe. Environmental constraints including climate change , 1996 .

[62]  B. Schmid,et al.  Diversity-dependent production can decrease the stability of ecosystem functioning , 2002, Nature.

[63]  J. McPartland Hyphal morphology of Botryosphaeria dothidea in vessels of unstressed and drought-stressed stems of Betula alba , 1984 .

[64]  W. Flückiger,et al.  Effects of air pollution and water stress on leaf blight and twig cankers of London planes [Platanus×acerifolia (Ait.) Willd.] caused by Apiognomonia veneta (Sacc. & Speg.) Höhn. , 1991 .

[65]  W. J. Shields,et al.  Soil nutrient levels and pH associated with Armillariellamellea on conifers in northern Idaho , 1979 .

[66]  E. Kruger,et al.  Effects of Moderate Water Stress on Disease Development by Sphaeropsis sapinea on Red Pine. , 1997, Phytopathology.

[67]  J. McLaughlin,et al.  Distribution, hosts, and site relationships of Armillaria spp. in central and southern Ontario , 2001 .

[68]  J. Rogers,et al.  The genus Biscogniauxia , 1998 .

[69]  M. Gleason,et al.  Duration of Water Stress Affects Development of Sphaeropsis Canker on Scots Pine , 1997, Arboriculture & Urban Forestry.

[70]  G. Salcedo,et al.  Biotic and abiotic stress can induce cystatin expression in chestnut , 2000, FEBS letters.

[71]  G. Stanosz,et al.  Primers for amplification of mt SSU rDNA, and a phylogenetic study of Botryosphaeria and associated anamorphic fungi. , 2001 .

[72]  J. Elkinton,et al.  Pathogenicity and virulence. , 2004, Journal of invertebrate pathology.

[73]  W. Jacobi,et al.  Effects of environmental stress on the development of Cytospora canker of aspen , 1996 .

[74]  Carl Gunnar Fossdal,et al.  Effects of Rhizoctonia infection and drought on peroxidase and chitinase activity in Norway spruce (Picea abies). , 2004, Physiologia plantarum.

[75]  J. Peñuelas,et al.  Drought-induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions , 2004 .

[76]  D. Smith,et al.  Water stress and Sphaeropsissapinea as a latent pathogen of red pine seedlings. , 2001, The New phytologist.

[77]  E. Hansen,et al.  Three new species of Phytophthora from European oak forests , 2002 .

[78]  P. Kuiper,et al.  Is there a gas (general adaptation syndrome) response to various types of environmental stress? , 1996, Biologia Plantarum.

[79]  P. Bachi,et al.  Enhancement of Sphaeropsis sapinea stem invasion of pines by water deficits , 1985 .

[80]  R. Blanchette,et al.  Differences in conidial morphology among isolates of Sphaeropsis sapinea , 1985 .

[81]  D. Redfern The effect of wood moisture on infection of Sitka spruce stumps by basidiospores of Heterobasidion annosum , 1993 .

[82]  A. Gould,et al.  The Effect of Moisture and Sunlight on the Severity of Dogwood Anthracnose in Street Trees , 1994, Arboriculture & Urban Forestry.

[83]  C. Chou Penetration of young stems of Pinus radiata by Diplodia pinea , 1978 .

[84]  E. Hogg,et al.  Growth and dieback of aspen forests in northwestern Alberta, Canada, in relation to climate and insects , 2002 .

[85]  R. Fluhr,et al.  The role of calcium and activated oxygens as signals for controlling cross-tolerance. , 2000, Trends in plant science.

[86]  T. Jung,et al.  First records of soilborne Phytophthora species in Swedish oak forests , 2003 .

[87]  J. Koricheva,et al.  Insect performance on experimentally stressed woody plants: a meta-analysis. , 1998, Annual review of entomology.

[88]  Z. Solel,et al.  Enhancement of sphaeropsis canker of aleppo pine by the Israeli pine bast scale , 2005, Phytoparasitica.

[89]  R. Valentini,et al.  Impact of drought and Hypoxylon mediterraneum on oak decline in the Mediterranean region , 1996 .

[90]  Zhonghua Ma,et al.  Effects of Water Stress on Botryosphaeria Blight of Pistachio Caused by Botryosphaeria dothidea. , 2001, Plant disease.

[91]  P. Manion,et al.  Amino acid content of water-stressed plantlets of Populus tremuloides clones in relation to clonal susceptibility to Hypoxylon mammatum in vitro. , 1990 .

[92]  L. Boddy,et al.  Fungal colonization of attached beech branches , 1988 .

[93]  A. Alves,et al.  Botryosphaeria corticola, sp. nov. on Quercus species, with notes and description of Botryosphaeria stevensii and its anamorph, Diplodia mutila. , 2004, Mycologia.

[94]  A. M. Waterman Diplodia pinea the cause of a disease of hard Pines. , 1943 .

[95]  A. Lehtijärvi,et al.  EFFECTS OF IRRIGATION, FERTILIZATION AND DROUGHT ON THE OCCURRENCE OF LOPHODERMIUM PICEAE IN PICEA ABIES NEEDLES , 1999 .

[96]  R. Irwin,et al.  Predicting Armillaria ostoyae infection levels in black spruce plantations as a function of environmental factors , 1997 .

[97]  W. Swart,et al.  RAPD marker and isozyme characterization of Sphaeropsis sapinea from diverse coniferous hosts and locations , 1999 .

[98]  Z. Solel,et al.  Effect of water stress in cypress on the development of cankers caused by Diplodia pinea f.sp. cupressi and Seiridium cardinale. , 1989 .

[99]  Jian-Kang Zhu,et al.  Cell Signaling during Cold, Drought, and Salt Stress Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000596. , 2002, The Plant Cell Online.

[100]  D. Klessig,et al.  Osmotic Stress Induces Rapid Activation of a Salicylic Acid–Induced Protein Kinase and a Homolog of Protein Kinase ASK1 in Tobacco Cells , 2000, Plant Cell.

[101]  D. Crombie,et al.  A comparison of water relations, visual symptoms, and changes in stem girth for evaluating impact of Phytophthoracinnamomi dieback on Eucalyptusmarginata , 1990 .

[102]  M. Daughtrey,et al.  Dogwood Anthracnose: A New Disease Threatens Two Native Cornus Species , 1994 .

[103]  T. Burgess,et al.  Comparison of genotypic diversity in native and introduced populations of Sphaeropsis sapinea isolated from Pinus radiata , 2001 .

[104]  G. Stanosz,et al.  Association of mortality of recently planted seedlings and established saplings in red pine plantations with Sphaeropsis collar rot. , 1996 .

[105]  M. Beck,et al.  Host nutritional status: the neglected virulence factor , 2004, Trends in Microbiology.

[106]  J. Stenlid,et al.  Effects of clear-cutting, thinning, and wood moisture content on the susceptibility of Norway spruce stumps to Heterobasidion annosum , 1998 .

[107]  M. Becker,et al.  LE DÉPÉRISSEMENT DU CHÊNE DES ANNÉES 1980 DANS LE CENTRE DE LA FRANCE, POINT DE DÉPART D'UNE MEILLEURE COMPRÉHENSION DE L'ÉQUILIBRE ET DE LA PRODUCTIVITÉ DE LA CHÊNAIE , 1994 .

[108]  D. Schoeneweiss CHAPTER 2 – WATER STRESS AS A PREDISPOSING FACTOR IN PLANT DISEASE , 1978 .

[109]  G. Platas,et al.  Identification of an endophytic Nodulisporium sp. from Quercus ilex in central Spain as the anamorph of Biscogniauxia mediterranea by rDNA sequence analysis and effect of different ecological factors on distribution of the fungus , 2001 .

[110]  M. Desprez-Loustau,et al.  Effects of variable root damage caused by Phytophthora cinnamomi on water relations of chestnut saplings , 2001 .

[111]  J. Roelofs,et al.  Nutrient availability in Corsican pine stands in the Netherlands and the occurrence of Sphaeropsis sapinea: a field study. , 1992 .

[112]  A. Termorshuizen,et al.  Geographical distribution of the Armillaria species in The Netherlands in relation to soil type and hosts , 1994 .

[113]  A. Vannini,et al.  Factors affecting discharge and germination of ascospores of Hypoxylon mediterraneum (De Not.) Mill. , 1996 .

[114]  J. Grégoire,et al.  Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis , 2004, Springer Netherlands.

[115]  K. Klepzig,et al.  Effects of available water on growth and competition of southern pine beetle associated fungi. , 2004, Mycological research.

[116]  L. Klosterman A research school of chemistry in the nineteenth century: Jean Baptiste Dumas and his research students , 1985 .

[117]  L. Boddy,et al.  Strip-cankering of beech (Fagus sylvatica): Pathology and distribution of symptomatic trees. , 1998, The New phytologist.

[118]  J. Colhoun,et al.  Effects of Environmental Factors on Plant Disease , 1973 .

[119]  N. Malajczuk,et al.  Influence of water potential on growth and cultural characteristics of Phytophthora cinnamomi , 1979 .

[120]  E. Kruger,et al.  Sphaeropsis sapinea and Water Stress in a Red Pine Plantation in Central Wisconsin. , 1997, Phytopathology.

[121]  J. J. Grant,et al.  Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. , 2004, The Plant journal : for cell and molecular biology.

[122]  L. Nageleisen,et al.  Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe , 2006 .

[123]  B. C. Sutton The Coelomycetes. Fungi imperfecti with pycnidia, acervuli and stromata. , 1980 .

[124]  A. Ramaley,et al.  Factors Affecting Cytospora Canker Occurrence On Aspen , 1996, Arboriculture & Urban Forestry.

[125]  R. Fox,et al.  EFFECT OF WATER STRESS ON INFECTION BY SPECIES OF HONEY FUNGUS (ARMILLARIA MELLEA AND A. GALLICA) , 2003 .

[126]  Ds Crombie,et al.  Water relations of root-pruned jarrah (Eucalyptus marginata Donn ex Smith) saplings. , 1987 .

[127]  B. Clinton,et al.  Tree Growth and Mortality in a Southern Appalachian Deciduous Forest Following Extended Wet and Dry Periods , 2003 .

[128]  E. Kruger,et al.  Effects of Water Stress on Colonization of Poplar Stems and Excised Leaf Disks by Septoria musiva. , 1997, Phytopathology.

[129]  M. Morelet,et al.  Sur un cas de variabilité chez Sphaeropsis sapinea , 1993 .

[130]  W. Jacobi,et al.  Pathogenicity of Cytospora Fungi on Six Hardwood Species , 2000, Arboriculture & Urban Forestry.

[131]  A. Solla,et al.  Influence of water stress on Dutch elm disease symptoms in Ulmus minor , 2002 .

[132]  D. Klessig,et al.  MAPK cascades in plant defense signaling. , 2001, Trends in plant science.

[133]  M. Becker,et al.  Le dépérissement du chêne en forêt de Tronçais Les causes écologiques , 1982 .

[134]  N. Paul,et al.  Water-stress modifies intraspecific interference between rust (Puccinia-Lagenophorae Cooke)-infected and healthy groundsel (Senecio-Vulgaris L) , 1987 .

[135]  D. Werf,et al.  Effects of fertilization with ammonium sulphate and potassium sulphate on the development of Sphaeropsis sapinea in Corsican pine , 1991, Netherlands Journal of Plant Pathology.

[136]  S. Gregory Bark necrosis of Acer pseudoplatanus L. in northern Britain , 1982 .

[137]  H. Hirt,et al.  Reactive oxygen species: metabolism, oxidative stress, and signal transduction. , 2004, Annual review of plant biology.

[138]  J. M. Duniway Water Relations of Water Molds , 1979 .

[139]  L. Xiong,et al.  Disease Resistance and Abiotic Stress Tolerance in Rice Are Inversely Modulated by an Abscisic Acid–Inducible Mitogen-Activated Protein Kinase Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008714. , 2003, The Plant Cell Online.

[140]  J. E. Bier THE RELATION OF BARK MOISTURE TO THE DEVELOPMENT OF CANKER DISEASES CAUSED BY NATIVE, FACULTATIVE PARASITES: I. CRYPTODIAPORTHE CANKER ON WILLOW , 1959 .

[141]  D. Appel Canker Expansion on Water-Stressed Pin Oaks Colonized byEndothia gyrosa , 1984 .

[142]  A. Bent,et al.  Probing plant-pathogen interactions and downstream defense signaling using DNA microarrays , 2002, Functional & Integrative Genomics.

[143]  K. Britton Anthracnose infection of dogwood seedlings exposed to natural inoculum in western North Carolina , 1993 .

[144]  T. Jung,et al.  Isolation, identification and pathogenicity of Phytophthora species from declining oak stands , 1996 .

[145]  M. Williams,et al.  Growth of lesions of Phytophthoracinnamomi in stems and roots of jarrah (Eucalyptusmarginata) in relation to rainfall and stand density in mediterranean forest of Western Australia , 1995 .

[146]  Jun-jun Liu,et al.  A Class IV Chitinase Is Up-Regulated by Fungal Infection and Abiotic Stresses and Associated with Slow-Canker-Growth Resistance to Cronartium ribicola in Western White Pine (Pinus monticola). , 2005, Phytopathology.

[147]  L. Vaillancourt,et al.  Latent Infection of Austrian and Scots Pine Tissues by Sphaeropsis sapinea. , 2001, Plant disease.

[148]  A. Vannini,et al.  Water stress: A predisposing factor in the pathogenesis of Hypoxylon mediterraneum on Quercus cerris , 1991 .

[149]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[150]  Pm Wargo Consequences of environmental stress on oak: predisposition to pathogens , 1996 .

[151]  D. Maynard,et al.  Armillaria root disease, stand characteristics, and soil properties in young lodgepole pine , 1998 .

[152]  M. Wingfield,et al.  Biology and control of Sphaeropsis sapinea on Pinus species in South Africa , 1991 .

[153]  S. Moricca Phomopsis alnea, the cause of dieback of black alder in Italy , 2002 .

[154]  M. Wingfield,et al.  Characterisation of the ‘C’ morphotype of the pine pathogen Sphaeropsis sapinea , 2002 .

[155]  G. H. Hepting Climate and Forest Diseases , 1963 .

[156]  B. Marçais,et al.  Influence of water stress on susceptibility of red oak (Quercus rubra) to Phytophthora cinnamomi , 1993 .

[157]  D. Crombie,et al.  Effect of phloem water relations on the growth of Phytophthora cinnamomi in Eucalyptus marginata , 1987 .

[158]  A. Hagan,et al.  Canker of dogwood caused by Lasiodiplodia theobromae, a disease influenced by drought stress or cultivar selection. , 1991 .

[159]  S. Covert,et al.  Pine genes regulated by the necrotrophic pathogen Fusarium circinatum , 2004, Theoretical and Applied Genetics.

[160]  D M Griffin,et al.  WATER POTENTIAL AND WOOD-DECAY FUNGI , 1977 .

[161]  P. Ayres 11 – Growth Responses Induced by Pathogens and Other Stresses , 1991 .

[162]  T. Jung,et al.  Phytophthora pseudosyringae sp. nov., a new species causing root and collar rot of deciduous tree species in Europe. , 2003, Mycological research.

[163]  D. Reheul,et al.  Species richness and susceptibility to heat and drought extremes in synthesized grassland ecosystems: compositional vs physiological effects , 2004 .

[164]  A. McElrone,et al.  Interactive effects of water stress and xylem-limited bacterial infection on the water relations of a host vine. , 2003, Journal of experimental botany.

[165]  N. Breda,et al.  Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences , 2006 .

[166]  Jonathan I. Watkinson,et al.  Photosynthetic Acclimation Is Reflected in Specific Patterns of Gene Expression in Drought-Stressed Loblolly Pine1[w] , 2003, Plant Physiology.

[167]  M. Mackenzie,et al.  Effect of pruning intensity and season on Diplodia pinea infection of Pinus radiata stem through pruning wounds , 1988 .

[168]  Michael J. Wingfield,et al.  Botryosphaeria dothidea endophytic in Eucalyptus grandis and Eucalyptus nitens in South Africa , 1996 .

[169]  R. Papendick,et al.  Influence of Water Potential of Soils and Plants on Root Disease , 1972 .

[170]  B. Marçais,et al.  Hosts and distribution of Collybia fusipes in France and factors related to the disease's severity , 2002 .

[171]  T. Kirisits Fungal Associates of European Bark Beetles With Special Emphasis on the Ophiostomatoid Fungi , 2007 .

[172]  M. Wingfield,et al.  Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. , 2004, Mycologia.

[173]  G. Stanosz,et al.  Differences in Aggressiveness of Sphaeropsis sapinea RAPD Marker Group Isolates on Several Conifers. , 1999, Plant disease.

[174]  M. Desprez-Loustau,et al.  Effects of root damage associated with Phytophthora cinnamomi on water relations, biomass accumulation, mineral nutrition and vulnerability to water deficit of five oak and chestnut species , 2001 .

[175]  M. Wingfield,et al.  Effects of water stress on the development of cambial lesions caused by Cryphonectria cubensis on Eucalyptus grandis , 1992 .

[176]  R. Mittler,et al.  The Combined Effect of Drought Stress and Heat Shock on Gene Expression in Tobacco1 , 2002, Plant Physiology.

[177]  D. Schoeneweiss Role of environmental stress in diseases of woody plants. , 1981 .