Resistance to Dutch Elm Disease Reduces Presence of Xylem Endophytic Fungi in Elms (Ulmus spp.)

Efforts to introduce pathogen resistance into landscape tree species by breeding may have unintended consequences for fungal diversity. To address this issue, we compared the frequency and diversity of endophytic fungi and defensive phenolic metabolites in elm (Ulmus spp.) trees with genotypes known to differ in resistance to Dutch elm disease. Our results indicate that resistant U. minor and U. pumila genotypes exhibit a lower frequency and diversity of fungal endophytes in the xylem than susceptible U. minor genotypes. However, resistant and susceptible genotypes showed a similar frequency and diversity of endophytes in the leaves and bark. The resistant and susceptible genotypes could be discriminated on the basis of the phenolic profile of the xylem, but not on basis of phenolics in the leaves or bark. As the Dutch elm disease pathogen develops within xylem tissues, the defensive chemistry of resistant elm genotypes thus appears to be one of the factors that may limit colonization by both the pathogen and endophytes. We discuss a potential trade-off between the benefits of breeding resistance into tree species, versus concomitant losses of fungal endophytes and the ecosystem services they provide.

[1]  A. Solla,et al.  Analysis of Spanish populations of Ophiostoma ulmi and O. novo‐ulmi using phenotypic characteristics and RAPD markers , 2007 .

[2]  E. Müller,et al.  Conidiogenesis of Fusarium nivale and Rhynchosporium oryzae and its taxonomic implications , 2007, Netherlands Journal of Plant Pathology.

[3]  B. Schulz,et al.  The endophytic continuum. , 2005, Mycological research.

[4]  Kevin M. Clarke,et al.  Estimating Species Richness , 2005 .

[5]  M. Desprez-Loustau,et al.  Spatial variability of phyllosphere fungal assemblages: genetic distance predominates over geographic distance in a European beech stand (Fagus sylvatica) , 2012 .

[6]  A. Santini,et al.  The history of elm breeding , 2004 .

[7]  J. Miller,et al.  Effect of a Rugulosin-producing Endophyte in Picea glauca on Choristoneura fumiferana , 2008, Journal of Chemical Ecology.

[8]  M. Wedin,et al.  Endophytic fungi in European aspen (Populus tremula) leaves—diversity, detection, and a suggested correlation with herbivory resistance , 2010, Fungal Diversity.

[9]  H. Balslev,et al.  Light Converts Endosymbiotic Fungus to Pathogen, Influencing Seedling Survival and Niche-Space Filling of a Common Tropical Tree, Iriartea deltoidea , 2011, PloS one.

[10]  J. Berghout,et al.  Spread and persistence of a rugulosin-producing endophyte in Picea glauca seedlings. , 2008, Mycological research.

[11]  P. Crous,et al.  Systematic reappraisal of species in Phoma section Paraphoma, Pyrenochaeta and Pleurophoma , 2010, Mycologia.

[12]  J. Martín,et al.  Phenolic metabolites in the resistance of northern forest trees to pathogens — past experiences and future prospects , 2008 .

[13]  M. Coimbra,et al.  Exogenous phenol increase resistance of Ulmus minor to Dutch elm disease through formation of suberin-like compounds on xylem tissues , 2008 .

[14]  L. Bernier,et al.  Fungal colonization and host defense reactions in Ulmus americana callus cultures inoculated with Ophiostoma novo-ulmi. , 2009, Phytopathology.

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

[16]  M. Srivastava,et al.  Downregulation of high-isoelectric-point extracellular superoxide dismutase mediates alterations in the metabolism of reactive oxygen species and developmental disturbances in hybrid aspen. , 2006, The Plant journal : for cell and molecular biology.

[17]  P. Fuentes-Utrilla,et al.  Phylogeography: English elm is a 2,000-year-old Roman clone , 2004, Nature.

[18]  M. C. Quecine,et al.  Endophytic fungi associated with transgenic and non-transgenic cotton , 2011 .

[19]  Haiying Liang,et al.  Transgenic American elm shows reduced Dutch elm disease symptoms and normal mycorrhizal colonization , 2007, Plant Cell Reports.

[20]  B. C. Sutton,et al.  The Phoma and Ascohyta Species Described by Wollenweber and Hochapfel in Their Study on Fruit-Rotting , 1974 .

[21]  B. T. Linaldeddu,et al.  Physiological responses of cork oak and holm oak to infection by fungal pathogens involved in oak decline , 2009 .

[22]  G. Newcombe,et al.  Endophyte-mediated resistance against white pine blister rust in Pinus monticola , 2008 .

[23]  K. I. Ugland,et al.  Changes in the root‐associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing , 2012, Molecular ecology.

[24]  L. M. Carris,et al.  Endophytic Fungi in Grasses and Woody Plants: Systematics, Ecology and Evolution , 1996 .

[25]  Fragmented environment affects birch leaf endophytes. , 2007, The New phytologist.

[26]  R. Rodriguez,et al.  Stress tolerance in plants via habitat-adapted symbiosis , 2008, The ISME Journal.

[27]  L. Boddy,et al.  Fungal decomposition of attached angiosperm twigs I. Decay community development in ash, beech and oak. , 1990, The New phytologist.

[28]  K. Clay Fungal Endophytes of Grasses: A Defensive Mutualism between Plants and Fungi , 1988 .

[29]  R. Hammerschmidt,et al.  Phenolic Compounds and Their Role in Disease Resistance , 1992 .

[30]  David C. Tank,et al.  Bioactive Endophytes Warrant Intensified Exploration and Conservation , 2008, PloS one.

[31]  S. Powers,et al.  Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. , 2010, The New phytologist.

[32]  J. Martín,et al.  Antifungal effect and reduction of Ulmus minor symptoms to Ophiostoma novo-ulmi by carvacrol and salicylic acid , 2010, European Journal of Plant Pathology.

[33]  J. Turok,et al.  The Conservation of Elm Genetic Resources in Europe , 2000 .

[34]  P. Capretti,et al.  Endophytic presence of Discula quercina on Declining Quercus cerris , 1999 .

[35]  J. Webber A natural biological control of Dutch elm disease , 1981, Nature.

[36]  D. Tilman,et al.  Fungal endophytes limit pathogen damage in a tropical tree , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Maffei,et al.  An ascomycetous endophyte isolated from Mentha piperita L.: biological features and molecular studies , 2002, Mycologia.

[38]  B. Potts,et al.  A framework for community and ecosystem genetics: from genes to ecosystems , 2006, Nature Reviews Genetics.

[39]  M. Maffei,et al.  In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. , 2003, The New phytologist.

[40]  C. Gostinčar,et al.  Redefinition of Aureobasidium pullulans and its varieties , 2008, Studies in mycology.

[41]  K. Rodrigues The foliar fungal endophytes of the Amazonian palm Euterpe oleracea , 1994 .

[42]  R. Redman,et al.  Fungal Life-Styles and Ecosystem Dynamics: Biological Aspects of Plant Pathogens, Plant Endophytes and Saprophytes , 1997 .

[43]  J. Martín-García,et al.  ITS-based comparison of endophytic mycota in twigs of native Populus nigra and cultivated P. x euramericana (cv. I-214) stands in Northern Spain , 2011, Annals of Forest Science.

[44]  V. Pando,et al.  Factors influencing endophytic communities in poplar plantations , 2011 .

[45]  T. White Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , 1990 .

[46]  W. Tao,et al.  Interactions of Taxol‐producing endophytic fungus with its host (Taxus spp.) during Taxol accumulation , 2009, Cell biology international.

[47]  K. Treseder,et al.  Microbial communities and their relevance for ecosystem models: Decomposition as a case study , 2010 .

[48]  J. Martín,et al.  Phenological and histochemical changes of Ulmus minor due to root absorption of phenol: Implications for resistance to DED , 2010 .

[49]  K. Saikkonen Forest structure and fungal endophytes , 2007 .

[50]  T. Sieber Endophytic fungi in forest trees: are they mutualists? , 2007 .

[51]  Luis Gil,et al.  Metabolic fingerprinting allows discrimination between Ulmus pumila and U. minor, and between U. minor clones of different susceptibility to Dutch elm disease , 2008 .

[52]  G. Bills Isolation and analysis of endophytic fungal communities from woody plants. , 1996 .

[53]  S. Shapiro,et al.  An Analysis of Variance Test for Normality (Complete Samples) , 1965 .

[54]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[55]  W. A. Sinclair Anatomical Marker for Resistance of Ulmus americana to Ceratocystis ulmi , 1975 .

[56]  G. Carroll,et al.  Internal fungi in old-growth Douglas fir foliage , 1977 .

[57]  K. Hyde,et al.  Genetic variation of Alternaria alternata, an endophytic fungus isolated from Pinus tabulaeformis as determined by random amplified microsatelites (RAMS) , 2004 .

[58]  James Francis White,et al.  Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? , 2010, Physiologia plantarum.

[59]  G. Kovács,et al.  The Dark Side Is Not Fastidious – Dark Septate Endophytic Fungi of Native and Invasive Plants of Semiarid Sandy Areas , 2012, PloS one.

[60]  A. Arnold,et al.  Endophytic fungi as biocontrol agents of Theobroma cacao pathogens , 2008 .

[61]  G. Newcombe Endophytes in Forest Management: Four Challenges , 2011 .

[62]  T. Bruns,et al.  Quantifying microbial communities with 454 pyrosequencing: does read abundance count? , 2010, Molecular ecology.

[63]  O. Petrini,et al.  A comparative study of fungal endophytes in xylem and bark of Alnus species in England and Switzerland , 1990 .

[64]  T. Hoshino,et al.  Cold adaptation in the phytopathogenic fungi causing snow molds , 2009, Mycoscience.

[65]  D. Rioux,et al.  Barrier zone formation in host and nonhost trees inoculated with Ophiostoma ulmi. I. Anatomy and histochemistry , 1991 .

[66]  C. Pieterse,et al.  Plant immune responses triggered by beneficial microbes. , 2008, Current opinion in plant biology.

[67]  L. M. Carris,et al.  Fungal endophytes of living branch bases in several European tree species. , 1996 .

[68]  J. Vivanco,et al.  Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum , 2002 .

[69]  A. Solla,et al.  Seasonal changes in wood formation of Ulmus pumila and U. minor and its relation with Dutch elm disease. , 2005, The New phytologist.

[70]  B. Schulz,et al.  The endophyte-host interaction: a balanced antagonism? , 1999 .

[71]  L. Bernier,et al.  Identification and monitoring of Ulmus americana transcripts during in vitro interactions with the Dutch elm disease pathogen Ophiostoma novo-ulmi , 2010 .

[72]  S. Lumyong,et al.  A Phylogenetic Evaluation of Whether Endophytes Become Saprotrophs at Host Senescence , 2007, Microbial Ecology.

[73]  P. Gonthier,et al.  Fungal Endophytic Communities in Healthy and Declining Quercus robur L. and Q. cerris L. Trees in Northern Italy , 2003 .

[74]  Jonathan M. Chase,et al.  Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. , 2011, Ecology letters.

[75]  W. L. Araújo,et al.  Culturable endophytic filamentous fungi from leaves of transgenic imidazolinone-tolerant sugarcane and its non-transgenic isolines , 2010, Archives of Microbiology.

[76]  T. Sieber,et al.  Endophytic Fungi in Four Winter Wheat Cultivars (Triticum aestivum L.) Differing in Resistance Against Stagonospora nodorum (Berk.) Cast. & Germ. =Septoria nodorum (Berk.) Berk. , 1988 .

[77]  J. Martín,et al.  Bordered pit and ray morphology involvement in elm resistance to Ophiostoma novo-ulmi. , 2009 .

[78]  L. Gil,et al.  Identification of native and hybrid elms in Spain using isozyme gene markers , 2000, Heredity.

[79]  K. Saikkonen,et al.  Micro-fungi and invertebrate herbivores on birch trees: fungal mediated plant-herbivore interactions or responses to host quality , 2002 .

[80]  A. Solla,et al.  Caracterización histórica, ecológica, taxonómica y fitosanitaria de una olmeda relicta en Rivas-Vaciamadrid (Madrid) , 2006 .

[81]  J. Stone,et al.  Endophytic fungi in evergreen shrubs in western Oregon: A preliminary study , 1982 .

[82]  C. Dunn The Elms: "Breeding,Conservation, And Disease Management" , 2012 .

[83]  D. Rioux,et al.  Ultrastructural and cytochemical studies of host and pathogens in some fungal wilt diseases: retro- and introspection towards a better understanding of DED , 2004 .

[84]  T. Whitham,et al.  Host plant genetics affect hidden ecological players: links among Populus, condensed tannins, and fungal endophyte infection , 2005 .

[85]  P. Coley,et al.  Are tropical fungal endophytes hyperdiverse , 2000 .