Avoidance by early flushing: a new perspective on Dutch elm disease research

doi:10.3832/ifor0508-002

Avoidance by early flushing: a new perspective on Dutch elm disease research

iForest - Biogeosciences and Forestry, Volume 2, Issue 4, Pages 143-153 (2009)
doi: https://doi.org/10.3832/ifor0508-002
Published: Jul 30, 2009 - Copyright © 2009 SISEF

Review Papers

PDF Version

Full Text

Citation

Geo-mapping

European elms (Ulmus glabra Huds., Ulmus laevis Pall. and Ulmus minor Mill.) have been severely damaged and are still endangered by an alien hypervirulent pathogen, Ophiostoma ulmi s. l., agent of the Dutch elm disease (DED). Consequently, several ex situ clone collections have been established throughout Europe for elm breeding and conservation. In this paper we summarise the studies carried out within the EU project RESGEN CT96-78, which launched the EU-coordinated evaluation of these collections. Our aim was to analyse the variation in timing of bud burst and to acquire basic knowledge on the environmental control of this adaptive trait in European elms, under the hypothesis that DED susceptibility is related to spring phenology. The variation in the bud burst date of European elms among collections and years was explained by a phenological model assuming that the thermal time required for bud burst decreases exponentially with increasing chilling during winter down to a level where chilling requirement is fully met. According to the fitted curves, European elms have low dormancy and short chilling requirement for dormancy release. Although no simulation was performed, on the basis of the model applied we can hypothesise that under climate warming elms would flush earlier in most of Europe. The bud burst date was directly related to latitude and elevation in U. minor. The order of bud burst of clones from different origins was stable among years. The observed geographic trends were largely determined by differences in chilling requirements that increased with latitude and elevation. Susceptibility to DED varied greatly within U. minor and was directly correlated with geographic origin and bud burst date, southern and early flushing clones showing the least symptoms. Our results suggest that early flushing represents a mechanism of disease avoidance owing to asynchrony between host’s susceptible period and time of natural infection by DED vectors (Scolytus). This escape mechanism, combined with true resistance and avoidance owing to unattractiveness for the vector’s feeding, might be exploited for breeding DED-resistant clones of indigenous species.

Keywords

Bud burst phenology, DED, Disease escape, Elm, Ulmus, Growth-differentiation balance hypothesis

Authors’ address

(1)

Department of Plant Biology and Forest Genetics, Swedish University of Agricultural Sciences, Box 7080, S-750 07 Uppsala (Sweden)

(2)

Istituto per la Protezione delle Piante - CNR, Via Madonna del Piano 10, 50019 Sesto Fiorentino, FI (Italy)

Corresponding author

A Santini
a.santini@ipp.cnr.it

Citation

Ghelardini L, Santini A (2009). Avoidance by early flushing: a new perspective on Dutch elm disease research. iForest 2: 143-153. - doi: 10.3832/ifor0508-002

Academic Editor

Marco Borghetti

Paper history

Received: Mar 02, 2009
Accepted: Jul 16, 2009

First online: Jul 30, 2009
Publication Date: Jul 30, 2009
Publication Time: 0.47 months

Open Access

This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 86351
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 76318
Abstract Page Views: 3914
PDF Downloads: 5151
Citation/Reference Downloads: 70
XML Downloads: 898

Web Metrics
Days since publication: 5593
Overall contacts: 86351
Avg. contacts per week: 108.07

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)

Total number of cites (since 2009): 31
Average cites per year: 2.07

(no Plumx Metrics available for this paper)

Publication Metrics

by Dimensions ^©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

(1)

Banfield WM (1941)
Distribution by the sap stream of spores of three fungi that induce vascular wilt diseases of elm. Journal of Agricultural Research 62: 637-681.
Gscholar

(2)

Banfield WM (1968)
Dutch elm disease recurrence and recovery in American elm. Phytopathologische Zeitschrift 62: 21-60.
CrossRef | Gscholar

(3)

Binz TG, Canevascini G (1996)
Xylanases from the Dutch elm disease pathogens Ophiostoma ulmi and Ophiostoma novo ulmi. Physiological and Molecular Plant Pathology 49: 159-175.
CrossRef | Gscholar

(4)

Bonsen KJM, Scheffer RJ, Elgersma DM (1985)
Barrier zone formation as a resistance mechanism of elms to Dutch elm disease. IAWA Bulletin 6 (1): 71-77.
Gscholar

(5)

Brasier CM (1977)
Inheritance of pathogenicity and cultural characteristics in Ceratocystis ulmi. Hybridisation of protoperithecial and non-aggressive strains. Transactions of the British Mycological Society 68: 45-52.
Gscholar

(6)

Brasier CM (1982)
The future of Dutch elm disease in Europe. In: “Research on Dutch elm disease in Europe, 1982” (Burdekin DA ed). Forestry Commission Bulletin 60, pp. 96-104.
Gscholar

(7)

Brasier CM (2000)
Intercontinental spread and continuing evolution of the Dutch elm disease pathogens. In: “The elms: breeding conservation and disease management” (Dunn CP ed). Kluwer Academic Publisher, Boston, USA, pp. 61-72.
Gscholar

(8)

Cannell MGR, Smith RI (1983)
Thermal time, chill days and prediction of bud burst in Picea sitchensis. Journal of Applied Ecology 20: 951-963.
CrossRef | Gscholar

(9)

Cleland EE, Chuine I, Menzel A, Mooney HA, Schwarz MD (2007)
Shifting plant phenology in response to global change. Trends in Ecology and Evolution 22 (7): 357-365.
CrossRef | Gscholar

(10)

Collin E (2002a)
The role of hybridisation in gene conservation. In: “Noble Hardwoods network: Report of the fourth and fifth meetings” (Borelli S ed). International Plant Genetic Resources Institute, Rome, pp. 50-67.
Gscholar

(11)

Collin E (2002b)
Strategies and guidelines for the conservation of the genetic resources of Ulmus spp. In: “Noble Hardwoods network: Report of the fourth and fifth meetings” (Borelli S ed). International Plant Genetic Resources Institute, Rome, pp. 50-67.
Gscholar

(12)

Collin E, Rusanen M, Ackzell L, Bohnens J, de Aguiar A, Diamandis S, Franke A, Gil L, Harvengt L, Hollingsworth P, Jenkins G, Meier-Dinkel A, Mittempergher L, Musch B, Nagy L, Paques M, Pinon J, Piou, D, Rotach P, Santini A, Vanden Broeck A, Wolf H (2004)
Methods and progress in the conservation of elm genetic resources in Europe. Investigación agraria: Sistemas y Recursos Forestales 13 (1): 261-272.
Gscholar

(13)

Cogolludo-Agustín MA, Agúndez D, Gil L (2000)
Identification of native and hybrid elms in Spain using isozyme gene markers. Heredity 85: 157-166.
CrossRef | Gscholar

(14)

Dixon EB (1964)
Attack response of the smaller European elm bark beetle, Scolytus multistriatus, in confinement. Journal of Economic Entomology 57 (1): 170-172.
Gscholar

(15)

Duchesne LC, Jengand RS, Hubbes M (1985)
Accumulation of phytoalexins in Ulmus americana in response to infection by a nonaggressive strain of Ophiostoma ulmi. Canadian Journal of Botany 63: 678-680.
CrossRef | Gscholar

(16)

Dunn CP (2000)
The elms: breeding, conservation and disease management. Kluwer Academic Publishers, Boston, USA.
Gscholar

(17)

Elgersma DM (1970)
Length and diameter of xylem vessels as factors in resistance of elms to Ceratocystis ulmi. The Netherlands Journal of Plant Pathology 76: 179-182.
CrossRef | Gscholar

(18)

Elgersma DM (1982)
Susceptibility and possible mechanisms of resistance to Dutch elm disease. In: Proceedings of the “Dutch elm disease symposium and workshop” (Kondo ES, Hiratsuka Y, Denyer WBG eds). Winnipeg (Manitoba - Canada), 5-9 October 1981, pp. 169-177.
Gscholar

(19)

Ellmore GS, Ewers FW (1985)
Hydraulic conductivity in trunk xylem of elm, Ulmus americana. IAWA Bulletin 6: 303-307.
Gscholar

(20)

Eriksson G (2001)
Conservation of noble hardwoods in Europe. Canadian Journal of Forest Research 31: 577-587.
CrossRef | Gscholar

(21)

Et-Touil A, Rioux D, Mathieu FM, Bernier L (2005)
External symptoms and histopathological changes following inoculation of elms putatively resistant to Dutch elm disease with genetically close strains of Ophiostoma. Canadian Journal of Botany 83: 656-667.
CrossRef | Gscholar

(22)

Ghelardini L, Falusi M, Santini A (2006)
Variation in timing of bud-burst of Ulmus minor clones from different geographical origins. Canadian Journal of Forest Research 36: 1982-1991.
CrossRef | Gscholar

(23)

Ghelardini L (2007)
Bud burst phenology, dormancy release and susceptibility to Dutch elm disease in elms (Ulmus spp.). Doctoral thesis no. 2007:134, Acta Universitatis Agriculturae Sueciae, Uppsala, Sweden, pp. 52.
Gscholar

(24)

Gibbs JN (1978)
Intercontinental epidemiology of Dutch elm disease. Annual Review of Phytopathology 16: 287-307.
CrossRef | Gscholar

(25)

Goodall-Copestake WP, Hollingsworth ML, HollingsworthPM, Jenkins GI, Collin E (2005)
Molecular markers and ex situ conservation of the European elms (Ulmus spp.). Biological Conservation 122: 537-546.
CrossRef | Gscholar

(26)

Guries RP (2001)
Elms: past, present, and future In: Proceeding of the “National conference on wilt diseases of shade trees” (Ash CL ed), St. Paul, Minnesota (USA), 25-28 August 1999. APS Press, pp. 29-36.
Gscholar

(27)

Hannerz M (1998)
Genetic and seasonal variation in hardiness and growth rhythm in boreal and temperate conifers - a review and annotated bibliography. SkogForsk, Report No. 2, pp. 144.
Gscholar

(28)

Hänninen H, Kramer K (2007)
A framework for modelling the annual cycle of trees in boreal and temperate regions. Silva Fennica 41 (1): 167-205.
Gscholar

(29)

Heide OM (1993a)
Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiologia Plantarum 88: 531-540.
CrossRef | Gscholar

(30)

Heide OM (1993b)
Dormancy release in beech buds (Fagus sylvatica) requires both chilling and long days. Physiologia Plantarum 89: 187-191.
CrossRef | Gscholar

(31)

Herms DA, Mattson WJ (1992)
The dilemma of plants - to grow or defend. Quarterly Review of Biology 67 (4): 478.
CrossRef | Gscholar

(32)

Heybroek HM (1993)
The Dutch elm breeding program. In: “Dutch elm disease research: cellular and molecular approaches” (Sticklen MB, Sherald JL eds). Springer-Verlag, New York, USA, pp. 16-25.
Gscholar

(33)

IPCC (2007)
Climate change 2007: synthesis report. Core Writing Team (Pachauri RK, Reisinger A eds). IPCC, Geneva, Switzerland, pp. 104.
Gscholar

(34)

Jeng RS, Alfenas AC, Hubbes M, Dumas MT (1983)
Presence and accumulation of fungitoxic substances against Ceratocystis ulmi in Ulmus americana: possible relation to induced resistance. European Journal of Forest Pathology 13: 239-244.
CrossRef | Gscholar

(35)

Kramer K (1995)
Phenotypic plasticity of the phenology of seven European tree species in relation to climatic warming. Plant Cell and Environment 18: 93-104.
CrossRef | Gscholar

(36)

Linvill DE (1990)
Calculating chilling hours and chill units from daily maximum and minimum temperature observations. HortScience 25 (1): 14-16.
Gscholar

(37)

Lorio PL (1986)
Growth-differentiation balanca: a basis for understanding southern pine beetle-tree interactions. Forest Ecology and Management 14: 259-273.
Gscholar

(38)

MacHardy WE, Beckman CH (1973)
Water relations in American Elm infected with Ceratocystis ulmi. Phytopathology 63 (1): 98-103.
Gscholar

(39)

Marcelis LFM (1996)
Sink strength as a determinant of dry matter partitioning in the whole plant. Journal of Experimental Botany 47: 1281-1291.
Gscholar

(40)

McNabb HS, Heybroek HM, MacDonald, WL (1970)
Anatomical factors in resistance to Dutch elm disease. The Netherlands Journal of Plant Pathology 76: 196-204.
CrossRef | Gscholar

(41)

Mittempergher L, La Porta N (1991)
Hybridization studies in the Eurasian species of elm (Ulmus ssp.). Silvae Genetica 40: 237-243.
Gscholar

(42)

Mittempergher L, Santini A (2004)
The history of elm breeding. Investigación agraria: Sistemas y Recursos Forestales 13: 161-177.
Gscholar

(43)

Murray MB, Cannell MGR, Smith RI (1989)
Date of budburst of fifteen tree species in Britain following climatic warming. Journal of Applied Ecology 26: 693-700.
CrossRef | Gscholar

(44)

Murray MB, Smith RI, Leith ID, Fowler D, Lee HSJ, Friend AD, Jarvis PG (1994)
Effect of elevated CO₂ nutrition and climatic warming on bud phenology in Sitka spruce (Picea sitchensis) and their impact on the risk of frost damage. Tree Physiology 14: 691-706.
Online | Gscholar

(45)

Myking T, Heide OM (1995)
Dormancy release and chilling requirement of buds of latitudinal ecotypes of Betula pendula and B. pubescens. Tree Physiology 15: 697-704.
Online | Gscholar

(46)

Myking T, Skrøppa T (2007)
Variation in phenology and height increment of northern Ulmus glabra populations: implications for conservation. Scandinavian Journal of Forest Research 22: 369-374.
CrossRef | Gscholar

(47)

Neely D (1968)
Twig inoculations on American elm with Ceratocystis ulmi. Phytopathology 58: 1566-1570.
Gscholar

(48)

Neely D (1970)
Dutch elm disease symptom progression. Plant Disease Report 54: 127-129.
Gscholar

(49)

Newbanks D, Bosh A, Zimmermann MH (1983)
Evidence for xylem disfunction by embolization in Dutch elm disease. Phytopatology 73: 1060-1063.
CrossRef | Gscholar

(50)

Ouellette GB, Rioux D (1992)
Anatomical and physiological aspects of resistance to Dutch elm disease. In: “Defense mechanisms in woody plants against Fungi” (Blanchette A, Biggs R eds). Springer-Verlag, Berlin, pp. 257-305.
Gscholar

(51)

Ouellette GB, Rioux D, Simard M, Cherif M (2004a)
Ultrastructural and cytochemical studies of host and pathogens in some fungal wilt diseases: retro- and introspection towards a better understanding. Investigación agraria: Sistemas y Recursos Forestales 13 (1): 119-145.
Gscholar

(52)

Ouellette GB, Rioux D, Simard M, Chamberland H, Cherif M, Baayen RP (2004b)
Ultrastructure of the alveolar network and its relation to coating on vessel walls in elms infected by Ophiostoma novo-ulmi and in other plants affected with similar wilt diseases. Investigación agraria: Sistemas y Recursos Forestales 13 (1): 147-160.
Gscholar

(53)

Pajares JA (2004)
Elm breeding for resistance against bark beetles. Investigación agraria: Sistemas y Recursos Forestales 13 (1): 207-215.
Gscholar

(54)

Pinon G, Husson C, Collin E (2005)
Susceptibility of native French elm clones to Ophiostoma novo-ulmi. Annals of Forest Science 62: 689-696.
CrossRef | Gscholar

(55)

Pomerleau R (1965)
The period of susceptibility of Ulmus americana to Ceratocystis ulmi under conditions prevailing in Quebec. Canadian Journal of Botany 43: 787-792.
CrossRef | Gscholar

(56)

Pomerleau R (1968)
Progression et localisation de l’infection par le Ceratocystis ulmi dans l’orme d’Ameérique. Phytopathologische Zeitschrift 63: 301-327.
CrossRef | Gscholar

(57)

Pope SA (1943)
Some studies on the Dutch elm disease and the causal organism. Doctoral Thesis, Cornell University, Ithaca (NY), USA.
Gscholar

(58)

Richards WC (1993)
Cerato-ulmin: a unique wilt toxin of instrumental importance in the development of Dutch elm disease In: “Dutch elm disease research: cellular and molecular approaches” (Sticklen M, J. Sherald J eds). Springer Verlag, New York, USA, pp. 89-151.
Gscholar

(59)

Rioux D (1996)
Compartmentalization in trees: new findings during the study of Dutch elm disease. In: “Histology, ultrastructure and molecular cytology of plant-microorganism interactions” (Nicole M, Gianinazzi-Pearson V eds). Kluwer Academic, Dordrecht, The Netherlands, pp. 211-225.
Gscholar

(60)

Rioux D, Ouellette GB (1989)
Light microscope observations of histological changes induced by Ophiostoma ulmi in various non-host trees and shrubs. Canadian Journal of Botany 67: 2335-2351.
CrossRef | Gscholar

(61)

Rioux D, Ouellette GB (1991a)
Barrier zone formation in host and nonhost trees inoculated with Ophiostoma ulmi. I. Anatomy and histochemistry. Canadian Journal of Botany 69: 2055-2073.
CrossRef | Gscholar

(62)

Rioux D, Ouellette GB (1991b)
Barrier zone formation in host and nonhost trees inoculated with Ophiostoma ulmi. II. Ultrastructure. Canadian Journal of Botany 69: 2074-2083.
CrossRef | Gscholar

(63)

Rioux D, Nicole M, Simard M, Ouellette GB (1998)
Immunocytochemical evidence that secretion of pectin occurs during gel (gum) and tylosis formation in trees. Phytopathology 88(6): 494-505.
CrossRef | Gscholar

(64)

Rohring E (1996)
Elms in Europe: ecology and Dutch elm disease. Forstarchiv 67: 179-198.
Gscholar

(65)

Rudinsky JA (1962)
Ecology of Scolytidae. Annual Review of Entomology 7: 327-348.
CrossRef | Gscholar

(66)

Sacchetti P, Tiberi R, Mittempergher L (1990)
Preference of Scolytus multistriatus (Marsham) during the gonad maturation phase between two species of elm. Redia 73: 347-354.
Gscholar

(67)

Santamour FS (1979)
Resistance of Himalayan small-leaved elm to Dutch elm disease. Journal of Arboriculture 5: 110-112.
Gscholar

(68)

Santini A, Ghelardini L, Falusi M, Bohnens J, Buron M, Collin E, Solla A, Van den Broeck A (2004)
Vegetative bud-burst variability of European elms. In: “New approaches to elm conservation”. Proceedings of the 2^nd International Elm Conference, Valsaìn (Spain) 20-23 May 2003. Investigatión Agraria: Sistemas y Recursos Forestales 13 (1): 37-45.
Gscholar

(69)

Santini A, Fagnani A, Ferrini F, Ghelardini L, Mittempergher L (2005)
Variation among Italian and French elm clones in their response to Ophiostoma novo-ulmi inoculation. Forest Pathology 35: 183-193.
CrossRef | Gscholar

(70)

Santini A, La Porta N, Ghelardini, L. Mittempergher L (2008)
Breeding against Dutch elm disease adapted to the Mediterranean climate. Euphytica 163: 45-56.
CrossRef | Gscholar

(71)

Savolainen O, Pyhajarvi K, Knurr T (2007)
Gene flow and local adaptation in trees. Annual Review of Ecology, Evolution and Systematics 38: 595-619.
CrossRef | Gscholar

(72)

Sengonca C, Leisse N (1984)
Significance of bark beetles (Col. Scolytidae) in the spread of the Dutch Elm Disease in the area of Euskirchen. Journal of Applied Entomology 98 (4): 413-423.
Gscholar

(73)

Shigo AL (1982)
Dutch elm disease: a CODIT perspective In: Proceedings of the “Dutch elm disease symposium and workshop” (Kondo ES, Hiratsuka Y, Denyer WBG eds). Winnipeg (Manitoba - Canada) 5-9 October 1981, pp. 151-168.
Gscholar

(74)

Shigo AL (1984)
Compartmentalization: a conceptual framework for understanding how trees grow and defend themselves. Annual Review of Phytopathology 22: 189-214.
CrossRef | Gscholar

(75)

Shigo AL, Tippet JT (1981)
Compartmentalization of America elm tissues infected with Ceratocystis ulmi. Plant Disease 65: 715-718.
Gscholar

(76)

Sinclair WA, Campana RJ (1978)
Dutch elm disease, perspectives after 60 years. Cornell University Agricultural Experiment Station, Search (Agriculture) 8: 1-52.
Gscholar

(77)

Sinclair WA, Zahand JP, Melching JB (1975)
Anatomical markers for resistance of Ulmus americana to Ceratocystis ulmi. Phytopathology 65: 349-352.
CrossRef | Gscholar

(78)

Smalley EG (1963)
Seasonal fluctuations in susceptibility of young elm seedlings to Dutch elm disease. Phytopathology 53: 846-853.
Gscholar

(79)

Smalley EB, Guries RP (1993)
Breeding elms for resistance to Dutch elm disease. Annual Review of Phytopathology 31: 325-352.
CrossRef | Gscholar

(80)

Smalley EB, Guries RP (2000)
Asian elms: source of disease and pest resistance In: “The elms: breeding, conservation, and disease management” (Dunn C ed). Kluver Academic Publishers, Boston, USA, pp. 215-230.
Gscholar

(81)

Smalley EB, Kais AG (1966)
Seasonal variation in the resistance of various elm species to Dutch elm disease. In: “Breeding pest-resistant trees” (Gerhold HD, Schreiner EJ, Mc Dermott RE, Winieski JA eds). Pergamon Press, Elmsford, NY (USA), pp. 279-292.
Gscholar

(82)

Solla A, Gil L (2002)
Xylem vessel diameter as a factor in resistance of Ulmus minor to Ophiostoma novo-ulmi. Forest Pathology 32: 123-134.
CrossRef | Gscholar

(83)

Solla A, Bohnens J, Collin E, Diamantis S, Franke A, Gil L, Burón M, Santini A, Mittempergher L, Pinon J, Van den Broek A (2005a)
Screening European elms for resistance to Ophiostoma novo-ulmi. Forest Science 51 (2): 134-141.
Gscholar

(84)

Solla A, Martin JA, Corral P, Gil L (2005b)
Seasonal changes in wood formation of Ulmus pumila and U. minor and its relation with Dutch elm disease. New Phytologist 166 (3): 1025-1034.
CrossRef | Gscholar

(85)

Sticklen MB, Bolyard MG, Hajela RK, Duchesne LC (1991)
Molecular and cellular aspects of Dutch elm disease. Phytoprotection 72: 1-13.
Gscholar

(86)

Stipes RJ, Campana R (1981)
Compendium of elm diseases. American Phytopathological Society, St. Paul, MN (USA), pp. 66.
Gscholar

(87)

Sutherland ML, Pearson S, Brasier CM (1997)
The influence of temperature and light on defoliation levels of elm by Dutch elm disease. Epidemiology 87 (6): 576-581.
Gscholar

(88)

Takai S, Kondo ES (1979)
Seasonal development of Dutch elm disease on white elms in Central Ontario, Canada. I. Following wound inoculation. Canadian Journal of Botany 57: 341-352.
CrossRef | Gscholar

(89)

Tchernoff V (1965)
Methods for screening and for the rapid selection of elms for resistance to Dutch elm disease. Acta Botanica Netherlandica 14: 409-452.
Gscholar

(90)

Temple B, Horgen PA (2000)
Biological roles for cerato-ulmin, a hydrophobin secreted by the elm pathogens, Ophiostoma ulmi and O. novo-ulmi. Mycologia 92 (1): 1-9.
CrossRef | Gscholar

(91)

Townsend AM (1971)
Relative resistance of diploid Ulmus species to Ceratocystis ulmi. Plant Disease Reporter 55: 980-982.
Gscholar

(92)

Ware G (1995)
Little-known elms from China: landscape tree possibilities. Journal of Arboriculture 21: 284-288.
Gscholar

(93)

Webber JF (2000)
Insect vector behaviour and the evolution of Dutch elm disease. In: “The elms: breeding, conservation and disease management” (Dunn CP ed). Kluwer Academic Publishers, Boston, USA, pp. 47-60.
Gscholar

(94)

Webber JF (2004)
Experimental studies on factors influencing the transmission of Dutch elm disease. Investigación agraria: Sistemas y Recursos Forestales 13 (1): 197-205.
Gscholar

(95)

Webber JF, Brasier CM (1984)
The transmission of Dutch elm disease: a study of the process involved. In: “Invertebrate-microbial interactions” (Anderson JM, Rayner ADM, Walton D eds). Cambridge University Press, Cambridge, UK, pp. 271-306.
Gscholar

(96)

Whiteley RE, Black-Samuelsson S, Jansson G (2003)
Within and between populations variation in adaptive traits in Ulmus laevis Pall., the European white elm. Forest Genetics 10 (4): 313-323.
Gscholar

(97)

Worrall J, Mergen F (1967)
Environmental and genetic control of dormancy in Picea abies. Physiologia Plantarum 20: 733-745.
CrossRef | Gscholar

(98)

Zimmermann MH, McDonough J (1978)
Dysfunction in the flow of food. In: “Plant disease - an advanced treatise. Vol III. How plants suffer from disease” (Horsfall JG, Cowling ED eds). Academic Press, New York, USA, pp. 117-140.
Gscholar

(99)

Zalapa JE, Brunet J, Guries RP (2007)
Hybridization and introgression patterns between native red elm (Ulmus rubra Muhl.) and exotic, invasive Siberian elm (Ulmus pumila L.) examined using species-specific microsatellite markers. In: Proceedings of “CONGEN3: The Third International Conservation Genetics Symposium”, New York (USA) 27-29 September 2007, pp. 20.
Gscholar

(100)

Zalapa JE, Brunet J, Guries RP (2009)
Patterns of hybridisation and introgression between invasive Ulmus pumila (Ulmaceae) and native U. rubra. American Journal of Botany 96: 116-1128.
CrossRef | Gscholar

iForest - Biogeosciences and Forestry

Contents

Search

Journal Info

Journal Subjects and Fields

For Authors

For Reviewers

For Readers

SISEF Publishing

Search iForest Contents