iForest - Biogeosciences and Forestry


Seven Ulmus minor clones tolerant to Ophiostoma novo-ulmi registered as forest reproductive material in Spain

Juan Antonio Martín (1), Alejandro Solla (2), Martin Venturas (1), Carmen Collada (1), Jorge Domínguez (1), Eva Miranda (1), Pablo Fuentes (3), Margarita Burón (1), Salustiano Iglesias (4), Luis Gil (1)   

iForest - Biogeosciences and Forestry, Volume 8, Issue 2, Pages 172-180 (2015)
doi: https://doi.org/10.3832/ifor1224-008
Published: Aug 13, 2014 - Copyright © 2015 SISEF

Research Articles

Collection/Special Issue: 3rd International Elm Conference, Florence (Italy - 2013)
The elms after 100 years of Dutch Elm disease
Guest Editors: A. Santini, L. Ghelardini, E. Collin, A. Solla, J. Brunet, M. Faccoli, A. Scala, S. De Vries, J. Buiteveld

The Spanish elm programme began in 1986 in response to the devastating impact of Dutch elm disease on natural elm stands and urban trees. Its main objectives were to conserve remaining genetic resources and select and breed tolerant native elm genotypes. After 27 years of work conducting susceptibility trials on thousands of elm genotypes, the first seven tolerant Ulmus minor trees are now being registered by the Spanish Environmental Administration. This paper presents the results of the susceptibility tests on these clones and their distinctive genetic, morphological and phenological features. In all susceptibility trials the commercial “Sapporo Autumn Gold” clone, which is highly tolerant to O. novo-ulmi, was used as a control. The registered clones were named “Ademuz”, “Dehesa de la Villa”, “Majadahonda”, “Toledo”, “Dehesa de Amaniel”, “Retiro” and “Fuente Umbría”. The most tolerant clone was “Dehesa de Amaniel”, as its wilting values were below 5% during the two consecutive inoculation trials performed in Madrid. “Fuente Umbría”, tested over four consecutive years in Guadalajara and Palencia, was the Spanish clone with the most reliable tolerance level to O. novo-ulmi. The “Ademuz” and “Majadahonda” clones had the highest ornamental scores and are promising trees for use in urban environments and tree breeding for ornamental quality. These two genotypes showed a later bud burst phenology than the other U. minor clones, demonstrating suitability to areas with late frost events. The Spanish programme aims to substantially increase the range of tolerant native elms through new selections and crossings to gain a better understanding of the genetic basis of resistance.


Dutch Elm Disease, Breeding, Plant Release, Resistance, Invasive Species

Authors’ address

Juan Antonio Martín
Martin Venturas
Carmen Collada
Jorge Domínguez
Eva Miranda
Margarita Burón
Luis Gil
ETSI Montes, Universidad Politécnica de Madrid, Ciudad Universitaria s/n, E-28040 Madrid (Spain)
Alejandro Solla
Ingeniería Forestal y del Medio Natural, Universidad de Extremadura, Avenida Virgen del Puerto 2, E-10600 Plasencia (Spain)
Pablo Fuentes
Institute of Evolutionary Biology, The University of Edinburgh, West Mains Rd., Edinburgh EH9 9JT (United Kingdom)
Salustiano Iglesias
Dirección General de Desarrollo Rural y Política Forestal, Ministerio de Medio Ambiente y Medio Rural y Marino, c/ Ríos Rosas 24, E-28003 Madrid (Spain)

Corresponding author

Luis Gil


Martín JA, Solla A, Venturas M, Collada C, Domínguez J, Miranda E, Fuentes P, Burón M, Iglesias S, Gil L (2015). Seven Ulmus minor clones tolerant to Ophiostoma novo-ulmi registered as forest reproductive material in Spain. iForest 8: 172-180. - doi: 10.3832/ifor1224-008

Academic Editor

Alberto Santini

Paper history

Received: Dec 30, 2013
Accepted: May 21, 2014

First online: Aug 13, 2014
Publication Date: Apr 01, 2015
Publication Time: 2.80 months

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

Allué-Andrade JL (1990)
Atlas fitoclimático de España. Taxonomías [Phytoclimatic atlas of Spain. Taxonomy]. Instituto Nacional de Investigaciones Agrarias, Ministerio de Agricultura Pesca y Alimentación, Madrid, Spain. [in Spanish]
Aoun M, Jacobi V, Boyle B, Bernier L (2010)
Identification and monitoring of Ulmus americana transcripts during in vitro interactions with the Dutch elm disease pathogen Ophiostoma novo-ulmi. Physiological and Molecular Plant Pathology 74: 254-266.
CrossRef | Gscholar
Brasier CM, Kirk SA (2010)
Rapid emergence of hybrids between two subspecies of Ophiostoma novo-ulmi with a high level of pathogenic fitness. Plant Pathology 59: 186-199.
CrossRef | Gscholar
Buiteveld J, van der Werf B, Hiemstra JA (2014)
Comparison of commercial elm cultivars and promising unreleased Dutch clones for resistance to Ophiostoma novo-ulmi. iForest (early view).
CrossRef | Gscholar
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
Collada C, Fuentes-Utrilla P, Gil L, Cervera MT (2004)
Characterization of microsatellite loci in Ulmus minor Miller and cross-amplification in U. glabra Hudson and U. laevis Pall. Molecular Ecology Notes 4: 731-732.
CrossRef | Gscholar
Ghelardini L, Santini A, Black-Samuelsson S, Myking T, Falusi M (2010)
Bud dormancy release in elm (Ulmus spp.) clones - a case study of photoperiod and temperature responses. Tree Physiology 30: 264-74.
CrossRef | Gscholar
Gil L, Fuentes-Utrilla P, Soto A, Cervera MT, Collada C (2004)
English elm (Ulmus procera) is a 2000-year-old Roman clone. Nature 431: 1053.
CrossRef | Gscholar
Guries RP, Smalley EB (2000)
Once and future elms: classical and molecular approaches to Dutch elm disease resistance. In: “The elms: breeding, conservation and disease management” (Dunn CP ed), Kluwer Academic Publishers, Boston, USA, pp. 231-248.
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.
Iglesias S (2005)
Normativa de comercialización de material forestal de reproducción [Marketing regulations for forest reproductive material]. In: “Manual para la Comercialización y Producción de Semillas y Plantas Forestales. Materiales de Base y Reproducción” (Alía A, Alba N, Agúndez D, Iglesias S eds), Organismo Autónomo Parques Nacionales, Ministerio de Medio Ambiente, Madrid, Spain, pp. 39-58. [in Spanish]
Ipinza R (1990)
Algunos aspectos relevantes sobre la taxonomía de los olmos ibéricos [Some relevant aspects of the taxonomy of Iberian elms]. In: “Los olmos y la grafiosis en España” (Gil L ed). ICONA, Madrid, pp. 69-98. [in Spanish]
Jeffers J, Richens R (1970)
Multivariate analysis of the English elm population. Silvae Genetica 19: 31-38.
Online | Gscholar
Martín JA, Solla A, Woodward S, Gil L (2005)
Fourier transform-infrared spectroscopy as a new method for evaluating host resistance in the Dutch elm disease complex. Tree Physiology 25: 1331-1338.
CrossRef | Gscholar
Martín JA, Solla A, Woodward S, Gil L (2007)
Detection of differential changes in lignin composition of elm xylem tissues inoculated with Ophiostoma novo-ulmi using Fourier transform infrared spectroscopy. Forest Pathology 37: 187-191.
CrossRef | Gscholar
Martín JA, Solla A, Coimbra MA, Gil L (2008a)
Metabolic fingerprinting allows discrimination between Ulmus pumila and U. minor and between U. minor clones of different susceptibility to Dutch elm disease. Forest Pathology 38: 244-256.
CrossRef | Gscholar
Martín JA, Solla A, Domingues MR, Coimbra MA, Gil L (2008b)
Exogenous phenol increase resistance of Ulmus minor to Dutch elm disease through formation of suberin-like compounds on xylem tissues. Environmental and Experimental Botany 64: 97-104.
CrossRef | Gscholar
Martín JA, Solla A, Esteban LG, de Palacios P, Gil L (2009)
Bordered pit and ray morphology involvement in elm resistance to Ophiostoma novo-ulmi. Canadian Journal of Forest Research 39: 420-429.
CrossRef | Gscholar
Martín JA, Solla A, Gil L, Garcia-Vallejo MC (2010a)
Phenological and histochemical changes of Ulmus minor due to root absorption of phenol: implications for resistance to DED. Environmental and Experimental Botany 69: 175-182.
CrossRef | Gscholar
Martín JA, Solla A, Witzell J, Gil L, García-Vallejo MC (2010b)
Antifungal effect and reduction of Ulmus minor symptoms to Ophiostoma novo-ulmi by carvacrol and salicylic acid. European Journal of Plant Pathology 127: 21-32.
CrossRef | Gscholar
Martín JA, Solla A, García-Vallejo MC, Gil L (2012)
Chemical changes in Ulmus minor xylem tissue after salicylic acid or carvacrol treatments are associated with enhanced resistance to Ophiostoma novo-ulmi. Phytochemistry 83: 104-109.
CrossRef | Gscholar
Martín JA, Solla A, Ruiz-Villar M, Gil L (2013)
Vessel length and conductivity of Ulmus branches: ontogenetic changes and relation to resistance to Dutch elm disease. Trees 27: 1239-1248.
CrossRef | Gscholar
Mittempergher L, Santini A (2004)
The history of elm breeding. Forest Systems 13: 161-177.
Online | Gscholar
Richens RH (1955)
Studies on Ulmus. I. The range of variation of East Anglian elms. Watsonia 3: 138-153.
Online | Gscholar
Santini A, Fagnani A, Ferrini F, Mittempergher L, Brunetti M, Crivellaro A, Macchioni N (2004)
Elm breeding for DED resistance: the Italian clones and their wood properties. Forest Systems 13: 179-184.
Online | Gscholar
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
Santini A, Pecori F, Pepori A, Brookes A (2011)
“Morfeo” elm: a new variety resistant to Dutch elm disease. Forest Pathology 42:171-176.
CrossRef | Gscholar
Smalley EB (1963)
Seasonal fluctuations in susceptibility of young elm seedlings to Dutch elm disease. Phytopathology 53: 846-853.
Smalley EB, Guries RP (2000)
Asian elms: sources of disease and insect resistance. In: “The elms: breeding, conservation and disease management” (Dunn CP ed). Kluwer Academic Publishers, Boston, USA, pp. 215-230.
Smalley EB, Lester DT (1973)
“Sapporo autumn gold” elm. Horticultural Science 8: 514-515.
Solla A, Gil L (2002)
Influence of water stress on Dutch elm disease symptoms in Ulmus minor Miller. Canadian Journal of Botany 80: 810-817.
CrossRef | Gscholar
Solla A, Gil L (2003)
Evaluating Verticillium dahliae for biological control of Ophiostoma novo-ulmi in Ulmus minor. Plant Pathology 52: 579-585.
CrossRef | Gscholar
Solla A, Burón M, Iglesias S, Gil L (2000)
Spanish program for the conservation and breeding of elms against DED. In: “The Elms: Breeding, Conservation and Disease Management” (Dunn CP ed), Kluwer Academic Publishers, Boston, pp. 295-303.
Solla A, Bohnens J, Collin E, Diamandis S, Franke A, Gil L, Burón M, Santini A, Mittempergher L, Pinon J, van den Broeck A (2005a)
Screening European elms for resistance to Ophiostoma novo-ulmi. Forest Science 51: 134-141.
Solla A, Martín 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 166:1025-1034.
CrossRef | Gscholar
Solla A, Martín JA, Ouellette G, Gil L (2005c)
Influence of plant age on symptom development in Ulmus minor following inoculation by Ophiostoma novo-ulmi. Plant Disease 89:1035-1040.
CrossRef | Gscholar
Solla A, López-Almansa JC, Martín JA, Gil L (2014)
Genetic variation and heritability estimates of Ulmus minor and U. pumila hybrids for budburst, growth and tolerance to Ophiostoma novo-ulmi. iForest [submitted].
Sutherland ML, Pearson S, Brasier CM (1997)
The influence of temperature and light on defoliation levels of elm by Dutch elm disease. Phytopathology 87: 576 -581.
CrossRef | Gscholar
Tchernoff V (1965)
Methods for screening and for the rapid selection of elms for resistance to Dutch elm disease. Acta Botanica Neerlandica 14: 409-452.
CrossRef | Gscholar
Townsend AM (2000)
USDA genetic research on elms. In: “The Elms: Breeding, Conservation and Disease Management” (Dunn CP ed). Kluwer Academic Publishers, Boston, USA, pp. 271-278.
Venturas M, López R, Martín JA, Gascó A, Gil L (2014)
Heritability of Ulmus minor resistance to Dutch elm disease and its relationship to vessel size, but not to xylem vulnerability to drought. Plant Pathology 63 (3): 500-509.
CrossRef | Gscholar
Vivas M, Martín JA, Gil L, Solla A (2012)
Evaluating methyl jasmonate for induction of resistance to Fusarium oxysporum, F. circinatum and Ophiostoma novo-ulmi. Forest Systems 21: 289-299.
CrossRef | Gscholar
Webber JF (2000)
Insect vector behavior and the evolution of Dutch elm disease. In: “The Elms: Breeding, Conservation and Disease Management” (Dunn CP ed). Kluwer Academic Publishers, Boston, MS, USA, pp. 47-60.
Weising K, Gardner RC (1999)
A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42: 9-19.
CrossRef | Gscholar
Whiteley RE, Black-Samuelsson S, Clapham D (2003)
Development of microsatellite markers for the European white elm (Ulmus laevis Pall.) and cross-species amplification within the genus Ulmus. Molecular Ecology Notes 3: 598-600.
CrossRef | Gscholar
Zalapa JE, Brunet J, Guries RP (2008)
Isolation and characterization of microsatellite markers for red elm (Ulmus rubra Muhl.) and cross-species amplification with Siberian elm (Ulmus pumila L.). Molecular Ecology Resources 8: 109-112.
CrossRef | Gscholar

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