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«Luisa Ghelardini Faculty of Natural Resources and Agricultural Sciences Department of Plant Biology and Forest Genetics Uppsala Doctoral thesis ...»

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Bud Burst Phenology, Dormancy

Release and Susceptibility to Dutch

Elm Disease in Elms (Ulmus spp.)

Luisa Ghelardini

Faculty of Natural Resources and Agricultural Sciences

Department of Plant Biology and Forest Genetics

Uppsala

Doctoral thesis

Swedish University of Agricultural Sciences

Uppsala 2007

Acta Universitatis Agriculturae Sueciae

2007: 134

Cover illustration courtesy of Ignazio Graziosi. Twig of a natural hybrid between

Ulmus minor Mill. and Ulmus pumila L.

ISSN 1652-6880 ISBN 978-91-85913-33-6 © 2007 Luisa Ghelardini, Uppsala Tryck: SLU Service/Repro, Uppsala 2007 Abstract Ghelardini, L. 2007. Bud Burst Phenology, Dormancy Release and Susceptibility to Dutch Elm Disease in Elms (Ulmus spp.). Doctor's dissertation.

ISSN 1652-6880, ISBN 978-91-85913-33-6 European elms (Ulmus glabra, U. laevis and U. minor) have been damaged and are still threatened by an alien hypervirulent pathogen, Ophiostoma ulmi s.l., the agent of Dutch elm disease (DED). Therefore, several ex situ clone collections were established throughout Europe for breeding and conservation purposes. This thesis was carried out within the RESGEN CT96-78 project, which launched the EU-coordinated evaluation of these collections. The aim of this thesis was to analyse the variation in bud burst date and to acquire basic knowledge on the environmental control of this adaptive trait with regard to DED susceptibility.

Bud burst date variation observed among collections and years in European elms was explained by a phenological model based on an inverse exponential relationship between thermal time and chilling to bud burst. According to the fitted curves, European elms have low dormancy and short chilling requirement for dormancy release.

Bud burst date in U. minor was directly related to latitude and elevation. The order of bud burst was stable among years. The observed geographic trends were largely determined by difference in chilling requirement for dormancy release which increased with latitude and elevation.

The effects of photoperiod and temperature on dormancy release in clones of European and Asian species were studied in partially controlled conditions in Italy. Dormancy was generally low and short in all clones. There was no evidence that photoperiod influenced dormancy release in these elms.

Susceptibility to DED was assessed in the Italian clone collection. Susceptibility varied greatly among taxonomic groups and within the most represented species, U. minor. In this species, DED susceptibility was directly correlated with geographic origin and date of bud burst, southern and early flushing clones showing the least symptoms. The results suggest that earliness of bud burst represents a mechanism of disease avoidance owing to an asynchrony between the susceptible period in the host and the time of natural infection by Scolytus insects, the main vectors of DED.

Key words: chilling, disease avoidance, Ophiostoma ulmi, photoperiod, rest, thermal time, Ulmus glabra, Ulmus laevis, Ulmus minor Author's address: Luisa Ghelardini, Istituto per la Protezione delle Piante – Consiglio Nazionale delle Ricerche C.N.R., Via Madonna del Piano 10, 50019 Sesto fiorentino (FI), Italy. Current address: Department of Plant Biology and Forest Genetics, SLU, Box 7080, SE-750 07 Uppsala, Sweden. E-mail: Luisa.Ghelardini@vbsg.slu.se Riassunto Ghelardini, L. 2007. Bud Burst Phenology, Dormancy Release and Susceptibility to Dutch Elm Disease in Elms (Ulmus spp.). Tesi di Dottorato.

ISSN 1652-6880, ISBN 978-91-85913-33-6 Gli olmi europei (Ulmus glabra, U. laevis and U. minor) sono stati severamente danneggiati e sono tuttora minacciati dal fungo Ophiostoma ulmi s.l., agente della grafiosi, una malattia letale dell'olmo. Varie collezioni di cloni ex situ sono state pertanto costituite in Europa per la selezione e la conservazione del germoplasma. Questa tesi è stata svolta nell’ambito del progetto RESGEN CT96-78, che ha avviato lo studio coordinato di queste collezioni a livello europeo. Scopo della tesi è stato quello di analizzare la variazione nella data di germogliamento e di acquisire conoscenze di base sul controllo ambientale del germogliamento in relazione alla suscettibilità alla grafiosi.

La variazione nella data di germogliamento degli olmi europei osservata tra le collezioni nei diversi anni è stata spiegata con un modello fenologico basato su una relazione esponenziale inversa tra il thermal time e il chilling necessari per il germogliamento. Sulla base delle regressioni cosí ottenute, si è dimostrato che gli olmi europei sono caratterizzati bassa dormienza e basse richieste di chilling.

La data di germogliamento in U. minor si è rivelata direttamente correlata a latitudine e altitudine di origine delle piante. L’ordine di germogliamento si è dimostrato stabile negli anni. I trend geografici osservati sono largamente determinati da differenze nelle esigenze di chilling per l’uscita dalla dormienza, direttamente proporzionali a latitudine e quota.

Inoltre sono stati studiati gli effetti del fotoperiodo e della temperatura sull’uscita dalla dormienza in cloni di olmi europei ed asiatici in condizioni parzialmente controllate in Italia. La dormienza era complessivamente bassa e il fotoperiodo non aveva alcuna influenza sull’uscita della dormienza nei cloni studiati.





La suscettibilità alla grafiosi nella collezione clonale saggiata variava largamente tra gruppi tassonomici e all’interno della specie più rappresentata, U. minor. In questa specie la

suscettibilità era direttamente correlata all’origine geografica e alla data di germogliamento:

i cloni meridionali, più precoci, mostravano una sintomatologia attenuata. Questi risultati suggeriscono che i cloni a germogliamento più precoce possano sfuggire alla malattia grazie all’asincronia che si instaura tra il periodo di suscettibilità dell’ospite e quello del volo degli insetti del gen. Scolytus, principali vettori della grafiosi.

Parole chiave: chilling, disease avoidance, Ophiostoma ulmi, photoperiod, rest, thermal time, Ulmus glabra, Ulmus laevis, Ulmus minor Indirizzo dell’autore: Luisa Ghelardini, Istituto per la Protezione delle Piante – Consiglio Nazionale delle Ricerche C.N.R., Via Madonna del Piano 10, 50019 Sesto fiorentino (FI), Italy. Recapito attuale: Department of Plant Biology and Forest Genetics, SLU, Box 7080, SE-750 07 Uppsala, Svezia. E-mail: Luisa.Ghelardini@vbsg.slu.se A Francesco (dopo la pioggia il sole) Quando, circondata dal suo intimo diurno buio, la neve crocchia, costipata resiste e ti parla attraverso le tue scarpe pesanti, stride, asciutta e dura, rimastica e inghiotte il freddo, non penseresti mai che se ne possa andare o qualcos’altro cambiare.

Contents Introduction, 11 Background, 11 The study genus – Ulmus, 12 The study species, 13 The European elms, 13 The Asian elms, 14 Dutch elm disease (DED), 15 The causal fungus, 15 Disease symptoms and cycle, 15 Host resistance, 16 Seasonal variation in host resistance and relation with growth rhythm, 18 Genetic improvement programs for DED resistance, 19 Dormancy in vegetative tree buds, 20 Dormancy phases, 20 Environmental signals involved in dormancy induction, 22 Temperature and light control of dormancy release, 23 Timing of bud burst, 25 Modelling bud burst, 26

Aims of this study, 28

Materials and Methods, 29 Plant material, 29 A temperature model for bud burst date in European elms – Paper I, 29 Susceptibility to DED and relation to spring phenology – Paper II, 30 Geographic variation in bud burst date in U. minor – Paper III, 31 Photoperiod and temperature effects on bud dormancy release in Ulmus spp. clones – Paper IV, 31 Main Results and Discussion, 32 A temperature model for bud burst date in European elms – Paper I, 32 Susceptibility to DED and relation to spring phenology – Paper II, 34 Geographic variation in bud burst date in U. minor – Paper III, 36 Photoperiod and temperature effects on bud dormancy release in Ulmus spp. clones – Paper IV, 37 Conclusions and future perspectives, 39 References, 41 Acknowledgements, 51 Appendix This thesis is based on the following papers, which will be referred to by their

Roman numerals:

I. 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 2nd International Elm Conference, 20-23 May 2003, Valsaìn, Spain.

Investigatión Agraria: Sistemas y Recursos Forestales 13 (1): 37-45.

II. 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.

III. 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.

IV. Ghelardini, L., Santini, A., Black-Samuelsson, S., Myking, T. & Falusi, M.

Bud dormancy release in elm (Ulmus spp.) clones – photoperiod and temperature effects. (Manuscript) Paper I, II and III are reprinted by kind permission of the publishers Additional publications Santini, A., La Porta, N., Ghelardini, L. & Mittempergher, L. 2007. Breeding against Dutch elm disease adapted to the Mediterranean climate. Euphytica DOI 10.1007/s10681-007-9573-5

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Background Many tree species native to the temperate mixed broadleaved forests in Europe are currently endangered because of various human induced threats. Human activities reduce natural habitats and introduce alien organisms, such as pathogens, pests or competitors, potentially dangerous for native species. European elms are an excellent example of this as they suffer from both of these threats. The habitat of Ulmus laevis Pall., which typically grows in the riverain deciduous forests of Central and Eastern Europe, has been largely reduced as a consequence of human activities. All three European elm species (U. laevis, Ulmus minor Mill. and Ulmus glabra Huds.) have been severely damaged during the last century and are still threatened by an alien hypervirulent pathogen, Ophiostoma novo ulmi, the agent of Dutch elm disease (DED).

As a consequence, European elms are undergoing extraordinary ex situ conservation measures (Eriksson 2001; Collin et al. 2004). Several national initiatives for collecting germplasm have been undertaken in Europe and different ex situ clone collections of European elms have been established. In order to provide these diverse initiatives a unitary design and concept within a European scope, a common conservation strategy was defined for the European elm species within the European Forest Genetic Resources (EUFORGEN) cooperative program (Collin et al. 2002) and the “Conservation of Elm Genetic Resources” EU project (RESGEN CT96-78) was set up in the late 1990s.

Ex situ collections are effective for dynamic conservation as far as they contain high genetic variability in adaptive traits, which is the indispensable requisite for adaptation and evolution as well as for genetic improvement by breeding. Genetic variability within the established ex situ collections of European elms has been investigated within the RESGEN project with DNA markers and in quantitative traits with adaptive value, i.e. resistance to DED and phenology. Special attention was given to the timing of bud burst which, apart from its general ecological importance, potentially affects DED susceptibility (reviewed in Paper II).

In the work presented here, we analysed the variability in susceptibility to DED within the Italian elm collection in relation to the timing of bud burst under field conditions (paper II). We also studied the variability in timing of budburst of the European elm species across collections and years as a function of environmental factors and geographic origin (paper I and III). Under controlled conditions we studied photoperiod and temperature effects during dormancy release in clones of four Asian and two European elm species (paper IV).

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Figure 1. Natural distribution range of the genus Ulmus Mirb.

From Stipes & Campana (1981). Redrawn by Ignazio Graziosi.

The taxonomy of Ulmus is controversial owing to high morphological variability, ease of hybridisation, which produces a large variety of fertile intermediate forms of difficult attribution, and long history of utilization by humans. Elms have since ancient times been cultivated and introduced outside their natural range, allowing hybridisation between taxa otherwise naturally separated (Richens 1983). On the basis of morphological characters, mainly of leaves and fruits, and more recently on the basis of molecular markers, 30 to 45 species of Ulmus have been classified and placed in five to nine taxonomic sections (Richens 1983; Wiegrefe et al. 1994; Buchel 2000).

Elms are allogamous and hermaphroditic, having small perfect flowers which, being wind-pollinated, are apetalous. Flowers generally appear in late winter or early spring before foliation but a small number of species flower in late summer or fall. The fruit is a roundish wind-dispersed samara containing one non dormant seed which is able to germinate soon after dissemination (Cronquist 1981; Richens 1983). Elms have ring-porous wood, with 1 to 3 rows of earlywood vessels.

Vessels in latewood are grouped in tangential to oblique bands together with vascular tracheids and parenchyma. Conduction is restricted to the outermost growth layers (Greenidge 1955; Ellmore & Ewers 1985). The ground-tissue is thick-walled. Paratracheal parenchyma is abundant in earlywood and among vessel groups in latewood (IAWA Committee 1989).



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