Ceratocystis platani
(canker stain of plane)

Pictures

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Identity

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Preferred Scientific Name

• Ceratocystis platani (J.M. Walter) Engelbr. & T.C. Harr. 2005

Preferred Common Name

• canker stain of plane

Other Scientific Names

• Ceratocystis fimbriata f. platani C. May & J.G. Palmer 1959
• Endoconidiophora fimbriata f. platani J.M. Walter

International Common Names

• English: blue stain canker; canker stain; canker stain: plane; canker: sycamore; coloured canker
• Spanish: pudricion negra de la batata
• French: chancre coloré; chancre colore du platane; tache chancreuse

Local Common Names

• Italy: cancro colorato

EPPO code

• CERAFP (Ceratocystis fimbriata f. sp. platani)

Summary of Invasiveness

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C. platani is an aggressive fungal pathogen that attacks plane trees (Platanus spp.) by entering through wounds and causing canker stain disease and tree death. It is thought to be native to south-eastern USA and has spread throughout urban P. acerifolia populations planted in the large cities of the East coast. It seems likely that it was introduced to Europe in wood packing materials during World War II and, although spread was initially slow, it has accelerated recently in southern France and was reported for the first time in Greece in 2003. The disease threatens natural and planted populations of economically, ecologically and aesthetically important plane trees.

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Ascomycota
•             Subphylum: Pezizomycotina
•                 Class: Sordariomycetes
•                     Subclass: Hypocreomycetidae
•                         Order: Microascales
•                             Family: Ceratocystidaceae
•                                 Genus: Ceratocystis
•                                     Species: Ceratocystis platani

Notes on Taxonomy and Nomenclature

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The sexual stage of Ceratocystis is a perithecioid ascoma with a long neck and evanescent asci. Elliott (1923, 1925) transferred Ceratocystis fimbriata to Ceratostomella. It was then transferred to Ophiostoma by Melin and Nannfeldt (1934) and to Endoconidiophora by Davidson (1935). The name Ceratocystis was revised by Bakshi (1950) and Hunt (1956) who considered Endoconidiophora and Ophiostoma synonyms and excluded the genus Ceratostomella because asci were persistent in all species.

Ceratocystis was linked to the anamorphic state Chalara on the basis of phialidic conidiogenesis in the anamorph (Von Arx, 1974; De Hoog and Scheffer, 1984; Nag Raj and Kendrick, 1992).

Ceratocystis fimbriata was originally described from sweet potato but has been used to encompass a large, diverse complex of species that attack a range of plants. Canker stain of plane had been included in C. fimbriata as C. fimbriata f. platani (May and Palmer, 1959) until phylogenetic studies by Engelbrecht and Harrington (2005) raised it to species level as C. platani.

Description

Top of page In culture (PDA, 25°C) the mycelium, at first hyaline, becomes brownish-green and gives off a pronounced banana odour. Growth is rapid (around 0.5 cm in 24 h). After 1-2 days, numerous hyaline, truncated, cylindrical endoconidia with a smooth surface (5-40 x 3-6 µm) are formed on conidiophores (60-90 µm long) and are produced in a daily cycle. More rarely, doliform or barrel-shaped endoconidia (7-12 x 6-9 µm), light brown with truncated but lightly rounded tips, are produced in a short chain. After 5-7 days, the fungus produces numerous thick-walled, globose or ovoid and dark olive-brown chlamydospores (11-19 x 9-15 µm) isolated or in short chains (2-5 spores). The cylindrical endoconidia and chlamydospores are particularly numerous on pruning cuts made in infected organs, producing an ash-coloured, powdery layer. Chlamydospores form in abundance inside the xylem vessels and can remain viable for a number of years. These spores take on a survival function (Bolay and Mauri, 1988; Clérivet and El Modafar, 1994; Panconesi, 1999; Clérivet et al., 2003).

The sexual stage can be observed in 12-20-day-old cultures. It is characterized by dark-brown ascoma (perithecia), which are superficial or partly immersed in the culture medium, more or less subglobose (120-330 µm diam), adorned with hyphal filaments and with a long neck (400-1000 µm long), dark and wide at the base, lighter and narrower at the tip. The neck is a cluster of hyphae formed in a more or less parallel arrangement. The tip of the neck is adorned with erect hyaline hyphae (48-102 µm long) among which is the ostiole from which the ascospores are expelled at maturity. The asci form and disintegrate very early. Ascospores (3.5-8 x 2.5-6 µm) are typically hat-shaped in form, lack a germ pore and are coated in the mass with a continuous gelatinous sheath. The ascospores are contained in a yellowish-white, water-repellent, mucilaginous matrix, which emerges from the body of the ascoma through the neck and is deposited among the ostiolary hyphae. The ascoma form abundantly on pruning cuts on infected organs or on infected wood that is stacked, more rarely in infected wood and sometimes in the central medulla of young infected trees (D'Ambra et al., 1977; Panconesi, 1999).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

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Canker stain is probably indigenous to the forests of North America (Panconesi, 1999). The first confirmed report of canker stain was in 1935 on Platanus orientalis in Delaware County, Pennsylvania, USA, by Crandal (1935) and Jackson and Sleeth (1935). The disease began to spread only when the pathogen was introduced into an urban, stressed environment on a susceptible species such as Platanus acerifolia. From 1920 to 1940, the disease spread to the larger cities of the East Coast of the USA causing very serious losses to urban plantings of P. acerifolia.

During the Second World War, wood from infected trees was used to package materials for the war and this is probably how the pathogen was introduced to the European continent (Panconesi, 1972; Cristinzio et al., 1973). The first centres of infection were the major port cities: Naples, Livorno, Syracuse (Italy), Marseille (France) and Barcelona (Spain). By 2001, 25,000 trees had been killed by the disease in the south of France, but its spread started to accelerate with 200 trees killed in the region of Lyon since 1992 (Vigouroux, 2001). Italy and France are currently the most affected European countries. In the south of France, the fungus spread from Provence northwards along the Rhône valley (cities of Avignon and Lyon) (Vigouroux, 1992). More recently, EPPO reports (EPPO, 2009) the following dates when departments became infected: Rhône (1992), Ain (1994), Savioie (2005), Loire (2005) and Isère (2008) and describes the situation in France as: Present, scattered outbreaks (Languedoc-Roussillon, Midi-Pyrénées, Provence-Alpes-Côte d’Azur, Rhône-Alpes), under official control.

In Switzerland, C. platani mainly occurs in Ticino but has also been detected in Geneva canton. In 2007, new outbreaks were reported near Ceresio and Malcantone (Ticino; EPPO, 2009).

C. platani was first found in Greece in 2003 on Platanus orientalis in natural stands in the Peloponnese and had spread in both planted and native Platanus spp. by 2005 (EPPO, 2009). Genetic studies indicate that the pathogen was introduced from another European country rather than from its native North America (Ocasio-Morales et al., 2007).

Risk of Introduction

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C. platani is an EPPO A2 quarantine organism (OEPP/EPPO, 1986). The localization of the fungus is well known but the spread of the disease from infected areas of a country to unaffected neighbouring, temperate areas is a serious threat. Indeed, considering the widespread occurrence of plane trees in southern mediterranean countries, and the sensitivity of Platanus acerifolia to the fungus, the phytosanitary risk is constantly present. The risk of introducing the fungus to unaffected countries by trade in unknown infected plants or Platanus wood used in carpentry is high. The recent introduction of the pathogen to Greece is thought to have been via another European country (Ocasio-Morales et al., 2007). 

Habitat List

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Category	Sub-Category	Habitat	Presence	Status
Terrestrial

Hosts/Species Affected

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The main hosts of C. platani are Platanus acerifolia, P. occidentalis and P. orientalis, either isolated trees or groups of trees growing in cities, in the countryside and along roadsides.

Growth Stages

Top of page Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

Top of page Panconesi (1981, 1999) provides a good description of the symptoms of canker stain. When infection is localized on a primary branch or on the trunk of a young plant, the most obvious symptom is a sunken, necrotic, spindle-shaped area, with the main axis lying lengthways. It is often possible to identify the wound from which the infective process was initiated at the centre of this area. In adult trees, a single branch with sparse, chlorotic foliage, and sudden withering of part of the foliage is usually seen first. Wilting occurs most often in the spring/summer period. The leaves are at first yellow, then dry out, but do not fall immediately. They are easily distinguishable from nearby healthy leaves. At times, some branches do not bud, or developing buds wither and die suddenly (Panconesi, 1981). The tree or the branch itself shows extensive lesions and numerous rounded bark swellings, which subsequently crack lengthways. The margins show no wound callus formation, and often extend in bluish-black veins, touched with orange. This type of extension is often most marked at the upper edge. If a lesion girdles the trunk or a main branch, the bark of the distal portions becomes a conspicuous reddish-brown. The cortical layer gradually becomes necrotic and turns a clear hazel-brown or wine-red colour until it dries up and cracks, leaving fairly regularly-shaped, rectangular plaques that eventually separate from the dark, sooty-coloured wood underneath (Panconesi, 1999).

Cross-sections of affected branches show bluish-black, then brown, spindle-shaped patches, extending radially, more or less side by side. Spreading lesions affect the phloem, cambium and extensive areas of the sapwood (Vigouroux, 1979; Panconesi, 1981). The killing of cambial tissue causes dark, lenticular spots on the face of the bark, which are often detectable at a considerable distance from the infection site. These spots are very important in diagnosing canker stain infection even when the tree has been invisibly infected through the roots (Panconesi, 1981).

A single infection site can attain a length of 2-2.5 m in a year. Canker can kill a tree of 30-40 cm diameter in 2-3 years and a large, vigorous tree in 4-7 years (Ferrari and Pichenot, 1974; Panconesi, 1981).

List of Symptoms/Signs

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Biology and Ecology

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Genetics

The genetic variability of C. platani was studied in Italian populations using RAPD and minisatellite markers and compared with a number of C. fimbriata isolates from various hosts growing in different parts of the world. A high level of homogeneity was revealed in the Italian population, whereas a certain variability was recognized in isolates from others hosts. The Italian population appears to be clonal, with the same genotype occurring throughout the country (Santini and Capretti, 1998, 2000).

Physiology and Phenology

C. platani can survive for several years in vitro (at -17°C) and in soil and dead trees. The fungus can survive for 7-15 days on the surface of a wound and 30 months in decaying parts of plane trees (Grosclaude et al., 1990, 1995). Survival of the pathogen is facilitated by the production of numerous chlamydospores.

Reproductive Biology

It is extremely difficult to observe reproductive structures in infected trees; however, it is easy to obtain them on the surface of bark pieces or on wounds taken from the edge of a canker and incubated at around 25°C. The conidia germinate when they come into contact with a plant wound and the resulting mycelium colonizes the exposed tissues; reproductive structures develop at the same time. The asexual form appears first (within 2-3 days). It consists of two endoconidial stages characterized by endoconidiophore hyphae, which produce cylindrical hyaline conidia and barrel-shaped sub-hyaline conidia. After 6-8 days the fungus produces numerous thick-walled, olive-brown conidia (chlamydospores). Dark perithecia (sexual stage) containing asci and ascospores are produced after 10-20 days. Sometimes asexual and sexual reproductive structures are produced inside vessels or wounds and in the medulla (Clérivet and El Modafar, 1994; Clérivet et al., 2003).

Isolates of C. platani can be either homothallic or heterothallic (Webster and Butler, 1967) and several different strains exist. An Italian study showed that the self-fertile strain is the most common. It has two endoconidial forms, chamydospores and perithecia. The self-sterile protoperithecial strain is also frequent and possesses the same asexual forms and primordia of immature, more or less well-developed perithecia called protoperithecia. Other strains have been identified, both in nature and in culture (sectorial mutation). The most common strains are: self-sterile, with only the three asexual forms; perithecium sterile, with the three asexual forms plus a perithecium which, though morphologically normal, is sterile because it lacks ascospores; and the protoperithecium self-fertile strain, which possesses the three asexual forms plus a fertile perithecium. The self-sterile strain can be induced to produce perithecia by hybridization with cylindrical conidia from the self-fertile strain (Panconesi, 1999).

Environmental Requirements

The optimum temperature for the growth and development of C. platani is 25°C; the fungus does not grow below 10°C or above 45°C. A high level of hygrometric pressure is also necessary for growth and development. The most favourable period for fungus development is May to September. A wound in the bark or wood of the roots, trunk or branches is necessary for fungal penetration. The urban environment (pollution, water deprivation, wounds, etc.) increases the sensitivity of plane trees to attack.

Means of Movement and Dispersal

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The pathogen is spread by entering wounds on the tree or through root anastomoses between neighbouring trees. The reproductive organs of the pathogen can be spread by rain, hail, wind, etc. and by animals (man, insects, small rodents, birds, etc.); conidia are also borne along in water currents (Panconesi, 1999, 2003). Corythuca ciliata ('tiger of plane tree') is frequently found on the leaves of plane trees and could be a potential vector of fungal spores, but there are no reports of its role as a vector.

The agent mainly responsible for the spread of the disease is man, because the pathogen may be spread during pruning operations if tools that have been used on a diseased tree are then used on a healthy one. Spores of the fungus can remain viable for about a month on pruning equipment (Crone, 1962). Ornamental practices and urban roadworks are also involved in dispersal as is boat travel along rivers and canals during which roots and trunks get damaged. Roots may be wounded by rodents when plane trees are grown along riversides, and roots and trunks can be wounded by terracing machinery, which may also carry infested soil (Panconesi, 1999).

Considerable amounts of infected sawdust may be produced during sanitary operations such as the treatment or removal of diseased trees. The fungus can survive for a long time in this sawdust. This type of infected material may also be transported by tools, agricultural machinery, man and watercourses and can contaminate healthy areas (Vigouroux, 1987).

The most likely means of international spread is by trade in unknown infected plants.

Plant Trade

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Wood Packaging

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Impact Summary

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Economic Impact

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The economic impact of canker stain disease relates to the use of plane trees as ornamental and shade trees. The felling of diseased mature trees in urban areas and along waterways and replacement with disease resistant trees or alternative species is costly to municipal governments. At Forte dei Marmi, one of the oldest infection centres in Italy, 90% of all plane trees died of the disease in the twenty-year period from 1972-1991 (Panconesi et al., 2003). The felling of thousands of diseased trees along the Canal du Midi in France has been reported in the news (Hadden and Hugh-Jones, 2011).

It is feared that removal of mature trees could negatively affect tourism to some of the affected areas. 

Environmental Impact

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The danger of this disease is its ability to disperse and the speed with which it kills trees (Panconesi, 1981). Canker stain appears to have lost importance in the eastern USA but has emerged recently in several locations in the natural Platanus occidentalis forests of Arkansas, USA (Panconesi et al., 2003).

In Italy and especially in the south-east of France the disease has caused serious losses to urban trees and the spread of the disease out of the cities is a danger to plane tree survival. In 1986, there was a first report of C. platani invading a natural forst of P. orientalis in Sicily (Panconesi et al., 2003) and, since its first detection in Greece in 2003, it is having a dramatic impact on natural populations of P. orientalis in the southwest (Ocasio-Morales et al., 2007).

Social Impact

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Plane trees have been planted in many European cities including Paris, London and Berlin to provide shade and aesthetic value, particularly along canals and rivers. Diseased trees present a health and safety risk and must be removed. The Canal du Midi running from Toulouse to the Mediterranean coast in France is a UNESCO World Heritage Site (http://whc.unesco.org) which is noted for its aesthetic architectural and landscape design and attracts large numbers of tourists. Thousands of diseased mature plane trees along its length are expected to need felling over the next few years.

Risk and Impact Factors

Top of page Invasiveness

• Proved invasive outside its native range
• Has high reproductive potential
• Has propagules that can remain viable for more than one year

Impact outcomes

• Ecosystem change/ habitat alteration
• Host damage
• Negatively impacts forestry
• Negatively impacts tourism
• Threat to/ loss of native species
• Transportation disruption

Impact mechanisms

• Pathogenic

Likelihood of entry/control

• Highly likely to be transported internationally accidentally
• Difficult/costly to control

Diagnosis

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The fungus can easily be isolated within 2 days from pieces of wood removed from cankers and plated on malt agar or PDA at 25°C. It can also be detected from soil and sawdust samples under the same culture conditions.

The original technique used to trap the fungus, described by Grosclaude et al. (1988), is more complex but provides good results. Healthy branches of Platanus acerifolia are stripped of their bark and pieces of the wood are placed in contact with the collected sample (wood, soil, sawdust, etc.) in a jar full of aerated water; wood blackening within a few days at room temperature is a positive result.

An ELISA test was perfected by Diop-Bruckler (1991). A diagnostic protocol has been published by EPPO (EPPO, 2003). Pillotti et al. (2012) developed a sensitive and effective Real-Time PCR method based on a Taqman probe for the diagnosis of C. platani on members of the genus Platanus.

Detection and Inspection

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The ability to inspect a tree to detect an attack by C. platani is dependent on the size of the tree and the accessibility of the roots. Attention must be paid to chlorotic foliage and sudden widespread withering of the foliage as these are usually the first symptoms of canker stain disease. Attack by C. platani must be considered a high possibility if all other symptoms (described under Symptoms) are present.

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Cultural Control and Sanitary Measures

As the disease is mainly spread by human activity, clean propagation and production methods can limit its dispersal (Smith, 1985). Planting material should be obtained from regions where the disease does not occur and plants should be grown in a place found to be free from the fungus during the last growing season (OEPP/EPPO, 1990). All pruning tools should be disinfected with alcohol before any pruning operations, even in uninfested regions. In infested regions, disinfection should be repeated between each tree.

In principle, all terracing machinery used in the vicinity of infested trees should be treated by water-jet and sprayed with 8-hydroxyquinoline sulfate, benomyl or sodium hypochlorite solution before moving to another site. When infected trees are felled, all debris and sawdust should be sprayed abundantly with fungicides before sweeping up and disposal. All wood should be burned (Vigouroux, 1979; Blankart and Vigouroux, 1982; Panconesi, 1999).

The wood used in industry for the manufacture of woodchip board should be treated by high temperatures (90-100°C) during the manufacturing process to kill the fungus (Panconesi, 1999).

Chemical Control

Chemical substances do not provide very satisfactory preventive or curative control of the disease. External treatments with substances that are effective against the fungus are not efficient on a diseased tree because the fungus grows in the conducting vessels of the wood. The injection of fungicide under pressure into the vascular system temporarily halts the infective process but the pathogen is not eliminated (Panconesi, 1999).

Biological Control

No biological control methods exist against C. platani. Several experiments with Bacillus subtilis or Trichoderma harzianum, a fungus known to have a strong antagonistic activity against the closely related C. fimbriata in vitro, failed to give the desired results (Turchetti and Panconesi, 1982; Mutto Accordi, 1989).

The necrotrophic action of some fungi against C. fimbriata is known but there are no reports of the use of these mycoparasites to control C. fimbriata (Panconesi, 1999).

Host-Plant Resistance

Host-plant resistance is unknown in the species Platanus acerifolia. However, a natural source of resistance was highlighted in the American species Platanus occidentalis in the south-eastern USA (FI McCracken, US Department of Agriculture, Southern Hardwoods Laboratory, Stoneville, Mississippi, USA, unpublished data). Unfortunately this source cannot be directly exploited in Europe as the species is not acclimatized to the region. A genetic improvement programme (Vigouroux, 1992; Clérivet et al., 2003) aimed at restoring the original hybrid (Platanus acerifolia) using Platanus orientalis and the resistant clones selectively obtained by McCracken as parents, yielded some clones with a good level of resistance against the fungus (Vigouroux and Olivier, 2001, 2004). However, the durability of resistance is not yet clearly established under the natural conditions of plane tree development.

References

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