어사시(御史詩)
金樽美酒千人血 금준미주천인혈
玉盤佳肴萬姓膏 옥반가효만성고
燭淚落時民淚落 촉루락시민루락
歌聲高處怨聲高 가성고처원성고
금술통의 맛좋은 술은 천백성의 피요. 옥쟁반의 좋은 안주 만백성의 기름이로다. 촛불이 눈물 흘릴 때 백성의 눈물 떨어지고, 노랫소리 높은 곳 백성의 원성또한 높구나. - 이도령이 전라도 암행어사로 남원에 당도하여 신임 남원부사 변사또의 무모한 학정을 고발하는 詩 -옥중시(獄中詩) 去歲何時君別妾 거세하시군별첩 昨已冬節又動秋 작이동절우동추 狂風半夜雨如雪 광풍반야우여설 何爲南原獄中囚 하위남원옥중수지난 해 언제쯤 님과 이별하였나요. 엊그제 겨울이더니 벌써 또 가을이군요. 거친 바람, 깊은 밤에 찬 비 내리는데 어이하여 이몸이 옥중 죄수가 되었나요. - 춘향이 신임 남원부사 변사또의 술시중을 거부하다 투옥되어 남원옥중에서 지은 詩 -
田家 전가 농가
朴趾源 박지원 1737~1805
翁老守雀坐南陂 옹노수작좌남피 참새 쫓는 노인네 밭둑에 앉아 있건만
粟拖拘尾黃雀垂 속타구미황작수 개꼬리 조 이삭에 노란 참새 매달렸네
長男中男皆出田 장남중남개출전 맏아들 둘째 아들 일하러 들로 나가고
田家盡日晝掩扉 전가진일진엄비 시골집 사립문은 하루 내내 닫혀 있네
鳶蹴鷄兒攫不得 연축계아확부득 소리개가 병아리를 채가려다 놓쳤는지
群鷄亂啼匏花籬 군계난제포화리 박꽃 핀 울 밑에 소란스레 우는 뭇 닭
小婦戴棬疑渡溪 소부대권의도계 함지를 인 새댁은 조심조심 내 건너고
赤子黃犬相追隨 적자황견상추수 누렁이와 벌거숭이 다투어 뒤따라가네
Summary of Invasiveness
The long distance spread of fire blight is a rare event which in most cases seems to be the result of plants or plant tissues being moved across the oceans. Short distance spread is the result of the characteristics of the pathogen, especially its ability to produce an exudate (bacteria embedded in exopolysaccharides) which is easily transported by wind, rain, insects or birds. This is very efficient; once the pathogen has moved into a new territory it almost always colonizes and becomes established. This is accompanied by economic losses in regions where apple, pear or loquat are grown commercially; it might prevent the survival of local cultivars and could disrupt international trade. To date fire blight has colonized most of North America, Western Europe and most of the countries around the Mediterranean Sea as well as New Zealand. Outbreaks of fire blight are irregular and difficult to control.
Taxonomic Tree
Domain: Bacteria
Phylum: Proteobacteria
Class: Gammaproteobacteria
Order: Enterobacteriales
Family: Enterobacteriaceae
Genus: Erwinia
Species: Erwinia amylovora
Distribution
It is generally thought that fire blight originated on wild hosts (presumably Crataegus) in the north-eastern USA, where it has been described after the import and cultivation of European apple and pear varieties (van der Zwet and Keil, 1979). The first description outside the USA was in New Zealand (1919). In Europe, fire blight was first described in the UK (Kent) in 1957. From this year on, a permanent spread of the disease was assessed in Northern, Western and Central Europe. In 1998, all countries belonging to the European Union (except Portugal) had fire blight on pears, apples or ornamentals, either widespread (England, Belgium, Germany), localized (France, Switzerland) or in restricted spots, under control and local eradication (Spain, Italy, Austria). It can be said that Western Europe has been invaded by fire blight in the second half of the twentieth century. However, even today, wide areas of Europe remain free of fire blight (in Italy, Spain and the south-east of France). Fire blight invaded a large area around the Mediterranean Sea. It most probably spread from an initial outbreak detected in the Nile delta region of Egypt in 1964. The disease was later found in Greece (Crete), Israel, Turkey, Lebanon, Iran and countries of Central Europe. The introduction of E. amylovora in Egypt and England has resulted in one continuous zone infected by fire blight, which encompasses most of Western Europe and most of the Mediterranean region. Only countries in North Africa seem to be free of fire blight; although the disease has recently been described in Morocco. A number of unconfirmed reports of fire blight (China, India, Korea, Saudi Arabia, Vietnam, Colombia) may rely on misdiagnosis, or insufficient description of the causal agent (confusion of fire blight with pear-blast symptoms caused by Pseudomonas syringae pv. syringae or with other Erwinia species reported on Asian pear). It must also be remembered that E. amylovora is a quarantine organism (list A2 OEPP), the economic consequences of a declaration of the presence of fire blight in a country may have costly consequences for the international trade of this country: it cannot be ruled out that the list of actually 'infected' countries is slightly longer than the list of officially declared areas. In most cases, attempts to eradicate the pathogen in newly infected countries, only slows down the spread of the disease. Until fire blight is again detected in Australia, this country might be the only case where eradication has been successful. Fire blight-like symptoms were detected on cotoneaster in the Royal Botanic Gardens, Melbourne, Victoria, in April 1997, and diagnostic tests confirmed that the causal organism was E. amylovora (Rodoni et al., 1999). An intensive eradication programme was undertaken and national surveys conducted for 3 years following the detection of E. amylovora have confirmed the absence of the disease in all states of Australia (Rodoni et al., 2002). A record of E. amylovora in New South Wales, Australia, cited in previous editions of the Compendium, was included as a result of a database error and has now been removed. There has been no positive detection of E. amylovora in New South Wales. Large areas of the world are still free of fire blight (South America, most of Africa and Asia) in spite of the fact that susceptible cultivars of European and American origin are grown in these areas, and that potentially susceptible host plants may be common in the environment. See also CABI/EPPO (1998, No. 257).
History of Introduction and Spread
Fire blight was first noticed in Hudson valley, New York (USA) in the 1780s. Whether fire blight was native in the regions surrounding the Hudson valley, such as Quebec and Ontario, is not known. From this initial focus fire blight spread throughout North America. It was also accidentally imported into England and Egypt. From those two outbreaks it spread and became established in most of Europe and around the Mediterranean Sea. The introductions to New Zealand and Bermuda have not spread beyond these islands. E. amylovora has never been introduced intentionally; its presence is either the result of accidental introduction (England, New Zealand, Egypt and Bermuda) or due to the ability of the bacterium to spread locally relatively easily.
Hosts/Species Affected
E. amylovora is a pathogen of plants in the family Rosaceae; most of the natural hosts are in the subfamily Maloideae (formerly Pomoideae), a few belong in the subfamilies Rosoideae and Amygdaloideae (Momol and Aldwinckle, 2000). Genera in the subfamily Spiraeoideae have been reported as hosts on the basis of artificial inoculation (van der Zwet and Keil, 1979). Strains of E. amylovora isolated from one host are pathogenic on most other hosts. This was the case for strains isolated from natural infections on Prunus salicina in the USA (Mohan and Thomson, 1996) and on Prunus domestica and Rosa rugosa in southern Germany (Vanneste et al., 2002a). Rubus strains (see Taxonomy and Nomenclature) are host specific; they are pathogenic on brambles but not on apple and pear (Starr et al., 1951; Braun and Hildebrand, 2005). Also, a few Maloideae strains exhibit differential virulence on apple; for example, strain Ea273 was not pathogenic across the same range of apple cultivars and rootstocks as common strain E4001A (Norelli et al., 1984, 1986). Within each group of susceptible host plants, species or cultivars may be found with a high level of resistance; such plants may show no, or limited, symptoms under natural conditions or even following artificial inoculation (Forsline and Aldwinckle, 2002; Luby et al., 2002). Lists of resistant cultivars are published for important crops (van der Zwet and Keil, 1979; Zeller, 1989; Thomas and Jones, 1992; Berger and Zeller, 1994; van der Zwet and Bell, 1995; Bellenot-Kapusta et al., 2002). Wild Pyrus (P. amygdaliformis, P. syriaca) in southern Europe and in the Mediterranean area, Crataegus (C. oxyacantha [C. laevigata], C. monogyna) in northern and central Europe, and ornamentals (Pyracantha, Cotoneaster, Sorbus) throughout Europe are important sources of inoculum for apple and pear orchards.
Symptoms
Fire blight's basic symptom is necrosis or death of tissues. Droplets of ooze on infected tissues are also an important symptom; they are the visible indication of the presence of fire blight bacteria. Except for minor differences, the symptoms of fire blight are basically the same on all host plants. Infected blossoms initially become water-soaked and of a darker green as the bacteria invade new tissues. Within 5- 30 plus days (commonly 5-10 days), the spurs begin to collapse, turning brown to black. Initial symptoms are often coincident with the accumulation of about 57 degree days, base 12.7°C, from the infection date (Steiner, 2000). Infected shoots turn brown to black from the tip; shoots often bend near the tip to form a so-called 'shepherd-crook' shape. Shoots invaded from their base exhibit necrosis of basal leaves and the stem. Leaves and fruits may be invaded through petioles or stems or infected through wounds, resulting in discoloration followed by collapse of the leaves and fruit. During wet, humid weather, infected leaves and particularly the fruit often exude a milky, sticky liquid, or ooze containing bacteria. From infected flowers and shoots, the bacteria may invade progressively larger branches, the trunk and even the rootstock. Infected bark on branches, scaffold limbs, trunk and rootstock turns darker than normal. When the outer bark is peeled away, the inner tissues are water-soaked often with reddish streaks when first invaded; later the tissues are dark brown to black. As disease progression slows, lesions become sunken and sometimes cracked at the margins, forming a canker. Trees with rootstock blight may exhibit liquid bleeding from the crown at or just below the graft union in early summer. Water-soaked, reddish and necrotic tissues are visible when the outer bark is removed. Trees with infected rootstocks often exhibit yellow to red foliage about a month before normal autumn coloration. Rootstocks such as M.26, M.9 and relatives of M.9 often show these symptoms without evidence of infection in the trunk of the scion. Infection of M.7 and a few other rootstocks occurs following infection of suckers arising from the rootstocks; the infected suckers exhibit typical shoot blight symptoms. Many trees with rootstock blight will die in the first year after infection; the remaining rootstock-infected trees often die within 2-3 years. Any plant tissues invaded by the bacteria can show ooze production on their surface. This exudate is a specific symptom of fire blight. Depending on weather conditions and on the time of the day, ooze may or may not be produced. It is most frequently observed early in the morning when the host water potential is positive. It may appear in different ways: droplets, threads or film on the plant's surface.
Biology and Ecology
The life cycle of E. amylovora can be described as follows: 1. Infection through flowers. The entry of bacteria through natural openings in the floral cup (hypanthium) may take place after multiplication on the surface of stigmas. 2. Infection, later in the season. The entry of bacteria through small wounds produced by strong winds, hail, and insects may take place in young leaves and at the tips of growing shoots. 3. Internal invasion. Entry of E. amylovora into healthy shoots, branches and rootstocks may take place within trees by the systemic movement of bacteria from infected spurs and shoots. 4. Canker formation. The development of areas between infected and uninfected woody tissues were E. amylovora survives the dormant season. Unlike some bacterial plant pathogens, E. amylovora is not an epiphytic bacterium; it is not able to multiply on the surface of healthy plants. The only stage where the bacteria multiply on the surface of the plant is on the stigmatic surfaces in the flower (Thomson, 1986). Pollinating and other flower-visiting insects are important for spreading the bacteria from both infested and infected flowers to healthy flowers. Other insects play a role in spread by visiting droplets of ooze exuding from cankers and then visiting healthy flowers. Free-water and high humidity in concert with temperature govern the rate of bacterial multiplication in the floral cup and the incidence and severity of flower infection (Pusey, 2000). Climatic conditions during spring and summer play a key role in the occurrence and development of fire blight (Billing, 2000). The presence of bacteria on the stigmas of healthy flowers (epiphytic populations) is related to daily temperature (Thomson et al., 1982). Temperatures between 18 and 30°C with rain during bloom favour flower infection, frequent storms with wind-driven rain (with sufficiently high temperatures) during the period of growth elongation favour shoot and fruit infections and the rapid development of the disease. Bacteria can be spread by wind and wind-driven rain within and between trees as ooze, strands (polysaccharide threads which may be present on the surface of infected plant) and aerosols (McManus and Jones, 1994). Secondary blossoms (rat-tails), which may be present on some hosts in late spring and summer, are often infected because weather conditions are more likely to be favourable when they are open. Severe infections may also take place in summer on shoots, leaves, fruits, following a hailstorm or any climatic event which wounds the plant surface, and is associated with rain. Rootstock blight can develop from the internal spread of bacteria from an infected scion (Momol et al., 1998). Malling (M.) 9 and M.26 rootstocks are highly susceptible to internal invasion and rootstock blight (Momol et al., 1998; Norelli et al., 2003). Dispersal of the pathogen may occur from the shipping of infected plant material. Latent infections may be present without any visible symptoms; the disease developing when the material is planted in the field. This mode of dispersal could introduce fire blight into new regions and countries.
Prevention and Control
Legislative Control (Exclusion)
Fire blight is a quarantine disease in most countries and, therefore, shipments of plants, or parts of plants that can be host to fire blight, are under strict regulation. This regulation requires that only healthy plants produced in healthy environments are shipped. At the European level (EU), the genera relevant to quarantine regulation for fire blight are the following: Chaenomeles, Cotoneaster, Crataegus, Cydonia, Eriobotrya, Malus, Mespilus, Pyracantha, Pyrus, Sorbus (other than S. intermedia) and Stranvaesia. In countries where fire blight is not yet detected, but exposed to permanent threat by nearby foci, a network for monitoring may be preventatively organized (Mazzucchi, 1994; Santos, 1995). In the EU, a list (map) of so-called 'protected zones' in which fire blight is considered as absent is periodically published. In such protected zones, the import of host plants of fire blight from a contaminated country is forbidden (except from 'protected areas'). In non protected zones, where fire blight is likely to be endemic, specific 'protected areas' are settled (minimal surface: 50 km²) in which special surveys and official control guarantee the absence of fire blight on plants grown in nurseries. From these areas plants are allowed to be shipped (Petter and de Guenin, 1993). Heat treatment of plant propagation material has been proposed (Keck et al., 1995). In some countries the production and commercialization of the most susceptible cultivars may be banned, or discouraged, particularly for certain cultivars of Cotoneaster, Pyrus, Malus and Crataegus.
Cultural Control
As is the case with most bacterial diseases, cultural practices are very important to control fire blight. These practices will tend to reduce the frequency of infections, by decreasing the potential entry of bacteria into the plant: suppression of blossoms by severe trimming of Crataegus hedges has been recommended in the Netherlands (Meijneke, 1984b); suppression of secondary blossoms in pear orchards is a proposed control measure in France (Lecomte and Paulin, 1992). A complementary strategy for reducing the severity of infection is to follow growing practices aimed at reducing tree vigour and the duration of shoot growth (also see Chemical Control/prohexadione calcium). Restricting nitrogen and water supply to the trees is the most common advice in this respect, together with a regular pruning of the trees. Insect control is no longer believed to be a key factor in the limitation of movement of bacteria from tree to tree. Nevertheless, care should be taken with transportation of beehives to avoid movement from an infected to a healthy orchard. Similarly, overhead irrigation should be avoided in an orchard with a history of fire blight. Cultural methods include the sanitation of trees, obtained by a prompt pruning out of symptoms as soon as they are detected in an orchard or a plantation (Steiner, 2000). The disinfection of tools (pruning shears) with chlorine or alcohol is probably useful (Teviotdale et al., 1991) during the growing season but not in winter when trees are dormant (Lecomte and Paulin, 1991). The early detection of symptoms is important to the success of sanitation programmes. Surveys in orchards and nurseries are recommended in spring just before bloom (active cankers), after bloom (new flower infection), in summer after hailstorms and near the end of the period of shoot elongation (shoot infections and cankers). These surveys must be followed by the removal (cutting out) of all visible infections. In most cases, warning systems will provide an indication of the most suitable period when these surveys are useful (Billing, 2000).Risking catastrophic tree losses from rootstock blight in high-density apple orchards can be avoided only by selecting trees propagated on resistant rootstocks for new orchards. Several promising highly resistant rootstocks have been released or will soon be released from rootstock-breeding programmes (Cline et al., 2001; Norelli et al., 2003). Some of these are dwarfing rootstocks suitable for high-density orchard systems; avoiding M.9 and M.26 rootstocks in favour of resistant rootstocks is the best control for rootstock blight. Rootstock blight has not been a problem on trees propagated on Budagovsky (B.) 9 and on some Japanese rootstocks (Bessho et al., 2001; Ferree et al., 2002). Susceptible cultivars (and rootstocks) should be avoided when establishing new orchards and ornamental planting in regions with significant fire blight problems; unfortunately, this advice is seldom followed in practice. For example, many of the most commercially successful apple cultivars introduced in recent years are much more susceptible to fire blight than many older cultivars and planting of these cultivars, particularly when propagated on highly susceptible rootstocks, has resulted in devastating financial losses (due to fire blight) to individual apple growers and entire apple industries.
Chemical Control
The number of chemicals of value for fire blight control is very limited; they belong to four categories: coppercontaining compounds, antibiotics, growth regulators and elicitors. Bordeaux mixture and fixed coppers were the first compounds used for control. The number and timing of applications depend on the sensitivity of each cultivar to copper injury and the economic significance of the injury. Spring treatments at green tip may reduce the survival of E. amylovora around canker margins (Steiner, 2000); the value of such treatments needs to be established. More commonly, coppers are applied during bloom to prevent flower infection and in summer to prevent shoot infection. Antibiotics (primarily streptomycin, also oxytetracycline, oxolinic acid and gentamicin) are used to prevent flower and shoot infections; they are more effective than, and not as phytotoxic as, coppers. A standard application schedule for streptomycin is two to three sprays in bloom and one to two sprays post-bloom for five sprays per year. Streptomycin has been used in North America since the 1950s and a few other countries such as New Zealand and Israel; more restrictive governmental regulation has limited and sometimes banned its use in other countries (McManus et al., 2002). Despite the selection of streptomycinresistant strains in several countries (Jones and Schnabel, 2000; McManus et al., 2002) streptomycin use continues because alternative methods are less effective. In Israel, oxolinic acid, a synthetic quinolone antibiotic, has been used as an alternative to streptomycin (Shtienberg et al., 2001). However, strains of E. amylovora resistant to this antibiotic have been regularly isolated from Israel (Kleitman et al., 2005). Warning systems, which provide information on risk periods (according to climate, to inoculum and to plant stages), are used in several countries for determining the need for chemical controls; timing of treatment based on warning systems often reduces the number of sprays without a reduction in effectiveness (Billing, 2000). Such systems have been developed in the USA (Thomson et al., 1982; Smith, 1993; Steiner, 2000), in Europe (Jacquart-Romon and Paulin, 1991 ; Berger et al., 1996 ; Berrie and Billing, 1997 ; Billing, 2000) and in Israel (Shtienberg et al., 2003). Some are available commercially. Warning systems have usually been developed for one climatic area; the use of these systems in another climatic area needs to be done very carefully, considering the influence of the different climaticparameters on the epidemiology of the fire blight pathogen (Billing, 2007 ). The plant growth regulator prohexadione calcium (Apogee, Regalis) inhibits gibberellin biosynthesis and longitudinal shoot growth (Rademacker, 2000). When vegetative growth is inhibited by this regulator, it is less susceptible to fire blight (Sobiczewski et al., 2001); however, the chemical itself is not toxic to E. amylovora. In field studies, spread of fire blight during summer was reduced following the application of prohexadione calcium near the end of bloom period (Yoder et al., 1999 ; Costa et al., 2001 ). Recently, the two acylcyclohexanediones: prohexadione calcium and trinexapac ethyl, were shown to be able to reduce the incidence of fire blight on apple and pear flowers (Spinelli et al., 2007 ). Prohexadione calcium has been registered for growth and fire blight control in the USA and a few other countries. Acibenzolar-S-methyl (ASM; tradenames Actigard, Bion) can stimulate the tree's natural defence mechanisms and provide a significant level of fire blight control (Brisset et al., 2000 ; Maxson-Stein et al., 2002). The highest level of control was obtained when sprays of ASM were initiated at the pink stage of bud development and repeated at weekly intervals, and the level of control increased as treatment rates were increased (Maxson-Stein et al., 2002). ASM was shown to stimulate the expression of pathogenicity related (PR) proteins in apple suggesting that resistance was induced through a systemic acquired resistance (SAR) pathway (Brisset et al., 2000; Maxson-Stein et al., 2002). Biological Control Many experiments with antagonistic bacteria have been performed to control fire blight. Extensive field trials have been conducted mainly with strains of Pseudomonas agglomerans and Pseudomonas fluorescens (Vanneste, 1996; Johnson and Stockwell, 1998), 2000; Mercier and Lindow, 2001; Vanneste et al., 2002b). A goal of many of these studies has been to assess factors that influence establishment and spread of the bacterial antagonist (Nuclo et al., 1998; Stockwell et al., 1998; Pusey 1999, 2002; Johnson et al., 2000). Other studies have emphasized the integration of bacterial antagonist with antibiotics (Lindow et al., 1996; Stockwell et al., 1996). In spite of encouraging results, consistency in the level of control has not been easy to obtain. This and the difficulties in registering biological control agents are probably the two main reasons why biological control of fire blight is not widely practiced at present. Host-Plant Resistance Several studies on fire blight susceptibility of species, seedlings, cultivars and rootstocks have been carried out to identify resistant cultivars or sources of fire blight resistance; these sources of resistance are being used by breeding programmes in several countries for apple, pear and ornamentals (Lespinasse and Aldwinckle, 2000). In additional to the use of traditional breeding methods to produce new resistant cultivars, the feasibility of using genetic engineering methods to enhance the resistance of existing cultivars is being evaluated by several breeding programmes (Norelli and Aldwinckle, 2000).
