Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Phoma tracheiphila
(mal secco)

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Datasheet

Phoma tracheiphila (mal secco)

Summary

  • Last modified
  • 27 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Phoma tracheiphila
  • Preferred Common Name
  • mal secco
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Ascomycota
  •       Subphylum: Pezizomycotina
  •         Class: Dothideomycetes
  • Summary of Invasiveness
  • P. tracheiphila is a conidial fungus causing serious damage and death to the host, particularly lemon [Citrus limon], in Citrus and related genera, in Mediterranean countries and the Black Sea reg
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Pictures

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PictureTitleCaptionCopyright
Lemon tree severely affected by mal secco. Leaf and shoot chlorosis is followed by dieback of twigs and branches.
TitleDamaged lemon tree
CaptionLemon tree severely affected by mal secco. Leaf and shoot chlorosis is followed by dieback of twigs and branches.
CopyrightG. Perrotta/Università di Catania
Lemon tree severely affected by mal secco. Leaf and shoot chlorosis is followed by dieback of twigs and branches.
Damaged lemon treeLemon tree severely affected by mal secco. Leaf and shoot chlorosis is followed by dieback of twigs and branches.G. Perrotta/Università di Catania
Left: Lemon tree killed by mal secco. Suckers from the rootstock (sour orange) are a very common response of the host to the disease.
Right: Mal fulminante; a rapid, fatal form of mal secco.
TitleSeverely damaged lemon trees
CaptionLeft: Lemon tree killed by mal secco. Suckers from the rootstock (sour orange) are a very common response of the host to the disease. Right: Mal fulminante; a rapid, fatal form of mal secco.
CopyrightR. Tuttobene/Edagricole
Left: Lemon tree killed by mal secco. Suckers from the rootstock (sour orange) are a very common response of the host to the disease.
Right: Mal fulminante; a rapid, fatal form of mal secco.
Severely damaged lemon treesLeft: Lemon tree killed by mal secco. Suckers from the rootstock (sour orange) are a very common response of the host to the disease. Right: Mal fulminante; a rapid, fatal form of mal secco.R. Tuttobene/Edagricole
Infected lemon twig: leaves fall, leaving petiole on twig.
TitleTwig: damage symptoms
CaptionInfected lemon twig: leaves fall, leaving petiole on twig.
CopyrightEdagricole
Infected lemon twig: leaves fall, leaving petiole on twig.
Twig: damage symptomsInfected lemon twig: leaves fall, leaving petiole on twig.Edagricole
Lemon tree affected by mal secco showing the characteristic salmon-pink discolouration of the wood.
TitleDiscoloured wood of lemon tree
CaptionLemon tree affected by mal secco showing the characteristic salmon-pink discolouration of the wood.
CopyrightEdagricole
Lemon tree affected by mal secco showing the characteristic salmon-pink discolouration of the wood.
Discoloured wood of lemon treeLemon tree affected by mal secco showing the characteristic salmon-pink discolouration of the wood.Edagricole
Mal nero on orange tree: chronic infection leads to browning of heartwood.
TitleHeartwood browning (orange tree)
CaptionMal nero on orange tree: chronic infection leads to browning of heartwood.
CopyrightEdagricole
Mal nero on orange tree: chronic infection leads to browning of heartwood.
Heartwood browning (orange tree)Mal nero on orange tree: chronic infection leads to browning of heartwood.Edagricole
Conidia (2-4 x 0.5-1.5 µm) in cirrus extruding from pycnidium; stained with lactophenol cotton blue. Pycnidia measure 60-165 x 45-140 µm.
TitlePycnidium extruding conidia in cirrus
CaptionConidia (2-4 x 0.5-1.5 µm) in cirrus extruding from pycnidium; stained with lactophenol cotton blue. Pycnidia measure 60-165 x 45-140 µm.
CopyrightR. Tuttobene
Conidia (2-4 x 0.5-1.5 µm) in cirrus extruding from pycnidium; stained with lactophenol cotton blue. Pycnidia measure 60-165 x 45-140 µm.
Pycnidium extruding conidia in cirrusConidia (2-4 x 0.5-1.5 µm) in cirrus extruding from pycnidium; stained with lactophenol cotton blue. Pycnidia measure 60-165 x 45-140 µm.R. Tuttobene

Identity

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Preferred Scientific Name

  • Phoma tracheiphila (Petri) L.A. Kantsch. & Gikaschvili 1948

Preferred Common Name

  • mal secco

Other Scientific Names

  • Bakerophoma tracheiphila (Petri) Cif. 1946
  • Deuterophoma tracheiphila Petri 1929

International Common Names

  • English: citrus mal secco; citrus wilt; mal secco disease of citrus; wilt of citrus
  • Spanish: mal nero of citrus; mal seco de los cítricos
  • French: désséchement des agrumes

Local Common Names

  • Germany: Welke: Zitrus

EPPO code

  • DEUTTR (Deuterophoma tracheiphila)

Summary of Invasiveness

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P. tracheiphila is a conidial fungus causing serious damage and death to the host, particularly lemon [Citrus limon], in Citrus and related genera, in Mediterranean countries and the Black Sea region. So far, however, it is unknown in Spain, Portugal and Morocco, as well as other major citrus-growing regions of the world. This fungus is of concern to many international plant protection organizations and must be prevented from being spread in infected propagative material. It was once reported as seedborne in lemon, but there is no further evidence of this means of transmission. Once in the orchard, the fungus can be carried as spores from pycnidia and from hyphae on the plant and on fallen debris by rain, wind and irrigation water, and perhaps by birds and insects.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Ascomycota
  •             Subphylum: Pezizomycotina
  •                 Class: Dothideomycetes
  •                     Subclass: Pleosporomycetidae
  •                         Order: Pleosporales
  •                             Family: Pleosporaceae
  •                                 Genus: Phoma
  •                                     Species: Phoma tracheiphila

Notes on Taxonomy and Nomenclature

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Originally described as Deuterophoma tracheiphila by Petri (1929; 1930), this fungus was transferred to the genus Phoma (Ciccarone and Russo, 1969). It is currently considered a member of the Phoma subgenus Plenodomus due to the presence of thick-walled cells of scleroplectenchyma tissue in the pycnidia (Boerema et al., 1994). Many species in this subgenus have Leptosphaeria teleomorphs and/or Phialophora synanamorphs (Boerema et al., 2004). Molecular phylogenetic studies have supported the status of P. tracheiphila in Phoma and shown a relationship to some Leptosphaeria species (Balmas et al., 2005). The production of conidia on “free” hyphae outside of pycnidia has been described as Acremonium-like (Petri, 1929), as Cephalosporium to Cadophora–like (Goidanich and Ruggieri, 1947) and as a Phialophora sp. (Boerema et al., 2004).

Description

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Mature pycnidia black, 60-165 x 45-140 µm, ostiolate, neck distinct, protruding into host epidermis, to 250 µm long. Conidia minute, unicellular, hyaline, 2-4 x 0.5-1.5 µm produced by phialides lining cavity, extruded through ostiole in whitish cirrhi. Single phialides 12-30 x 3-6 µm also borne on hyphae growing on exposed wood surfaces, wounded plant tissues and within host xylem elements. Conidia larger, hyaline, unicellular, straight or curved, with rounded apices, 3-8 x 1.5-3.0 µm. Blastoconidia (sensu Goidanich et al., 1948) ovoid to subpyriform, 15-17 x 7-9 µm, produced inside the xylem vessel of host and in agar culture. No teleomorph is known. For more information see: Petri (1930); Graniti (1955); Ciccarone (1971); Punithalingam and Holliday (1973); and Boerema et al. (1994).
 

Distribution

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P. tracheiphila occurs in most citrus-growing countries of the Mediterranean and Black Sea basins (CABI/EPPO, 2004), but has not been reported from Spain, Portugal or Morocco (Duran-Vila and Moreno, 2000; Licciardello et al., 2006; Migheli et al., 2009). In Turkey, it was restricted to a certain area when discovered in 1933, but spread later with the expansion of citrus plantations (Tuzcu et al., 1989).
 
The presence of P. tracheiphila in Colombia, Uganda and Queensland, Australia has been reported, but these identifications are considered doubtful and the records are excluded from the distribution mapped by CABI/EPPO (2004). See also Migheli et al. (2009).

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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ArmeniaPresentDuran-Vila and Moreno, 2000
Georgia (Republic of)PresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
IraqPresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
IraqPresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
IsraelRestricted distributionCMI, 1989; CABI/EPPO, 2004; Ezra et al., 2007; EPPO, 2014
LebanonPresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
LebanonPresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
SyriaPresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
SyriaPresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
TurkeyRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
YemenRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
YemenRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014

Africa

AlgeriaRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
AlgeriaRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
EgyptPresentPunithalingam and Holliday, 1973; CMI, 1989; CABI/EPPO, 2004; EPPO, 2014
EgyptPresentPunithalingam and Holliday, 1973; CMI, 1989; CABI/EPPO, 2004; EPPO, 2014
LibyaPresentPunithalingam and Holliday, 1973; CMI, 1989; CABI/EPPO, 2004; EPPO, 2014
LibyaPresentPunithalingam and Holliday, 1973; CMI, 1989; CABI/EPPO, 2004; EPPO, 2014
TunisiaPresentCMI, 1989; CABI/EPPO, 2004; Hajlaoui et al., 2008; EPPO, 2014

South America

ColombiaAbsent, unreliable recordEPPO, 2014

Europe

AlbaniaPresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
AlbaniaPresentCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
AustriaAbsent, no pest recordEPPO, 2014
BelgiumAbsent, no pest recordEPPO, 2014
CyprusRestricted distribution1933CMI, 1989; CABI/EPPO, 2004; EPPO, 2014
FranceRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
-CorsicaPresent, few occurrencesEPPO, 2014
GreeceWidespreadProtopapadakis and Zambettakis, 1981; CMI, 1989; CABI/EPPO, 2004; EPPO, 2014; Karapapa et al., 2015
-CretePresentEPPO, 2014
ItalyPresentCMI, 1989; CABI/EPPO, 2004; Balmas et al., 2005; EPPO, 2014
-SardiniaPresentEPPO, 2014
-SicilyPresentEPPO, 2014
NetherlandsAbsent, confirmed by surveyNPPO of the Netherlands, 2013; EPPO, 2014Based on ongoing long-term monitoring for plant passport system.
Russian FederationRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
Russian FederationRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014
-Southern RussiaRestricted distributionCMI, 1989; CABI/EPPO, 2004; EPPO, 2014Caucasus region
UKAbsent, no pest recordEPPO, 2014

Risk of Introduction

Top of page P. tracheiphila is of quarantine concern to most regional plant protection organizations (APPPC, CPPC, COSAVE, IAPSC, NAPPO). The fungus does not occur in several citrus-growing countries of the EPPO region, especially in the Iberian peninsula and Morocco. The introduction of P. tracheiphila is principally a threat to lemon growing in Spain and Portugal. The fact that P. tracheiphila does not already occur throughout the Mediterranean citrus-growing areas is possibly linked with the severe restrictions on movement of citrus propagating material mainly in relation to virus diseases. There is no obvious climatic or cultural factor limiting potential establishment of mal secco in uninfected areas.

RISK CRITERIA CATEGORY

ECONOMIC IMPORTANCE High

DISTRIBUTION Limited

SEEDBORNE INCIDENCE Yes

SEED TRANSMITTED Not recorded

SEED TREATMENT None

OVERALL RISK Low
 

Habitat List

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CategoryHabitatPresenceStatus
Terrestrial-managed
Managed forests, plantations and orchards Present, no further details Harmful (pest or invasive)

Hosts/Species Affected

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Almost all Citrus species are susceptible to P. tracheiphila by inoculation (Perrotta and Graniti, 1988; Tuzcu et al., 1989). Lemon (Citrus limon) is probably the most affected crop (Perrotta and Graniti, 1988). Other susceptible species are citron (Citrus medica), bergamot (Citrus bergamia), mandarins (Citrus reticulata), and sour orange, (Citrus aurantium). In the field, hybrids of Citrus, related genera (Fortunella, Poncirus and Severinia), and other species, have different degrees of resistance to the disease (Solel and Salerno, 2000). Most cultivars of sweet oranges (Citrus sinensis), grapefruit (Citrus paradisi), and some mandarins and clementines (Citrus deliciosa and C. reticulata), are only occasionally affected (Solel and Salerno, 2000). A number of rootstocks such as Citrus reshni, Poncirus trifoliata and, to a lesser extent, Citrus sinensis x Phoma trifoliata have been reported to be resistant (Perrotta and Graniti, 1988). Results of susceptibility tests can differ between investigators and between tests that use artificial inoculation and those that expose trees to natural infection (Tuzcu et al., 1989).

 

Growth Stages

Top of page Fruiting stage, Vegetative growing stage

Symptoms

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The first symptoms appear in spring as shoot and interveinal leaf chlorosis followed by a dieback of twigs and branches. Raised black points within lead-grey or ash-grey areas of withered twigs indicate the presence of pycnidia. The growth of sprouts from the base of the affected branches and suckers from the rootstock are a very common response of the host to the disease. Individual branches or sectors may be infected initially (Solel and Salerno, 2000). Gradually the pathogen affects the entire tree, which eventually dies. When the wood of infected twigs, branches or trunks is cut or stripped of bark, the characteristic salmon-pink or orange-red discolouration of the wood may be seen; this internal symptom is associated with gum production within the xylem vessels (Perrotta and Graniti, 1988).
 
In addition to the more common form of mal secco, two other forms of the disease are distinguished: “mal fulminante”, in which the tree declines and dies rapidly, apparently due to root infection; and “mal nero”, which is a chronic infection of the tree that causes a browning of the heartwood (Perrotta and Graniti, 1988).

List of Symptoms/Signs

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SignLife StagesType
Fruit / premature drop
Leaves / abnormal colours
Leaves / abnormal leaf fall
Leaves / wilting
Stems / dieback
Stems / witches broom
Whole plant / plant dead; dieback
Whole plant / wilt

Biology and Ecology

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Life Cycle

The fungus enters through wounds in leaves, branches and roots; penetration through stomata is questionable (Zucker and Catara, 1985; Perrotta and Graniti, 1988). Cultivation practices as well as wind, frost and hail, which cause injuries to various parts of the trees, favour infection. Inoculum may be provided both by conidia produced in pycnidia on withered twigs and by conidia produced from phialides borne on hyphae on exposed woody surfaces of the tree or on debris on the ground. The conidia are thought to be waterborne for the most part (Solel, 1976). The temperature range at which infection will occur is between 14 and 28°C. In the Mediterranean region, infection periods depend on local climatic and seasonal conditions; in Sicily, infections usually occur between September and April (Somma and Scarito, 1986).

The length of the incubation period may vary according to the season (Grasso and Tirrò, 1984). The optimum temperature for growth of the pathogen and symptom expression is 20-25°C, whereas the maximum temperature for mycelial growth in culture is 30°C (Perrotta and Graniti, 1988). Discarded prunings containing affected twigs or branches can be a source of inoculum for several weeks. A relative humidity near saturation and temperatures between 20 and 25°C are best for production of phialides on hyphae in wounds and natural leaf scars (De Cicco et al., 1986). The fungus can survive within infected twigs in the soil for more than 4 months (De Cicco et al., 1987).

Reproductive Biology

No teleomorph is known, and the genetic uniformity among isolates in Italy (Balmas et al., 2005) and Israel (Ezra et al., 2007) indicates that sexual recombination is not commonly occurring in these Mediterranean regions.

Physiology and Phenology

P. tracheiphila produces an extracellular glycoprotein toxin that reproduces the symptoms of veinal chlorosis, necrosis and wilt when injected into lemon leaves (Nachmias et al., 1977). This toxin has been named “malseccin” (Reverberi et al., 2008).

In Italy, two types of strains have been reported: chromogenic strains that produce a red pigment in culture; and non-chromogenic strains that do not produce this pigment, but show a yellow colour (Graniti, 1969). Limited data indicate no difference in pathogenicity that is clearly related to this variation, although variation in virulence does occur in P. tracheiphila (Magnano di San Lio et al., 1992; Magnano di San Lio and Perrotta, 1986). Among 600 isolates from lemon [Citrus limon] in Sicily, all but a few were chromogenic, and there were no remarkable differences in colony morphology within either type. On some media, some of the chromogenic isolates underwent sectoring to yield a variant that does not produce pycnidia (Magnano di San Lio and Perrotta, 1986). In Israel, both chromogenic and non-chromogenic strains could be isolated from a single tree (Ezra et al., 2007).

Associations

Acervuli of the Colletotrichum state of Glomerella cingulata, a secondary invader of withered twigs, are often associated with the pycnidia of P. tracheiphila (Migheli et al., 2009).

Climate

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ClimateStatusDescriptionRemark
BW - Desert climate Tolerated < 430mm annual precipitation
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers

Means of Movement and Dispersal

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Natural Dispersal

Conidia are dispersed from the trees and debris by rain splash or overhead irrigation (Solel and Salerno, 2000). Some may become airborne; Balmas et al. (2005) obtained isolates in Italy from air samples. Laviola and Scarito (1989) found the fungus spreading only a short distance, between 15 and 20 m, from a source of inoculum, although the prevailing wind direction did increase the distance.

Vector Transmission

Transmission by vectors has not been reported, but is possible. Birds and insects have been suggested as non-specific carriers of the fungus between trees (Perrotta and Graniti, 1988).

Accidental Introduction

Systemic infection due to release of spores in the xylem will result in most parts of the tree being able to carry the fungus. The pathogen has been detected in asymptomatic parts (Balmas et al., 2005; Ezra et al., 2007). Isolation from lemon seed was reported (Stepanov and Shaluishkina, 1952), but seedborne transmission to new trees was not demonstrated. If not carried out carefully, pruning, whether or not carried out for disease control, may contaminate the tools used.

Seedborne Aspects

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Incidence

P. tracheiphila has been detected in lemon seeds (Stepanov and Shaluishkina, 1952). There is no evidence that it is seedborne in other species.

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Plants or parts of plantsPropagating material, pruning debris, fallen leaves Yes Perrotta and Graniti, 1988
WaterRain splash, surface flow Yes Punithalingam and Holliday, 1973; Solel and Salerno, 2000
Wind Yes Balmas et al., 2005; Laviola and Scarito, 1989

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Bark fruiting bodies; hyphae; spores Yes Yes Pest or symptoms usually visible to the naked eye
Leaves hyphae; spores Yes Yes Pest or symptoms usually visible to the naked eye
Stems (above ground)/Shoots/Trunks/Branches fruiting bodies; hyphae; spores Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Wood hyphae; spores Yes Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Plant parts not known to carry the pest in trade/transport
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Growing medium accompanying plants
Roots
Seedlings/Micropropagated plants

Impact Summary

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CategoryImpact
Economic/livelihood Negative

Economic Impact

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In the Mediterranean region, P. tracheiphila is the most destructive fungal pathogen of lemons [Citrus limon]. Up to 100% of trees in an orchard of a susceptible lemon cultivar can be affected (Perrotta and Graniti, 1988). Destructive outbreaks of the disease may occur after frost spells and hail storms in spring (Perrotta and Graniti, 1988). In general, injury to the tree through severe cold weather may predispose it to fungal attack. The symptoms of the disease are most severe in spring and autumn; at high summer temperatures, spread of the fungus in the vascular system ceases and the symptoms do not develop further (Ruggieri, 1953). In the areas where the pathogen is present, the disease reduces the quantity and quality of lemon production and limits the use of susceptible species and cultivars. It has been estimated that complete control of the pathogen could cause a doubling of lemon harvests (Gulsen et al., 2007).

The potential impact of invasion by this fungus on the lemon industry alone may be estimated from the fact that fresh lemon fruit are produced and shipped from countries on five continents (Migheli et al., 2009). Restrictions to prevent importation of possibly infected fruit of additional Citrus species could create economic damage in other countries.

Risk and Impact Factors

Top of page Invasiveness
  • Invasive in its native range
  • Abundant in its native range
  • Fast growing
  • Has high reproductive potential
  • Reproduces asexually
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts livelihoods
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult/costly to control

Diagnosis

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Control of P. tracheiphila by exclusion, eradication, and treatment will be facilitated by rapid detection of the pathogen. Molecular techniques have been developed to provide a fast, specific and sensitive method that isolation in culture and morphological examination cannot. The standard PCR assay of Balmas et al. (2005) provides a more specific and sensitive test than the older one of Rollo et al. (1990); it distinguishes the pathogen from other Phoma species and detects its presence in both symptomatic and asymptomatic tissue, including wood. Another protocol was developed by Ezra et al. (2007) with specific concern for detection in fruit and distinguishing P. tracheiphila from other fungal pathogens of Citrus. Nevertheless, the standard method may not be sensitive enough for all monitoring or quarantine purposes (Demontis et al., 2007). Real-time PCR protocols have been published by Licciardello et al. (2006) and Demontis et al. (2007). These are capable of detecting pathogen DNA in picogram quantities in host tissue, so are suitable for quantitative work and detection of latent infections.
 
Sequences of several regions of nuclear DNA, including those of the ITS region obtained by Balmas et al. (2005) are available for P. tracheiphila on GenBank (NCBI, 2010). A diagnostic protocol for P. tracheiphila is detailed in OEPP/EPPO (2007).

 

Detection and Inspection

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The leaves of affected trees should be checked for the chlorosis around veins that is an early symptom of the disease (Perrotta and Graniti, 1988). By stripping the bark or cutting into the wood, one can examine trees for the presence of the typical salmon-pink to orange-red discolouration of the xylem (Migheli et al., 2009). An ashy colour of the dead twigs will result from lifting of the epidermis by growth of pycnidia produced underneath (Perrotta and Graniti, 1988). The fungus can be isolated from infected twigs on various solid media, including PDA (Magnano di San Lio and Perotta, 1986).

Similarities to Other Species/Conditions

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The species of Phoma in the section Plenodomus, including P. tracheiphila, are difficult to identify in culture, because there is frequently little production of pycnidia and those produced do not have typical distinguishing morphology (Boerema et al., 2004). The limited host range of most species is useful; the species most morphologically similar to P. tracheiphila, Phoma coonsii, is found on apple (Malus pumila) in Japan and North America (Boerema et al., 2004). Species in the section Phoma that have a wide host range and may also appear on Citrus as saprophytes or secondary pathogens are difficult to identify in vitro (Boerema et al., 2004). The “mal secco” pathogen can be distinguished primarily by its production of conidia from phialides on “free” hyphae both on the plant and in culture (De Cicco et al., 1986; Boerema et al., 2004).
 
A difficulty with isolation of P. tracheiphila is the frequent need to separate it from Colletotrichum gloeosporioides, which infects the lesions as a secondary pathogen, but can grow faster in culture (Migheli et al., 2009). Colonies of the primary pathogen are easily distinguished from the reddish to orange colonies of the common epiphytic fungus, Epicoccum sp. (Migheli et al., 2009), whose clusters of dark, rough-walled, multicellular conidia (Ellis, 1971) are distinctive. The reddish pigments produced by P. tracheiphila on oatmeal agar after growth under alternating NUV light and darkness turn blue when concentrated sodium hydroxide (NaOH) is added (Boerema et al., 2004). In cultures on PDA, the red pigments form clusters of crystals on the mycelium and agar (Solel and Salerno, 2000).
 
Other diseases that may result in sudden or slow wilting and dieback of citrus, sometimes with veinal chlorosis, are infection with the tristeza virus, if the tree has a sour orange rootstock, and Phytophthora rot or foot rot, if the rootstock is virus-tolerant (Timmer et al., 2000). Huanglongbing, a systemic disease caused by an invasive bacterium in Asia and Africa, also causes slow decline of citrus trees, with yellowing of leaves and dieback of branches (Garnier and Bove, 2000). Drought, mechanical wounding, frost injury and other stresses can weaken trees and allow infections by weakly pathogenic fungi that result in branch cankers and dieback (Graham and Menge, 2000).

Prevention and Control

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Prevention

SPS measures

In countries or areas where the disease has not yet been reported, great care must be taken not to use plants from nurseries located in areas where the pathogen occurs for new plantings or replantings. P. tracheiphila is on the A2 list of quarantine organisms for the European and Mediterranean Plant Protection Organization (EPPO) for whom the threat is most immediate. It is of concern for exclusion by other regional plant protection organizations worldwide (Migheli et al., 2009).

Eradication

In 1998, the government of Italy mandated the destruction of infected plant material, including the uprooting and burning of the tree stumps (Migheli et al., 2009).

Control

Cultural control and sanitary measures

P. tracheiphila may be kept under control by pruning infected twigs as soon as the first symptoms appear (Salerno and Cutuli, 1982). Common practices aimed either at saving the affected trees or at eradicating the inoculum include removal of whole branches and grafting the resulting pollarded tree with resistant cultivars or species. Burning of the pruned branches is recommended in order to eliminate possible sources of inoculum (Solel and Salerno, 2000). Injury during cultural practices must be avoided; cultivation of the orchard in the autumn may create wounds in the roots that will be slow to heal (Duran-Vila and Moreno, 2000).

Biological control

Infection with the citrus exocortis viroid was shown to prevent infection by the fungus (Solel et al., 1995). Trees have been inoculated with a hypovirulent strain of the pathogen in an effort to achieve a similar effect (Solel and Salerno, 2000).

Cirvilleri et al. (2005) found a genetically heterogeneous group of rhizosphere-inhabiting pseudomonad bacteria, mostly Pseudomonas fluorescens and Pseudomonas putida, that inhibited Phoma tracheiphila growth in culture; 248 isolates were obtained from both wild-type and transgenic rolABC rough-lemon rootstocks and 13 from only the genetically modified plants. The possible role these organisms could have in Citrus protection was not examined.

Chemical control

Chemical control is not widely used except in nurseries. Copper fungicides and ziram are the most common products used. The protectant copper fungicides will need to be applied repeatedly to the canopy during the period of greatest susceptibility from autumn to spring (Solel and Salerno, 2000). Systemic products such as carboxin and benzimidazole are also effective only as preventives (Solel and Salerno, 2000) and some that were effective as soil drenches in pot tests were found ineffective in the field (Solel et al., 1972). A mixture of a protectant and a systemic fungicide is recommended by Duran-Vila and Moreno (2000), particularly after weather conditions, such as a freeze, hailstorm, or strong winds that cause wounds to the tree.

Host resistance

The best method of controlling the disease would be to grow resistant clones, but unfortunately this is not easily achieved. In some areas of Sicily, the susceptible cultivar Femminello has been replaced by the resistant lemon cultivar Monachello, which is of inferior quality. Resistant clones of cv. Femminello have been selected, but they either do not adapt to different environmental conditions or have still to be tested in the field (Gentile et al., 1992; Salerno and Cutuli, 1992). The cultivar, Santa Teresa was recommended as resistant and suitable for Greece (Protopapadakis and Zambettakis, 1981). Recently, in Turkey, selection and breeding have resulted in a good genotype of lemon, Tuzcu 894, which has high yield per tree, good fruit weight, high juice content and low seed number, and so may be a replacement for the common agronomically desirable, but susceptible cultivar, Kutdiken (Uzun et al., 2009).

Various, more rapid, modern means have been used to try to obtain resistant germplasm. Somatic hybrids of susceptible and resistant lines were of intermediate resistance (Tusa et al., 2000). Budwood was irradiated to produce mutant tissue; types with varied levels of resistance were obtained (Gulsen et al., 2007). Protoplasts (Gentile et al., 1992) and culture callus (Bas and Koç, 2006) of Citrus species have been exposed to the toxin malseccin as a means of selection. Most recently, Femminello lemon plants have been transformed with a Trichoderma harzianum endo-chitinase gene coding for a protein that is then produced in the leaves and inhibits growth of the pathogen in culture (Gentile et al., 2007).

Gaps in Knowledge/Research Needs

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The reasons why the pathogen is not a problem in countries at the western end of the Mediterranean region may have significance for control of the disease. Exploration of possible biological controls, acting either outside or inside the tree, should be continued.

References

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Balmas V; Scherm B; Ghignone S; Salem AOM; Cacciola SO; Migheli Q, 2005. Characterisation of Phoma tracheiphila by RAPD-PCR, microsatellite-primed PCR and ITS rDNA sequencing and development of specific primers for in planta PCR detection. European Journal of Plant Pathology, 111(3):235-247. http://springerlink.metapress.com/link.asp?id=100265

Bas B; Koç NK, 2006. In vitro selection of Kütdiken lemon 20b to canditate for resistance to Phoma tracheiphila. Plant Pathology Journal (Faisalabad), 5(1):35-40. http://www.ansinet.org/ppj

Boerema GH; de Gruyter J; van Kesteren HA, 1994. Contributions towards a monograph of Phoma (Coelomycetes) - III. I. Section Plenodomus: Taxa often with a Leptosphaeria teleomorph. Persoonia, 15(4):431-487.

Boerema GH; Gruyter Jde; Noordeloos ME; Hamers MEC, 2004. Phoma identification manual. Differentiation of specific and infra-specific taxa in culture [ed. by Boerema, G. H.\Gruyter, J. de\Noordeloos, M. E.\Hamers, M. E. C.]. Wallingford, UK: CABI Publishing, viii + 470 pp. http://www.cabi.org/CABeBooks/default.aspx?site=107&page=45&LoadModule=PDFHier&BookID=188

CABI/EPPO, 1998. Distribution maps of quarantine pests for Europe (edited by Smith IM, Charles LMF). Wallingford, UK: CAB International, xviii + 768 pp.

CABI/EPPO, 2004. Phoma tracheiphila. Distribution Maps of Plant Diseases, No. 155. Wallingford, UK: CAB International.

Ciccarone A, 1971. The fungus of mal secco in citrus. Phytopathologia Mediterranea, 10:68-75.

Ciccarone A; Russo M, 1969. First contribution to the systematics and morphology of the causal agent of the "mal secco" disease of citrus (Deuterophoma tracheiphila Petrie). In: Proceedings of the 1st International Citrus Symposium, Vol. III. 1239-1249.

Cirvilleri G; Spina S; Scuderi G; Gentile A; Catara A, 2005. Characterization of antagonistic root-associated fluorescent pseudomonads of transgenic and non-transgenic citrange Troyer plants. Journal of Plant Pathology, 87(3):179-186.

De Cicco V; Ippolito A; Salerno M, 1987. Duration of the infective capacity of soil containing mal secco infected lemon twigs. Proceedings of the 7th Congress of the Mediterranean Phytopathological Union, Granada, Spain, 20-26 September, 1987, 175-176.

De Cicco V; Paradies M; Ippolito A; Salerno M, 1986. Formation of Phoma tracheiphila free phialides in controlled environments. Phytopathologia Mediterranea, 25:107-110.

Demontis MA; Cacciola SO; Orru M; Balmas V; Chessa V; Maserti BE; Mascia L; Raudino F; Magnano Di San Lio G; Migheli Q, 2007. Development of real-time PCR systems based on SYBR(r) Green I and TaqMan(r) technologies for specific quantitative detection of Phoma tracheiphila in infected citrus. European Journal of Plant Pathology, 120:339-347.

Deng ZN; Gentile A; Domina F; Nicolosi E; Tribulato E; Vardi A, 1995. Recovery of Citrus somatic hybrids tolerant to Phoma tracheiphila toxin, combining selection and identification by RAPD markers. Current issues in plant molecular and cellular biology. Proceedings of the 8th International Congress on Plant Tissue and Cell Culture, Florence, Italy, 12-17 June, 1994., 177-183; [^italic~Current Plant Science and Biotechnology in Agriculture^roman~ Volume 22]; 15 ref.

Duran-Vila N; Moreno P, 2000. Enfermedades de los cítricos. Madrid, Spain: Ediciones Mundi-Prensa, 165 pp.

Ellis MB, 1971. Dematiaceous Hyphomycetes. Wallingford, UK: CAB International.

EPPO, 2007. Phoma tracheiphila. Bulletin OEPP/EPPO Bulletin, 37(3):521-527. http://www.blackwell-synergy.com/doi/full/10.1111/j.1365-2338.2007.01159.x

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Ezra D; Kroitor T; Sadowsky A, 2007. Molecular characterization of Phoma tracheiphila, causal agent of Mal secco disease of citrus, in Israel. European Journal of Plant Pathology, 118(2):183-191. http://springerlink.metapress.com/link.asp?id=100265

Garnier M; Bove JM, 2000. Huanglonbing (greening). In: Compendium of Citrus Diseases. Second edition [ed. by Timmer, L. W.\Garnsey, S. M.\Graham, J. H.]. St. Paul, Minnesota, USA: American Phytopathological Society, 46-48.

Gentile A; Deng Z; Malfa Sla; Distefano G; Domina F; Vitale A; Polizzi G; Lorito M; Tribulato E, 2007. Enhanced resistance to Phoma tracheiphila and Botrytis cinerea in transgenic lemon plants expressing a Trichoderma harzianum chitinase gene. Plant Breeding, 126(2):146-151. http://www.blackwell-synergy.com/doi/pdf/10.1111/j.1439-0523.2007.01297.x

Gentile A; Tribulato E; Deng ZN; Vardi A, 1992. Selection of "Femminello" lemon plants with tolerance to the toxin of Phoma tracheiphila via cell culture. VII International Citrus Congress, Acireale, Italy, March 8-13, 1992.

Goidanich G; Ruggieri G, 1947. The Deuterophomaceae of Petri. Annali della Sperimentazione Agraria N.S., 1:431-438.

Goidanich G; Ruggieri G; Gagnotto A, 1948. Presence of a third type of agamic fructification in Deuterophoma tracheiphila Petri. Annali della Sperimentazione Agraria N.S., 2:671-675.

Graham JH; Menge JA, 2000. Branch and twig diebacks. In: Compendium of Citrus Diseases. Second edition [ed. by Timmer, L. W.\Garnsey, S. M.\Graham, J. H.]. St. Paul, Minnesota, USA: American Phytopathological Society, 70-71.

Graniti A, 1955. Morphology of Deuterophoma tracheiphila Petri and a discussion of the genus Deuterophoma. Bollettino dell'Accademia Gioenia Sez., 4(3): 93-110.

Graniti A, 1969. Host-parasite relation in Citrus diseases as exemplified by Phytophthora gummosis and Deuterophoma "mal secco". Proceedings of the 1st International Citrus Symposium Vol. III, 1187-1200.

Grasso S; Tirro A, 1984. Observations on the seasonal susceptibility of lemon to mal secco infections. Rivista di Patologia Vegetale, 20(1):13-19

Gulsen O; Uzun A; Pala H; Canihos E; Kafa G, 2007. Development of seedless and mal secco tolerant mutant lemons through budwood irradiation. Scientia Horticulturae, 112(2):184-190. http://www.sciencedirect.com/science/journal/03044238

Hajlaoui MR; Kalai L; Mnari-Hattab M; Guermech A; Abdelaal NB, 2008. Occurrence of 'mal nero' disease on mandarin and orange trees in Tunisia. Plant Pathology, 57(4):784. http://www.blackwell-synergy.com/loi/ppa

Karapapa V; Doudoumis V; Tsiamis G, 2015. First report of Phoma tracheiphila causing severe mal secco disease on a mandarin hybrid (cv. Ortanique) grafted onto Citrumelo rootstock in western Greece. New Disease Reports, 31:20. http://www.ndrs.org.uk/article.php?id=031020

Laviola C; Scarito G, 1989. Distance and direction of dissemination of Phoma tracheiphila (Petri) Kanc. et Ghik. propagules. Phytopathologia Mediterranea, 28:161-163.

Licciardello G; Grasso FM; Bella P; Cirvilleri G; Grimaldi V; Catara V, 2006. Identification and detection of Phoma tracheiphila, causal agent of citrus mal secco disease, by real-time polymerase chain reaction. Plant Disease, 90(12):1523-1530. HTTP://www.apsnet.org

Magnano di San Lio G; Cacciola SO; Pane A; Grasso S, 1992. Relationship between xylem colonization and symptom expression in citrus mal secco disease. VII International Citrus Congress, Acireale, Italy, March 8-13, 1992.

Magnano di San Lio G; Perrotta G, 1986. Variability in Phoma tracheiphila. In: Cavalloro E Di Martino R, ed. Proceedings of the Experts' Meeting, Acireale, Italy, 26-29 March, 267-270.

Migheli Q; Cacciola SO; Balmas V; Pane A; Ezra D; San Lio GMdi, 2009. Mal secco disease caused by Phoma tracheiphila: a potential threat to lemon production worldwide. Plant Disease, 93(9):852-867. http://apsjournals.apsnet.org/loi/pdis

Nachmias A; Barash I; Solel Z; Strobel GA, 1977. Purification and characterization of a phytotoxin produced by Phoma tracheiphila, the causal agent of mal secco disease of citrus. Physiological Plant Pathology, 10(2):147-157.

NCBI, 2010. Entrez cross-database search engine. Entrez cross-database search engine. Bethesda, Maryland, USA: National Center for Biotechnology Information, U.S. National Library of Medicine, unpaginated. http://www.ncbi.nlm.nih.gov/sites/gquery

Perrotta G; Graniti A, 1988. Phoma tracheiphila (Petri). Kantschaveli et Gikashvili. In: Smith IM, Dunez J, Lelliot RA, Phillips DH, Archer SA, eds. European Handbook of Plant Diseases. Oxford, UK: Blackwell Scientific Publications, 396-398.

Petri L, 1929. On the systematic position of parasitic fungi of lemon plants affected by mal secco. Bollettino della Stazione di Patologia Vegetale, 9:393-396.

Petri L, 1930. Latest research on the morphology, biology and parasitism of Deuterophoma tracheiphila. Bollettino della Stazione di Patologia Vegetale, 10:191-221.

Protopapadakis E; Zambettakis C, 1981. Study of the susceptibility of different lemon clones to mal secco (disease caused by the fungus Deuterophoma tracheiphila Petri). (Etude de la sensibilite de differents clones du citronnier au mal-secco (maladie provoquee par le champignon Deuterophoma tracheiphila Petri).) Bulletin Trimestriel de la Societe Mycologique de France, 97(3):143-148.

Punithalingam E; Holliday P, 1973. Deuterophoma tracheiphila. CMI Descriptions of Pathogenic Fungi and Bacteria, No. 399. Wallingford, UK: CAB International.

Reverberi M; Betti C; Fabbri AA; Zjalic S; Spadoni S; Mattei B; Fanelli C, 2008. A role for oxidative stress in the Citrus limon/Phoma tracheiphila interaction. Plant Pathology, 57(1):92-102. http://www.blackwell-synergy.com/loi/ppa

Rollo F; Salvi R; Torchia P, 1990. Highly sensitive and fast detection of Phoma tracheiphila by polymerase chain reaction. Applied Microbiology and Biotechnology, 32(5):572-576.

Ruggieri G, 1953. Periodicity of infection by mal secco and main strategies of control. Giornale di Agricoltura, 34.

Salerno M; Cutuli G, 1981. The management of fungal and bacterial diseases of citrus in Italy. Proceedings of the International Society of Citriculture, 1:360-362.

Salerno M; Cutuli G, 1982. The management of fungal and bacterial diseases of citrus in Italy. Proceedings of the International Society of Citriculture, 1981 No. 1, 360-362.

Salerno M; Cutuli G, 1992. Mal secco disease. In: Salerno M, Cutuli G, eds. Guida illustrata di patologia degli agrumi. Bologna, Italy: Edagricole, 22-29.

Solel Z, 1976. Epidemiology of mal secco disease of lemons. Phytopathologische Zeitschrift, 85(1):90-92

Solel Z; Mogilner N; Gafny R; Bar-Joseph M, 1995. Induced tolerance to mal secco disease in Etrog citron and Rangpur lime by infection with the citrus exocortis viroid. Plant Disease, 79(1):60-62

Solel Z; Pinkas J; Loebenstein G, 1972. Evaluation of systemic fungicides and mineral oil adjuvants for the control of mal secco disease of lemon plants. Phytopathology, 62(9):1007-1013.

Solel Z; Salerno M, 1989. Mal secco. In: Whiteside JO, Garnsey SM, Timmer LW, eds. Compendium of Citrus Diseases. St. Paul, Minnesota, USA: American Phytopathological Society, 18-19.

Solel Z; Salerno M, 2000. Mal secco. In: Timmer LW, Garnsey SM, Graham JH, eds. Compendium of Citrus Diseases. Second edition. St. Paul, Minnesota, USA: American Phytopathological Society, 33-35.

Somma V; Sammarco G, 1986. Further researches on the periodicity of infections by Phoma tracheiphila in Sicily and preliminary observations on the incubation period of "mal secco" disease of Citrus. Giornate Fitopatologiche, 2:115-124.

Somma V; Scarito G, 1986. Three years of observations on the periodicity of Phoma tracheiphila (Petri) Kanc. & Ghik. infections in Sicily. Phytopathologia Mediterranea, 25(1-3):103-106

Stepanov KM; Shaluishkina VI, 1952. Lemon fruit and seeds - sources of initial infectious dessication. Microbiology Moscow, 28:48-51.

Thanassoulopoulos CC, 1985. Epidemiological aspects ol Malsecco disease of lemons. Proceedings of the Integrated Pest Control in Citrus-Groves. Acireale, Italy, 249-255.

Timmer LW; Garnsey SM; Graham JH, 2000. Brief guide to field identification of citrus diseases. In: Compendium of Citrus Diseases. Second edition [ed. by Timmer, L. W.\Garnsey, S. M.\Graham, J. H.]. St. Paul, Minnesota, USA: American Phytopathological Society, 84-87.

Tusa N; Bosco SFdel; Nigro F; Ippolito A, 2000. Response of cybrids and a somatic hybrid of lemon to Phoma tracheiphila infections. HortScience, 35(1):125-127.

Tuttobene R, 1993. Citrus mal secco. Informatore Fitopatologico, 43(6):25-30

Tuttobene R, 1994. Monitoring of Phoma tracheiphila inoculum. Difesa delle Piante, 17(1-2):69-74

Tuzcu O; Cinar A; Kaplankiran M; Erkilic A; Yesiloglu T, 1989. Resistance of some Citrus species and hybrids to mal secco (Phoma tracheiphila Kanc. et Ghik.) disease. Fruits, 44(3):139-148.

Uzun A; Gulsen O; Kafan G; Seday U; Tuzcu O; Yesiloglu T, 2009. Characterization for yield, fruit quality, and molecular profiles of lemon genotypes tolerant to 'mal secco' disease. Scientia Horticulturae, 122:556-561.

Zucker WV; Catara A, 1985. Scanning electron microscopy observations on foliar penetration by Phoma tracheiphila. (Osservazioni al microscopio elettronico a scansione sulla penetrazione fogliare di Phoma tracheiphila.) Informatore Fitopatologico, 35(4):33-35.

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02/04/10 Updated by:

Systematic Mycology & Microbiology Laboratory, USDA-ARS, 10300 Baltimore Ave., Beltsville, MD 20705, USA

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