Section outline

  • Diana Marčiulynienė

    Lithuanian Research Centre for Agriculture and Forestry, Institute of Forestry, Kaunas; Lithunia

    Lithuanian Research Centre for Agriculture and Forestry | LinkedIn

      • The genus Lecanosticta includes nine species, among which Lecanosticta acicola is the oldest documented and most well-known (van der Nest et al., 2019). The pathogen is an ascomycete fungus causing brown spot needle blight (BSNB), a foliar disease affecting native and non-native Pinus spp. in many regions of the world. Damage is expressed as yellow to brown spots or bands of discoloration that result in premature needle shedding with significant growth reduction and possible death of the trees. In the European Union, L. acicola is a regulated non-quarantine pest (European Commission, 2019).

      • Kingdom: Fungi, Phylum: Ascomycota, Subphylum: Pezizomycotina, Class: Dothideomycetes, Subclass: Dothideomycetidae, Order: Mycosphaerellales, Family: Mycosphaerellaceae, GenusLecanosticta, Species: Lecanosticta acicola (von Thümen) Sydow

      • Synonyms

        • Cryptosporium acicola (von Thümen)
        • Dothiostroma acicola (von Thümen) Schischkina & Tsanava
        • Lecanosticta pini Sydow
        • Mycosphaerella dearnessii Rostrup
        • Oligostroma acicola Dearness
        • Scirrhia acicola (Dearness) Siggers
        • Septoria acicola (von Thümen) Saccardo
        • Systremma acicola (Dearness) Wolf & Barbour

        Local names

        • Brown spot needle blight (English)
        • Brown spot of pine (English)
        • Needle blight of pine (English)
        • Tache brune des aiguilles du pin (French)
        • Mancha parda de las aciculas del pino (Spanish)
        • Hnědá sypavka borovice (Czech)
        • Hnedá sypavka borovíc (Slovak)
        • Smieđa pjegavost iglica (Croatian)
        • Braunfleckenkrankheit (German)
        • Lecanosticta-Nadelbräune (German)
        • Lecanosticta dos anéis do pinheiro (Portuguese)
        • Rjavenje borovih iglic (Slovenian)
      • The susceptible hosts are 44 species of pines, Cedrus libani, C. atlantica and Picea glauca. However, the susceptibility varies a lot among provenances and/or environmental conditions (EPPO, 2024; Tubby et al., 2023). The occurrence of pine hybrids complicates the approach to the list of host species, therefore van der Nest et al. (2019) mentioned 53 different species and hybrids of pine which can host L. acicola.

      • Disease symptoms vary depending on the host tree, with more severe symptoms occurring in the lower parts of the crown and then progressing upwards in the trees (Sinclair and Lyon, 2005; Skilling and Nicholls, 1974).

        At the beginning of infection, a small yellow, sometimes light grey‐green or reddish brown, irregular circular spot, with defined margins, appears on the needles (Hedgcock, 1929). As the infection matures, the yellow spots soon become brown, resin‐soaked (depending on the host), and framed with yellow edges like a halo (Skilling and Nicholls, 1974). It might happen that the symptoms appear only as chlorosis without bands, for example on P. strobus (Broders and kt., 2015). Dark, subcuticular fruiting structures (acervuli) develop, releasing olivaceous, cylindrical, curved or straight conidia with 0-6 septa, rounded apex and truncate base, often with oil droplets, size ca. 30 x 4 µm (Jurc and Jurc, 2010; Tubby et al., 2023). The needles begin to die from the top towards the base before eventually shedding from the trees (Hedgcock, 1929; Skilling and Nicholls, 1974). Usually, only second and third-year needles are affected, leaving healthy new growth at the branch tips. New growth tips are infected through the inoculum on the old needles the following season. (Skilling and Nicholls, 1974).

        L. acicola symptoms are easily confused with those caused by Dothistroma septosporum and D. pini (Barnes et al., 2004, 2016). Therefore, microscopic, and molecular diagnostics are important for accurate identification.

         

      • The pathogen was firstly found by de Thümen (1878) on long leave pine (P. palustris) in the south-eastern USA. Later it has spread and developed into three lineages. The northern lineage occurs in northern USA, Canada and Europe, the southern lineage is dominant in southern USA and Europe as well, and a third lineage occurs only in Mexico, which is probably the centre of origin of the pathogen (Huang et al., 1995, Janoušek et al., 2016). In the southern USA the pathogen was a cause of timber damages in 1980’s exceeding million cubic metres per hectar (Cordell et al., 1990). Also in other parts of the USA the value of Christmas and amenity trees were significantly affected (Tubby et al. 2023).

        To Europe the pathogen was probably introduced before 1980s and observed in Spain and Croatia (Tubby et al. 2023). Historic data about the spread of L. acicola, however, remain doubtful because of very common misidentification due to its similarity to Dothistroma septosporum. More recent reports of the disease increased significantly after 2008 (van der Nest et al. 2019).

      • So far, the pathogen has been registered in 31 countries. It is mainly distributed in Europe and North America. It is less distributed in South America (Colombia) and Asia (Eastern China, South Korea, and Japan; EPPO, 2024).

      • Long range

        The long-distance transport of L. acicola is mediated by human activities. Trade with seedlings is the most often way of introduction into intact areas (Jankovský et al. 2009, Janoušek et al. 2016, Tubby et al. 2023). Considerable option is an inadvertent transport of infective needles by tourists. L. acicola is considered not to be seed-borne because the pathogen cannot survive on the surface of pine seeds for more than 30–34 days (Jianren and Chuandao, 1988). Therefore, long distance spread is probably not intermediated by seeds.

        Short range

        Warm and humid weather is particularly favorable for the development and natural spread of L. acicola. Conidia and ascospores are released throughout the year at temperatures ranging from –5.5 to 28 °C with a maximum temperature of up to 35 °C (Kais, 1971; Siggers, 1944; Wyka et al., 2018). The exact dispersal distance of conidia is not known, but similarities with Dothistroma suggest that conidia, and more likely rare airborne ascospores, may naturally disperse over 1 km (Mullett et al., 2016; Tubby et al., 2023). Germination does not occur at temperatures below 5 °C, although most strains survive and germinate soon after the temperature rises (Siggers, 1944). High levels of conidial dispersal are influenced by rain, but the distribution of conidia varies depending on the rainfall season in a specific geographic region (van der Nest et al., 2019).

      • Due to the significant impact on growth of trees, their mortality and invasiveness, the pathogen was listed as a quarantine pathogen in many countries, but since 2019 it has been reclassified as “regulated non-quarantine pest” for European union. However, there are still countries, where it remained quarantine, like Morocco, Tunisia, China and Norway (EPPO, 2024).

      • Ecological Impacts

        L. acicola slows down growth of pines or even delimits their existence being the most severe problem in the juvenile phase of a tree. Pines have normally high demand on light, therefore they cannot survive in understory of a mixed forest in case they are suppressed by infection of the brown spot needle blight. Pine forests and their habitat play often an important ecological role due to high tolerance of pines to drought and nutrient content in soil, ability to survive in wetlands or naturally afforest or regenerate at clearings as a pioneer. Probably the most critical ecological role it plays in mountains, close to the tree-line, where it exhibits its extreme tolerance to a harsh environment. Records of L. acicola from past 15 years come often from these specific sites, where the role of pine is crucial, like for example peat bogs (Jankovský et al. 2009, van der Nest et al. 2019) and high altitudes of Alps (La Porta and Capretti 2000).

        Indirect, but strong ecological impact has been noted in the USA where one of the earliest methods used against L. acicola on the fire-tolerant P. palustris were large controlled burns (Hedgecock, 1929).

          

        Economic Impacts

        Probably the most severe economic impact of L. acicola was calculated in the USA. The timber losses on P. palustris and other infected species in 1980s exceeded 453,000 cubic meters per acre (Cordell et al. 1990). But the losses were reported not only on timber. L. acicola discoloring needles strongly affects the appearance of Christmas trees. From 1960s to 1980s millions of Christmas trees rendered unmarketable in the north-central USA (Phelps et al., 1978). The economic impact on amenity trees in municipal greens is obvious, as well as costs for eradication of the pathogen in tree nurseries.

      • Detection

        Apart of detection based on visible symptoms, fruiting structures and spores, L. acicola can be identified via isolation to pure culture. It can be isolated on Malt Extract Agar from symptomatic needles following surface sterilization. Firstly, a white aerial mycelium appears which turns greenish olive to dark olive, forming stromatic and erumpent colonies producing an olive-green conidial slime. At 20°C in daylight, the mycelium grows 2.5–3 mm a week. Colonies produce a yellow diffusate (EPPO, 2015).

        L. acicola can be detected by methods of molecular biology. Probably the most used protocol applies real-time quantitative PCR with hydrolysis probes and detects simultaneously Dothistroma septosporum, D. pini and L. acicola. The amplified target gene of L. acicola is a single-copy gene Translation Elongation Factor I alpha (Ioos et al. 2010). This assay has been developed to detect the pathogen directly from the needles. Conventional PCR test (Ioos et al. 2010) with lower sensitivity can be used as well and it is sufficient for DNA extracted from a pure culture.

        Another possibility of a sensitive molecular in planta detection and identification of L. acicola is an assay developed primarily for outdoor use, without using an expensive laboratory equipment. It is based on a Loop-mediated Isothermal Amplification (LAMP) and it was designed and validated by Aglietti et al. (2021).

        Aerobiological monitoring of L. acicola inoculum must be based on the fact that conidia (majority of L. acicola propagules) are mostly transported via droplets of water. Therefore, the distance they are able to travel is rather short and higher concentrations can be expected only bellow infected branches. However, Wyka et al. (2018) observed conidia during some samplings even 60.6 m far from the source. These authors were sampling the conidia with passive spore traps made of microscopic slides covered by petroleum jelly and evaluated the samples microscopically.  

        Preventive measures and suppression measures

        The most effective measures to avoid infection with L. acicola are to use healthy seedlings (Cordell et al., 1990; Skilling and Nicholls, 1974) and to plant in areas away from previously infected plantations that serve as a reservoir of infection (Tainter and Baker, 1996). Thinning is recommended as a preventive measure against L. acicola in natural pine stands (McIntire et al., 2018). Pruning is not recommended during rainy or wet periods due to the increased risk of infection (Skilling and Nicholls, 1974). When performing pruning, it is necessary to disinfect and clean all tools after each use (Kais, 1978).

        Winter burning every 3 years can be used to protect P. palustris from L. acicola infection. For other Pinus spp., controlled burning depends on tolerance to fire damage (Siggers, 1932). When the disease is detected, especially in regions and countries where L. acicola is a quarantine organism, it is suggested to completely eradicate the diseased trees or stands (Pehl and Cech, 2008).

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