Streptomyces is a gram positive, aerobic, filamentous, spore-forming bacterium in the Streptomycetaceae family of the Actinobacteria. The filamentous mycelia have few or no cross walls. Spores are formed in spiral chains at the tips of hyphae. Streptomyces is the largest genus in the Actinobacteria and nearly 600 species are recognized.

Scientific description of Common Scab (2020)

Based on Charkowski A., Sharma K., Parker M.L., Secor G.A., Elphinstone J. (2020) Bacterial Diseases of Potato. In: Campos H., Ortiz O. (eds) The Potato Crop. Springer, Cham

The authors of this content are Amy Charkowski, Kalpana Sharma, Monica L. Parker, Gary A. Secor, John Elphinstone
Common Scab of Potato Caused by Streptomyces Species

Taxonomy and Nomenclature

Streptomyces is a gram positive, aerobic, filamentous, spore-forming bacterium in the Streptomycetaceae family of the Actinobacteria. The filamentous mycelia have few or no cross walls. Spores are formed in spiral chains at the tips of hyphae. Streptomyces is the largest genus in the Actinobacteria and nearly 600 species are recognized.

Most Streptomyces are soil-dwelling saprophytes and some species have a beneficial symbiosis with eukaryotes, including plants. At least 12 Streptomyces species cause common scab, netted scab, and/or pitted scab on potato.

The names of several pathogenic Streptomyces species, such as S. scabies, were grammatically incorrect when they were first named and the scientific community has only recently begun using corrected names, such as S. scabiei.

Common scab is usually caused by S. scabiei (Thaxter 1892; Lambert and Loria 1989b), S. acidiscabiei (Lambert and Loria 1989a), or S. turgidiscabiei (Miyajima et al. 1998). Other species that cause scab symptoms on potato include the pitted scab pathogen S. caviscabiei (Goyer et al. 1996), three species first reported in France, including S. europaeiscabiei, S. reticuliscabiei, and S. stelliscabiei (Bouchek-Mechiche et al. 2000), three species first reported in Korea, including S.

luridiscabiei, S. niveiscabiei, and S. puniciscabiei (Park et al. 2003), and one species reported in Japan, S. cheloniumii (Oniki et al. 1986a, b).

The species S. reticuliscabiei is genomically the same as S. turgidiscabiei, but causes netted scab symptoms rather than typical common scab lesions (Bouchek-Mechiche et al. 2000, 2006). S. diastatochromogenes was recently reported as a common scab pathogen of potato, but there is no information available on its relative importance and the species identification was based solely on 16S rDNA sequence (Yang et al. 2017).

A related species, S. ipomeae, causes root rot of sweet potato. Additional Streptomyces species capable of causing common scab have been isolated, but not yet described as species (see Table 1 in Bignell et al. 2014) and additional pathogenic species certainly remain to be discovered.

Nonpathogenic strains exist within the pathogenic species, and none of the nonpathogenic strains appear to encode the phytotoxin thaxtomin (Wanner 2006, 2007, 2009).

Host Range

Potato is the most economically important host of plant pathogenic Streptomyces species. Plant pathogenic species are also able to cause disease on root crops, such as carrot, beet, parsnip, radish, sweet potato, and turnip (Goyer and Beaulieu 1997), and on peanut pods (Kritzman et al. 1996), but the economic impact of Streptomyces on these crops is less important than other diseases that infect these root crops.

Geographical Distribution

Pathogenic Streptomyces are present in soils wherever potato is grown and, as the name denotes, the disease it causes is one of the most common and most important potato diseases worldwide. Multiple species are present in individual fields and tubers (Wanner 2009; Lehtonen et al. 2004; Dees et al. 2013).

Some species have only been reported from limited geographical regions, but no comprehensive global surveys have been done, so the distribution of pathogenic Streptomyces species remains mostly unexplored.

The spread of this pathogen is managed mainly through quality regulations which prohibit planting or shipping of severely affected seed, so there are essentially no limits on the spread of pathogenic Streptomyces through seed potatoes.

Establishment of new Streptomyces strains in field soil is dependent on numerous complex factors, including soil chemistry and resident soil microbes, making establishment of pathogenic Streptomyces strains transported on seed potatoes unpredictable.

Symptoms

Streptomyces can cause necrosis on all underground parts of a potato (image below), including roots, stolons, and stems, and it can reduce growth of roots from seed tubers (Han et al. 2008). This pathogen can also cause necrosis on and kill potato seedlings grown from true potato seed. It does not directly cause foliar symptoms, although plant vigor may be reduced due to root necrosis caused by Streptomyces.

Common scab symptoms on potato (Courtesy: AHDB Potatoes Sutton Bridge Crop Storage Research)

There is a wide variation in tuber symptoms caused by Streptomyces, including pitted scab, erumpent scab, and mild netted scab and symptom type depends, at least in part, on which toxins the infecting strain produces and the potato genotype. The pathogen colonizes tubers as they initiate, often entering the tube through lenticels.

Whitish-grey bacterial mycelia and spores are sometimes visible in pitted scab lesions at harvest. The disease does not progress in storage, although tubers with severe pitted scab lesions will dehydrate and will not sprout the following season.

Epidemiology

Streptomyces has a relatively complex life cycle compared to many bacterial pathogens. It grows vegetatively as filamentous mycelia-like cells. When resources are depleted, the vegetative cells undergo programed cell death, nutrients are transferred to aerial reproductive hyphae, and spores are formed.

These hyphae are sometimes visible without magnification inside scab lesions. Pathogenic Streptomyces grow best in soils with a pH between 5.2 and 8.0, and temperature of 20–22 °C, which are conditions that also favor potato growth.

Streptomyces survives and disperses mainly through cylindrical spores formed at hyphal tips. The spores can disperse in water, on soil-dwelling invertebrates, and on seed tubers. Streptomyces spores can survive in soil for 20 or more years and the spores are heat resistant.

The pathogen spores germinate and enter the plant through natural openings, such as lenticels, or through wounds. Tubers are most susceptible to Streptomyces colonization during the first month of development.

Streptomyces cannot cause lesions on mature tubers and lesion size and severity does not progress during storage, although tubers with severe pit scab may become dehydrated and will not sprout the following season.

Because multiple Streptomyces species are present in field soil and on diseased plants, epidemiological studies now rely on molecular detection of the species present in order to understand the impacts of management methods, soil characteristics, or biocontrol strains. PCR assays capable of distinguishing Streptomyces species are available (Wanner 2009).

PCR assays designed to detect genes encoding thaxtomin are also used in epidemiological studies because detection of thaxtomin DNA is correlated with ability of an isolate to cause common scab (Wanner 2006, 2007, 2009; Flores-González et al. 2008) and with development of common scab symptoms in field soils (Qu et al. 2008).

Soils that suppress common scab exist and ongoing work is aimed at identifying the communities that lead to suppressiveness. Soils that suppress common scab have high Streptomyces populations. These saprophytic streptomycetes produce antibiotics that inhibit pathogenic Streptomyces or that compete with pathogenic Streptomyces for resources, thereby reducing common scab (for a comprehensive review, see Schlatter et al. 2017).

Pathogenicity Determinants and Resistance

Bacteria in this genus have unusually large linear genomes of 10–12 Mb and they produce diverse secondary metabolites. In the plant pathogenic Streptomyces, large pathogenicity islands encompassing several hundred genes encode virulence genes required for production of secondary metabolites, such as toxins, cytokinin, nitric oxide, and secreted proteins (Bignell et al. 2010; Joshi and Loria 2007).

At least two of these pathogenicity islands are mobile (Bukhalid et al. 2002) and one of them can mobilize at least one otherwise nonmobile pathogenicity island (Zhang and Loria 2017). As a result, pathogenicity can be transferred to previously nonpathogenic species (Zhang and Loria 2017).

Phytotoxins are the main Streptomyces pathogenicity determinants and the toxin thaxtomin appears to be required for pathogenicity (for a recent review, see Bignell et al. 2014). Thaxtomins, which are nitrated dipeptides (tryptophan and phenylalanine), are required for the development of common scab symptoms (King et al. 1989, 1991; Kinkel et al. 1998).

Thaxtomin appears to weaken plant cell walls and cause plant cell hypertrophy through inhibition of cellulose synthesis and cell wall acidification (Fry and Loria 2002; Bischoff et al. 2009). This toxin can be used in potato breeding since seedling tolerance to thaxtomin is correlated with tolerance to common scab in the field (Hiltunen et al. 2011).

The other types of toxins produced by pathogenic Streptomyces, including coronatine-like toxins (Fyans et al. 2015), concanamycin (Natsume et al. 2017), borrelidin (Cao et al. 2012), and FD-891 (Natsume et al. 2005), are not necessarily produced by all pathogenic strains and production of these toxins may affect whether an individual strain produces pitted, net, or erumpent common scab symptoms.

For example, concanamycin, a type of toxin produced by S. scabies, but not by some other Streptomyces species, may be required for formation of pitted scab lesions and appears to be synergistic with thaxtomin (Natsume et al. 2017).

Enzymes may also play a role in Streptomyces pathogenicity. Streptomyces lesions typically do not autofluoresce, suggesting that suberin formation is either inhibited or digested. Two genes that encode potential suberinases are present in the S. scabies genome and biochemical evidence supports that suberin is degraded (Beaulieu et al. 2016; Komeil et al. 2013).

Degradation of suberin also appears to increase expression of the numerous cellulases produced by S. scabies (Padilla-Reynaud et al. 2015). Streptomyces toxin production is induced by plant-derived molecules, including the disaccharide cellobiose, a breakdown product of cellulose.

Little is known about the genetic basis of resistance to common scab. Suggested mechanisms include phellum layer thickness (Thangavel et al. 2016), phellum suberization (Thangavel et al. 2016; Khatri et al. 2011), detoxification of thaxtomin (Acuna et al. 2001), or sustained expression of disease defense genes (Merete Wiken Dees et al. 2016).

Differences in ability of potato varieties to support growth of nonpathogenic Streptomyces species may also affect susceptibility to common scab (Wanner 2007).

Significance and Economic Loss

Common scab can cause complete loss, although this is usually associated with mismanagement of the crop, such as adding too much lime to a field, insufficient irrigation, or highly susceptible varieties planted in fields with high disease pressure.

Direct losses occur annually, however, worldwide, and common scab is often listed among the most important potato diseases (for example, Hill and Lazarovits 2005).

Management

  • The best option is disease tolerance or resistance, but currently there are limited options for potato varieties with high tolerance to common scab. Common scab symptom development is affected by soil moisture and chemistry, the soil microbial community, crop rotation, and host genetics in a complex manner that has made predicting common scab severity and managing this disease difficult.

    A comprehensive review of these challenges was published by Dees and Wanner (2012). Recommendations for management of common scab usually include adequate irrigation during tuber formation, and low soil pH (
    Typically, sulfur fertilizers are used to reduce soil pH and this can reduce disease severity (Pavlista 2005). However, these methods sometimes fail to provide adequate management and can lead to other production problems.

    For example, over-irrigation during tuber formation can lead to development of powdery scab and several other potato diseases, and low soil pH limits farmer options for crop rotations and selects for S. acidiscabies.

  • Chemical treatments can work for a season, but are often expensive and damaging to the soil, making this the least sustainable disease management option. Some commonly used effective chemicals include fludioxonil as a seed piece treatment, chloropicrin as a soil fumigant, and pentachloronitrobenzene as an in-furrow treatment (Al-Mughrabi et al. 2016; Powelson and Rowe 2008). Fluazinam may also provide some control of common scab (Santos-Cervantes et al. 2017).

  • Crop rotation choices can also reduce common scab severity (Powelson and Rowe 2008; Larkin and Halloran 2014; Larkin et al. 2011; Larkin and Griffin 2007). These crop rotations tend to include brassica crops as a biofumigant and commonly planted green manures that are allelopathic and that help control multiple soil-borne potato diseases.

    Soil amendments, such as rice bran, chelated iron, or peat can decrease common scab, likely by increasing the population of nonpathogenic streptomycetes (Tomihama et al. 2016; Sarikhani et al. 2017). Some soil amendments, such as manure, which increases soil pH, will increase common scab severity.

  • Biocontrol with nonpathogenic Streptomyces strains also shows promise and the mechanism of biocontrol is likely similar to that seen in suppressive soils, which is thought to be due to both resource completion and antibiotic production (Schlatter et al. 2017). Suppressive soils develop through repeated monoculture of potato, but this practice results in accumulation of other soil-borne pathogens.

    However, repeated inoculations of soils with a single antagonistic Streptomyces strain can result in common scab suppression in as little as 3 years, and suppressive lasted for 2 years beyond the last inoculation (Hiltunen et al. 2017).
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