Potato Research

, Volume 55, Issue 3, pp 249–268

In Search of Better Management of Potato Common Scab

Authors

  • Merete W. Dees
    • Plant Health and Plant Protection DivisionBioforsk, Norwegian Institute for Agricultural and Environmental Research
    • Genetic Improvement of Fruit and Vegetables LaboratoryUS Department of Agriculture Agricultural Research Services
Article

DOI: 10.1007/s11540-012-9206-9

Cite this article as:
Dees, M.W. & Wanner, L.A. Potato Res. (2012) 55: 249. doi:10.1007/s11540-012-9206-9

Abstract

Common scab (CS) is an important disease and quality problem in potato crops worldwide. CS degrades the appearance of the potato tubers, thereby diminishing market value. Knowledge of CS has expanded considerably over recent years, enabling improved detection of the causal pathogens and increased understanding of mechanisms of pathogenicity, and providing potential methods of modulating pathogen response for disease resistance. However, effective control of this disease remains elusive, and will require increased understanding of both the host and the pathogen. Traditional control strategies such as irrigation and reduced soil pH are not sufficient and often fail. Optimizing environmental conditions for reduction of CS can also lead to favorable conditions for other diseases. The most desirable control method would be disease-resistant potato cultivars. However, no currently available commercial potato cultivar has been shown to be completely resistant to CS. In this review, we provide an overview of potato CS caused by plant pathogenic Streptomyces species, recent research on mechanisms and management of the disease, and knowledge gaps that limit successful control of this ubiquitous and troublesome disease.

Keywords

Gram-positive plant pathogenPathogenicity factorsStreptomyces sppThaxtomin

The Disease and the Causal Agent

Common scab, caused by filamentous Gram-positive bacteria in the genus Streptomyces, is an important disease of potatoes (Solanum tuberosum L.) worldwide. The disease mainly affects the quality of potato by producing superficial, pitted, or raised lesions on the tuber surface. Common scab (CS) has been rated among the top five diseases by potato seed producers in the USA (Slack 1991). Economic losses from CS were estimated at between 15.3 and 17.3 million Canadian dollars in 2002 (Hill and Lazarovits 2005), and costs associated with CS in Tasmania, Australia have been estimated at $3.66 million Australian dollars per acre, about 4% of the industry value (Wilson 2004). Yield may also be affected by delayed emergence and increased amounts of small tubers (Hiltunen et al. 2005).

Streptomyces spp. causing CS are soil-bourne, but may also be transmitted by seed tubers (Wilson et al. 1999; Wang and Lazarovits 2005).

Streptomyces is a soil-inhabiting, saprophytic genus well-known for production of antibiotics (Chater 2006; Chater et al. 2010). Only a few of the several hundred described species are known to be pathogenic on plants. Streptomyces scabies (Thaxter) was the first described species causing CS on potatoes (Lambert and Loria 1989b; Waksman and Henrici 1948) and is found in many potato-growing areas worldwide. It is the dominant CS-causing species in the USA, although it seems to be infrequent in Europe (Bouchek-Mechiche et al. 2000a; Flores-González et al. 2008; Wanner 2009). More recently, Streptomyces turgidiscabies has been found to cause CS on potato, first in Japan (Miyajima et al. 1998) and Finland (Kreuze et al. 1999), and later throughout the world including China, Korea, North America, Norway, Sweden, and the UK (Dees et al. 2012; Kim et al. 1999; Lehtonen et al. 2004; Thwaites et al. 2010; Wanner 2009; Zhao et al. 2008). Streptomyces europaeiscabiei was first described in France in 2000 and is frequently found in Europe, Korea, and North America (Bouchek-Mechiche et al. 2000a; Dees et al. 2012; Flores-González et al. 2008; Song et al. 2004; Wanner 2009). Streptomyces acidiscabies was first described from low pH soils in the USA (Lambert and Loria 1989a) and was later found in Canada, China, Japan, Korea, and the UK (Song et al. 2004; St-Onge et al. 2008; Thwaites et al. 2010; Tóth et al. 2001; Zhao et al. 2010). Streptomyces stelliscabiei has been reported from France and the USA (Bouchek-Mechiche et al. 2000a; Wanner 2006). Streptomyces luridiscabiei, Streptomyces puniciscabiei, and Streptomyces niveiscabiei were identified from Korea (Park et al. 2003a). More recently, the groups Streptomyces sp. IdahoX and S. sp. DS3024 have been identified from North America (Hao et al. 2009; Wanner 2007b). Streptomyces ipomoeae is the causal agent of soil rot of sweet potato (Clark et al. 1998; Loria et al. 1997). An overview of Streptomyces species found to be pathogenic on potato can be found in Table 1 and in Wanner (2009).
Table 1

An overview of Streptomyces species found to be pathogenic on potato

Species

Diseasea

Reported from

Reference

S. scabies

CS

Finland, Japan, Korea, North America, South Africa

Bukhalid et al. 2002; Lambert and Loria 1989b; Lindholm et al. 1997; Park et al. 2003b; St-Onge et al. 2008; Wanner 2009

S. europaeiscabiei

CS, NS

France, Korea, North America, Norway, Western Europe

Bouchek-Mechiche et al. 2000a; Dees et al. 2012; Flores-González et al. 2008; Song et al. 2004; Wanner 2009

S. turgidiscabies

CS

China, Finland, Japan Korea, North America, Norway, Sweden, UK

Dees et al. 2012; Kim et al. 1999; Kreuze et al. 1999; Lehtonen et al. 2004; Miyajima et al. 1998; Thwaites et al. 2010; Wanner 2009; Zhao et al. 2008

S. acidiscabies

AS

China, Japan, Korea, North America, UK

Lambert and Loria 1989a; Song et al. 2004; St-Onge et al. 2008; Thwaites et al. 2010; Tóth et al. 2001; Zhao et al. 2010

S. stelliscabiei

CS

France, North America

Bouchek-Mechiche et al. 2000a; Wanner 2006

S. reticuliscabiei

NS

France

Bouchek-Mechiche et al. 2000a; Bouchek-Mechiche et al. 2000b; Pasco et al. 2005

S. luridiscabiei

CS

Korea

Park et al. 2003a

S. puniciscabiei

CS

Korea

Park et al. 2003a

S. niveiscabiei

CS

Korea

Park et al. 2003a

S. sp. IdahoX

CS

North America

Wanner 2007b

S. sp. DS3024

CS

North America

Hao et al. 2009

S. ipomoeae

Soil rot on sweet potato

North America

Clark et al. 1998; Loria et al. 1997

aCS common scab, NS netted scab, AS acid scab

Most plant pathogenic species are closely related members of the diastatochromogenes clade, with the exceptions of S. acidiscabies/Streptomyces niveascabiei, S. turgidiscabies, Streptomyces reticuliscabiei, and Streptomyces puniscabiei (Labeda 2010; Wanner 2009). All of the known disease-causing Streptomyces species also have non-pathogenic members.

In Europe, two potato scab diseases caused by plant pathogenic Streptomyces species have been reported (Bouchek-Mechiche et al. 2000b; Pasco et al. 2005). CS is caused primarily by S. scabies, S. europaeiscabiei, S. stelliscabiei, and S. turgidiscabies (Bouchek-Mechiche et al. 2000a; Flores-González et al. 2008; Kreuze et al. 1999). Netted scab is caused by S. reticuliscabiei and sometimes S. europaeiscabiei (Bouchek-Mechiche et al. 2000a; Bouchek-Mechiche et al. 2000b; Pasco et al. 2005). Some strains of S. europaeiscabiei can cause either CS or netted scab depending on soil temperature (Bouchek-Mechiche et al. 2000b). S. reticuliscabiei and S. turgidiscabies are closely related and may be a one genomospecies, with two pathogenic groups causing separate diseases (Bouchek-Mechiche et al. 2006). Recent phylogenetic analysis using multilocus sequence typing showed that S. reticuliscabiei and S. turgidiscabies are most accurately described as separate species (Labeda 2010).

Outside of the netted scab—common scab situation described above, there is no evidence that the different pathogenic Streptomyces species differentially affect disease. However, individual isolates within a pathogenic species vary in their aggressiveness (Lindholm et al. 1997; Wanner 2004, 2006; Wanner and Haynes 2009). Although we do not know the physiological or genetic bases for differences in aggressiveness, specific plant genotype–pathogen isolate interactions have been described (Wanner and Haynes 2009).

Host Range

Streptomyces species causing CS disease are not tissue- or host-specific (Loria et al. 2006). The bacteria are able to infect seedlings of a range of monocot and dicot plants under controlled conditions (Leiner et al. 1996). Seedling infection differs from infection of underground stems/stolons in that roots are also affected (Bignell et al. 2010). Under field conditions, the CS host range for several Streptomyces species includes a number of tap root crops such as radish, beet, carrot, and parsnip in addition to potato (Goyer and Beaulieu 1997).

Symptoms

Symptoms of CS vary from superficial to deep-pitted or raised lesions, and all symptoms can be found in tubers from the same plant. Lesions are usually corky and brown/dark coloured; they may be discrete, or may coalesce to cover large patches of the tuber surface. Netted scab symptoms have been described as superficial, brown corky lesions on the tuber periderm (Bång 1979; Bång 1995; Scholte and Labruyère 1985). Incidence and severity of CS vary from location to location and from year to year in the same region. Symptom development depends on the susceptibility of the potato cultivar, and various factors including environmental conditions, pathogen virulence and pathogen inoculum density play a role (Bukhalid et al. 2002; Keinath and Loria 1991; Lambert and Loria 1989b; Lazarovits et al. 2007; Ryan and Kinkel 1997).

The plant side of the interaction between pathogenic Streptomyces and potato is not well understood. Although phytopathogenic streptomycetes have a broad host range (Goyer and Beaulieu 1997), not all tissues and developmental stages of potato (and presumably other host plants) are similarly susceptible to CS. Plant pathogenic Streptomyces cause symptoms on underground plant parts including stems, stolons, and developing tubers, but not roots. Above-ground parts of Streptomyces-infected plants remain healthy, unless the scabby portion of the underground stem restricts water and nutrient conduction between roots and shoots (Fig. 1; Wanner, personal communication).
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Fig. 1

Underground stem damage to Green Mountain, a potato cultivar susceptible to CS caused by Streptomyces spp. a Foliar symptoms in susceptible cultivar planted in sterile soil inoculated with a single S. scabies isolate (OH01-6a). If noticed in the field, plants with these symptoms could be mistaken for virus-infected material and removed, or would die early and not be noticed. b Appearance of underground stems of susceptible plants, not inoculated (left) or grown in S. scabies-inoculated sterile soil (right). c Closer view of underground stem damage in cv. Green Mountain grown in S. scabies-inoculated sterile soil. d Stem and tuber damage in S. scabies-inoculated cv. Green Mountain does not include roots, which remain healthy unless the underground stem is completely severed

Plant pathogenic Streptomyces affect expanding tissue during tuber development. The window of vulnerability to infection by pathogenic Streptomyces strains has not been conclusively established, although young tubers, approximately 0–6 weeks after tuber initiation, are reported to be most vulnerable to pathogen attack (Adams 1975; Khatri et al. 2010, 2011). Anatomical and physiological changes occur during tuber development, including increases in phellem thickness (numbers of layers of cells and suberisation (Khatri et al. 2011)) although CS lesions may occur around lenticels, it has been demonstrated that lenticels and wounds are not required as a port of entry for Streptomyces (Hooker and Page 1960). Lesions stop expanding once the skin is mature (Loria et al. 2006) and the disease does not develop further on tubers in storage.

Other biochemical mechanisms have also been postulated to play a role in CS severity. A study by Goto (1981) indicated that the content of reducing sugar (glucose and fructose) in tuber peel is positively correlated with CS severity, and differential glycosylation of Streptomyces-produced thaxtomin, partially inactivating the toxin, has been proposed as a mechanism of resistance or susceptibility among cultivars (Acuña et al. 2001).

Virulence Mechanisms

Plant pathogenicity in Streptomyces is based on production of the toxin thaxtomin, which is the only known pathogenicity determinant for CS (Bignell et al. 2010; Healy et al. 2000; King et al. 1989). Thaxtomins are nitrated cyclic dipeptides, and are essential for induction of the characteristic symptoms of CS on potato tubers (King et al. 1991). Purified thaxtomin A, the main toxin, produces necrotic lesions very similar to some CS lesions on immature potato tubers (Lawrence et al. 1990), and deletion of thaxtomin biosynthetic genes results in loss of pathogenicity on potato (Healy et al. 2000). Differing ratios of thaxtomins could explain some of the variation in CS symptoms (Hiltunen et al. 2006). Thaxtomin A has been shown to be synthesized by S. scabies, S. turgidiscabies, and S. acidiscabies (Healy et al. 2000; King et al. 1989). No example of a pathogenic Streptomyces strain lacking genes for biosynthesis of thaxtomin has been definitively identified (Wanner 2009). Thaxtomin has an impact on cellulose biosynthesis (Bischoff et al. 2009; Scheible et al. 2003), and may aid lesion formation on expanding plant tissue by inhibiting primary cell wall deposition.

All pathogenic strains appear to harbour a very similar thaxtomin biosynthesis gene cluster. Genes conferring pathogenicity are found in a very large PAI (Kers et al. 2005) in S. turgidiscabies. TxtAB genes encoding thaxtomin synthase are found together with other genes required for production of thaxtomin, including the txtC gene encoding a P450 monooxygenase, a nitric oxide synthase (nos/txtD), and a second P450 monooxygenase gene (txtE). An AraC/XylS-type regulatory gene within the cluster, txtR, controls transcription of the cluster (Joshi et al. 2007b).

No other factor has yet been proven to be a pathogenicity determinant in S. scabies or related species, but several genes, located in the 674 kB S. turgidiscabies PAI and in multiple “pathogenicity islets” in S. scabies, have been implicated as encoding possible pathogenicity factors (Huguet-Tapia et al. 2011; Kers et al. 2005). The virulence-related genes nec1 and tomA are present in many common scab-inducing Streptomyces strains, but not in all, and they are not required for pathogenicity (Seipke and Loria 2008; Wanner 2009). Nec1 encodes a protein inducing necrosis in plant tissue (Bukhalid and Loria 1997). It has been shown to play a role in virulence in seedlings of several species (Joshi et al. 2007a), though not yet on potato tubers. TomA encodes a homolog of family 10 glycosylhydrolases found in Fusarium oxysporum f. sp. lycopersici and Clavibacter michiganensis subsp. michiganensis (Kaup et al. 2005; Seipke and Loria 2008). The over-expressed protein product had no effect on pathogenicity when measured using a potato tuber slice assay (Seipke and Loria 2008).

Other genes in the S. scabies genome or/and the S. turgidiscabies PAI sequence that could play a role in pathogenicity/aggressiveness include: (a) the CFA-like gene cluster producing coronafacic acid, which is similar to a gene cluster found in gram-negative plant pathogens, and forms part of a toxin; (b) cutinase; (c) two S. scabies genes (CS76661 and CS90061) that encode secreted microbial expansin-like proteins; (d) genes homologous to iaaH (indole-3-acetimide hydrolase) and iaaM (tryptophan-2-monooxygenase) for production of the plant hormone IAA; and (e) a microbial version of the ethylene-forming enzyme (Bignell et al. 2010). Another interesting operon present in the PAI of S. turgidiscabies (but not S. scabies) is the fas operon, which produces the phytohormone cytokinin (Huguet-Tapia et al. 2011; Joshi and Loria 2007). Genes with roles in morphological differentiation, development of aerial mycelia, and sporulation are also candidates for roles in pathogenicity, as expression of these genes is required for the initiation of synthesis of antibiotics and other secondary products in a number of Streptomyces species (Flardh and Buttner 2009). Despite the locations of these intriguing genes in PAIs or islets, so far none of these has been shown to have a role in potato CS lesion formation and enlargement, though coronafacic acid reduces virulence in tobacco seedlings (Bignell et al. 2010), and auxins have been implicated as inhibitors of thaxtomin A toxicity (Tegg et al. 2008) or production (Legault et al. 2011).

Horizontal gene transfer of PAIs from pathogenic to saprophytic strains of Streptomyces is the basis for emergence of new pathogenic species (Bukhalid et al. 2002; Healy et al. 1999; Kers et al. 2005). Horizontal transfer of plasmids, bacteriophages, transposons, integrative conjugative elements (ICEs), and genomic islands are important mechanisms of bacterial evolution (Juhas et al. 2009), and there is considerable evidence that these transfer mechanisms operate in Streptomyces (Combes et al. 2002; Goyer 2005; Huguet-Tapia et al. 2011; Kers et al. 2005; Kim et al. 2008; Zhou et al. 2004). Only certain Streptomyces species harbour a PAI, or portions of a PAI; this could be due to stable transfer only into certain species [e.g., the large and complex PAI of S. turgidiscabies (an ICE) has integrated into a specific chromosomal location (Huguet-Tapia et al. 2011)], or to lack of stable maintenance in most Streptomyces species. Pathogenicity-associated genes have been found in non-pathogenic Streptomyces (Wanner 2009), and these gene clusters are probably widely found in soil-inhabiting Streptomyces. Though non-pathogens are found together with pathogenic species in CS lesions, few have acquired a PAI, suggesting the existence of natural barriers to exchange of PAI(s).

Plant and Microbial Factors Affecting Thaxtomin Production

During the last decade, factors responsible for induction of thaxtomin production have been sought. Three molecules of plant origin, cellobiose, cellotriose, and suberin, as well as complex carbohydrates that could break down into simpler oligosaccharides, have been implicated in stimulating or inducing thaxtomin production (Johnson et al. 2007; Lauzier et al. 2008; Lerat et al. 2010; Wach et al. 2007). Cellobiose combined with suberin was most effective (Lerat et al. 2010), though the stimulatory effects seem relatively weak. Earlier studies indicated that amino acids, particularly tryptophan which is a substrate for thaxtomin biosynthesis, also inhibited thaxtomin production at higher concentrations (Lauzier et al. 2002). Tryptophan is a substrate for both thaxtomin and auxin biosynthesis. Auxins have been implicated as inhibitors of thaxtomin production (Tegg et al. 2008), though only when added at very high levels, which are not biologically relevant (Tegg et al. 2008; 2012). In the most recent chapter of this story, tryptophan concentration is a switch between thaxtomin and auxin production (Legault et al. 2011). Genes for biosynthesis of thaxtomin, but not auxin, were inhibited by tryptophan (see Fig. 3 for a diagrammatic overview of these relationships). Auxin can be produced by both plants and bacteria, and it is not clear whether the source of auxin or tryptophan is the plant, the bacterium, or possibly both.

Control of Common Scab

Although CS on potato was first described more than 100 years ago (Loria et al. 1997), scientists still have little understanding of the factors that contribute to occurrence and severity of the disease. On the pathogen side, lack of understanding of the types and consequences of genetic diversity and the genetic basis for differences in aggressiveness of isolates hinders development of control strategies. Information on pathogen variability is also essential in selecting CS-resistant plant germplasm. On the plant side, the physiological or genetic basis for differences in CS severity seen in different potato cultivars is poorly understood, and no source of true resistance to CS has been identified (Agrios 2005; Hosaka et al. 2000; Powelson et al. 1993). Physiological differences such as skin set properties and thaxtomin sensitivity may partly explain differential cultivar susceptibility. More research is needed on the mechanisms of resistance/susceptibility to CS.

Environmental factors, such as pH, soil moisture, and soil microbial flora, in combination with potato cultivar and virulence of the pathogen, make management of CS a difficult task. Phenotyping CS in the field is complicated by the variability of CS disease pressure and severity seen in different years (for a few examples, see Peters et al. 2004; Wilson et al. 2001; Haynes et al. 2010). Survival of plant pathogenic Streptomyces as saprophytes on plant debris in soil further complicates effective disease control. Several studies indicate that control measures may be soil-specific (Lazarovits et al. 2007; Sturz et al. 2004), though it is unclear whether this is due to physical soil properties, or soil microbial flora (Sturz et al. 2005; Sturz et al. 2004; Wiggins and Kinkel 2005). The existence of CS-suppressive soils suggests that microbial flora is important (Neeno-Eckwall et al. 2001), and cultivar-specific assemblages of microflora have recently been described in potato (Manter et al. 2010; Weinert et al. 2011).

Inconsistent and/or inadequate results have been obtained with nearly all methods of CS control, including reducing soil pH, keeping plants well-irrigated from the time of tuber initiation through tuber enlargement, crop rotation, and cover crops (Davis et al. 1976; Lazarovits 2010; Peters et al. 2004; Waterer 2002). A summary of different methods used to control CS is found in Table 2.
Table 2

Control practices for common scab and their effectiveness

Control practice

Effectiveness

Irrigation during tuber formation

Often fails

Lowering soil pH to <5.2

Limits crop rotation, can fail

Crop rotation

Inconsistent, can fail. Streptomyces spp. can survive as saprophytes, or on other host plants

Biological control

Can work under controlled conditions, but variable in the field. More investigation needed

Disease-free seed tubers

Not sufficient, Streptomyces spp. are soil-bourne

Chemical fumigation

Can work for a season; expensive, environmentally unfriendly

Seed treatments with fungicides

Results erratic

Sulphur fertilizer

Reported to reduce scab severity in some locations

Resistant potato cultivars

Most desirable and reliable method

Irrigation and pH

Irrigation timing and reduction of soil pH are traditional management strategies to suppress CS (Davis et al. 1976; Lambert and Manzer 1991; Lapwood et al. 1970; Loria 2001), but contradictory data exist for both strategies. For example, Lapwood and Wellings showed that irrigation applied early in the season decreased CS on susceptible potato cultivars (Lapwood and Wellings 1973), while Larkin found that irrigation increased CS (Larkin et al. 2011). Netted scab was reported to increase in severity with increased soil moisture (Scholte and Labruyère 1985), and S. turgidiscabies also tolerates higher levels of moisture. Despite disparities in results from year to year (Wilson et al. 2001; Larkin et al. 2011) irrigation is considered to be a useful management tool, especially in combination with other management methods (Loria 2001).

CS is typically considered to be inhibited by lower soil pH (Lacey and Wilson 2001). However, emerging species of Streptomyces such as S. acidiscabies and S. turgidiscabies tolerate lower pH than S. scabies (Lambert and Loria 1989a; Lindholm et al. 1997). Interestingly, a soil pH above 8.5 has been shown to inhibit CS (Waterer 2002).

Soil Fumigation

Soil fumigation and planting resistant potato cultivars remain the primary means for controlling soil-bourne plant diseases and pests, including CS. Fumigation is increasingly constrained by increased costs, urbanization, and its negative environmental impacts. Soil fumigants are expensive and environmentally unfriendly, and are increasingly regulated or are being removed from the market. The primary soil fumigants used in potato culture are pentachloronitrobenzene, also known as Blocker® (Amvac), has been tested with some success (Davis et al. 1976; Hutchinson 2005). However, studies show that use at higher concentrations (20 lbs/A) can reduce tuber size or yield (Wharton et al. 2011). Pic-plus (chloropicrin plus a solvent) has shown some efficacy against CS in trials in Michigan, Ontario, and Florida (Hutchinson 2005; Wharton et al. 2011). Requirement of minimum soil temperatures above 45 °F (7 °C) for application and 30-day post-application planting restrictions limit chloropicrin use in most northerly areas (Wharton et al. 2011). Chloropicrin is also expensive, and the effects seem to last for only a single season (Wharton et al. 2011).

Foliar Sprays

Foliar sprays of auxins and related molecules have been tried for controlling CS (McIntosh et al. 1981; McIntosh et al. 1988; Tegg et al. 2008). Although these can be effective in reducing CS, they affect plant growth, including tuber size and weight of tubers.

Soil Chemistry

Potatoes are grown in soils of many types, and CS occurs in all of them. The conclusion of different studies of soil chemistry and added fertilizers is that the relationship between CS severity and soil chemical components is complex and cannot easily be generalized (Lacey and Wilson 2001; Lazarovits et al. 2007). Sulphur fertilizers alter soil pH and affect soil microbial communities, and have been reported to provide some mitigation against CS (Davis et al. 1974; Sturz et al. 2004; Pavlista 2005).

Crop Rotation/Cover Crops, Green Manures, and Organic Soil Amendments

Crop rotation has been used as a strategy to reduce Streptomyces inoculum in the field (Griffin et al. 2009; Larkin et al. 2010; Wiggins and Kinkel 2005). However, plant pathogenic Streptomyces spp. can survive in the soil for many years, possibly due to their ability to live saprophytically. Recent studies by Larkin et al. (2010) show that canola and rapeseed rotations consistently reduce the severity of CS. Addition of winter rye further reduced CS. The combined effect of canola or rapeseed rotation and winter rye cover crop reduced CS severity by 20–33% compared to continuous potato with no cover crop. A more recent study by Larkin et al. (2011) showed that a disease-suppressive cropping system reduced CS severity by 25–40% over 3 years. The disease-suppressive system made use of multiple potential strategies for suppressing soil-bourne diseases, including the use of disease-suppressive rotation crops, a longer rotation period, crop diversity, green manures, and fall cover crops. A soil-conserving system (3-year, barley/timothy–timothy–potato) and the standard rotation system (2-year, barley/red clover–potato) reduced CS in some years. A soil-improving system (3-year, barley/timothy–timothy–potato; yearly additions of compost) did not reduce CS after 3 years. Use of crop residues of brassicas as biofumigants is becoming widespread (Matthiessen and Kirkegaard 2006; Larkin and Griffin 2007).

A 2005 study showed that potatoes planted in soil with corn or alfalfa grown the previous year had lower levels of CS than potatoes grown in a continuous potato cropping system (Wiggins and Kinkel 2005). Green manure treatment may contribute to active management of the pathogen inhibitory activity of the streptomycete community to achieve plant disease control. However, Peters et al. (2004) found that at low disease pressure, tillage or rotation did not influence CS severity in a 3-year crop rotation system. The relationship between tillage, rotation, cover crop and CS seems to be complex.

Numerous organic soil amendments have been tried in efforts to decrease severity of CS and other soil-bourne diseases, to induce plant defence responses and to improve soil quality (Lazarovits 2010). Many soil amendments that have been investigated for mitigation of soil-bourne diseases are industrial or agricultural waste products, such as crab shells, meat and bone meal, feather meal, poultry and swine manure, and soy meal. Some of these have significantly reduced disease, including CS, but the level of disease control is product- and soil-specific (Lazarovits 2010; Lazarovits et al. 1999; Soltani et al. 2002). The mechanism(s) of this control have been described in a few cases. High nitrogen amendments are degraded by soil microorganisms to generate toxic levels of ammonia and/or nitrous acid. Toxic components of manure were identified as volatile fatty acids (vinegar). Although many of these amendments reduced pathogen populations, total soil microbial numbers increased by 10- to 1,000-fold after applications. The practical use of many agricultural waste products is limited by human health and safety issues, concerns about run-off of this material into waterways, and by their limited availability.

Biological Control

Biological control of CS offers an attractive alternative to classical control strategies. As producers of antibiotics and extracellular enzymes, non-pathogenic Streptomyces species have potential as biological control agents against CS (Doumbou et al. 2001) as well as other soil-bourne diseases (Sabaratnam and Traquair 2002; Xiao et al. 2002). Antagonistic streptomycetes naturally present in potato fields can suppress CS (Lorang et al. 1995; McQueen et al. 1985). Use of non-pathogenic strains of Streptomyces in inhibition of pathogenic Streptomyces has been demonstrated (Liu et al. 1995). Recent research indicates that Streptomyces species closely related to CS-causing species are abundant on the skins of CS-resistant cultivars, and are more frequent in less-severe superficial CS lesions than in pitted lesions (Wanner 2007a). Some non-pathogenic Streptomyces species have been investigated for their potential to control CS, with mixed results (Hiltunen et al. 2009; Wanner, personal communication). Most studies to date have focused on antagonists to S. scabies (Beausejour et al. 2003; Lorang et al. 1995) with only one report of antagonists against S. turgidiscabies (Hiltunen et al. 2009). This may not be important in the field, since thaxtomin production seems to be the primary mechanism of pathogenicity.

The bacterium Pseudomonas has recently been associated with control of CS (St-Onge et al. 2011). This Pseudomonas produces phenazine-1-carboxylic acid, well-known for its suppressive and antagonistic effects on fungi, but not previously known to inhibit actinomycetes. This Pseudomonas strain inhibited growth of S. scabies in vitro, repressed txtA and txtC expression in S. scabies, and protected against potato CS in greenhouse assays (St-Onge et al. 2011). Control of CS using Bacillus sp. sunhua has also been demonstrated. In a pot assay, culture broth from Bacillus sp. sunhua had a suppressive effect on CS, decreasing the infection rate from 75% to 35% (Han et al. 2005).

Isolates from nine fungal species, mostly ascomycetes, have also been reported to show antagonistic activity against potato CS pathogens (Tagawa et al. 2010). The antagonistic activity of these fungi was increased under low pH conditions, suggesting that fungal isolates might be effectively combined with traditional methods such as soil acidification to enhance biocontrol.

The use of bacteriophages to reduce infection on tubers by S. scabies has been investigated, but more work needs to be done to efficiently utilize phages as biocontrol agents in the field (Goyer 2005; McKenna et al. 2001).

CS and Plant Defence

CS resistance does not seem to follow a typical plant disease resistance model, with a plant resistance gene responding to a pathogen and setting in motion a defence response. There is no evidence for a plant defence response to Streptomyces or to thaxtomin in potato, although calcium influxes and changes in extracellular pH, both classic early hallmarks of defence responses, are induced by thaxtomin in tissue cultures of Arabidopsis and tobacco (Errakhi et al. 2008; Tegg et al. 2005), and abundant defence and abiotic proteins are expressed in healthy potato skin/periderm tissue (Barel and Ginzberg 2008; Soler et al. 2011). An extensive cDNA library from CS tubers did not contain typical defence-response genes (Flinn et al. 2005). Further studies of gene/protein expression patterns during skin maturation in different potato cultivars would be of great interest, especially if correlated with CS susceptibility or resistance.

Tolerant Cultivars and Genetics of CS Resistance

The most desirable method of controlling CS is disease-resistant potato cultivars. Unfortunately, at present there are no completely resistant cultivars and commercially available cultivars show varying degrees of resistance or tolerance to CS (Fig. 2). The mechanism and genetics of tolerance to CS remain to be understood.
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Fig. 2

The continuous distribution of median CS severity values in 61 cultivars and diploid species shows that the genetic basis of CS resistance (or tolerance) is likely to be complex. A few cultivars are quite resistant (the first 12 from the left), with most cultivars showing inadequate resistance. These data come from a single experiment with a S. scabies isolate (ME01-11h) at 1010 colony-forming units per pot (three replicates per treatment). Disease severity indices (depicted on the Y-axis) account for both the type of lesions and the area covered by lesions, and were derived by multiplying the lesion type score by the percentage of tuber surface covered with lesions. The CS lesion type was recorded on a 0 to 5 scale, with 0 = no CS, 1 = superficial discrete lesions, 2 = superficial coalescent lesions, 3 = raised discrete lesions, 4 = raised coalescent lesions, and 5 = any type of pitted lesion. In this box plot, the cultivars are arranged by increasing median severity index (red dashes in the boxes). Also indicated are mean severity scores (called Av SxA on the graph and presented as yellow circles with red outline), the first plus third interquartile range (boxes), and the maximum and minimum severity score, which are usually 500 and 0, that is, there are nearly always outliers at the extremes. All tubers larger than 0.5 cm in diameter were scored, so tuber numbers were not equal

Although several genetic studies have been published concluding that one or a few genes are responsible for CS resistance in haploid or diploid potato populations (Cipar and Lawrence 1972; Krantz and Eide 1941; Murphy et al. 1995), this does not seem likely to be the case in (tetraploid) potato cultivars (Dionne and Lawrence 1961; Goth et al. 1993; Haynes et al. 2010; McKee 1958). As shown in Fig. 2, there is nearly continuous variation in CS symptom severity among a random selection of commercially grown potato cultivars and breeding lines, strongly suggesting that multiple genes are involved. A segregating tetraploid population showed continuous variation in CS resistance, indicating complex genetics (Driscoll et al. 2009). A reproducible way to phenotype potatoes for CS resistance is urgently needed in order to gain an understanding of the underlying genetics. The absence of such an assay is a major obstacle in phenotypic testing for resistance to CS. Even under the best-controlled circumstances, with a known pathogenic Streptomyces strain at a known concentration, and in controlled environmental conditions (greenhouse or growth chambers), a range in symptoms from nearly none to severe CS can be seen on tubers from a single potato plant in a single pot. This is well-illustrated in the box plots in Fig. 2, where every scab index rating between 0 and 500 is found among the outliers from a single pot. This lack of a simple phenotype significantly complicates data analysis, and thus progress toward understanding the genetics behind resistance.

Recently, Wilson and colleagues used somatic cell selection with thaxtomin A as a positive selective agent to isolate variants of potato cv. Russet Burbank with strong to extreme resistance to CS (Wilson et al. 2010). Hiltunen et al. (2011) have also shown that elimination of CS-sensitive progeny from a potato breeding population can be accomplished using thaxtomin A as a selective agent. The promising results from these studies could eliminate years of field trials in resistance screening and elevate the overall levels of CS resistance in potato breeding populations. Additionally, a number of potato breeding programmes now have germplasm that is significantly more resistant to CS than older cultivars (Douches et al. 2001; Haynes et al. 2010; Tarn et al. 2003). Some of this CS resistance has been introduced from wild species, which have potential to provide new genes for CS resistance (Hosaka et al. 2000).

Future Perspectives

A summary of what is known about the mechanism behind the complex interactions between the pathogenic Streptomyces species and the potato plant is presented in Fig. 3. The biosynthetic pathway for the pathogenicity determinant thaxtomin and the gene cluster encoding thaxtomin biosynthesis have been fully elucidated (Bignell et al. 2010), and numerous details of regulation of this gene cluster have been described (Legault et al. 2011; Lerat et al. 2010). Definitive verification of pathogenicity determinants is still missing for CS in developing potatoes, as is information on plant-derived factors involved in the interaction between pathogenic Streptomyces and potato tubers, indicated in the red boxes in Fig. 3. Potato cultivars which exhibit a high degree of tolerance to CS should be given more attention in order to elucidate the mechanism behind resistance, such as tryptophan production or excretion into the rhizosphere. With the advent of the complete sequence of the potato genome, and the development of thousands of SNPs (http://solcap.msu.edu/extension.shtml), interest has increased in phenotyping progeny of crosses with at least one CS-resistant parent, with the expectation that we will soon be able to identify gene regions in the near-neighbourhood of loci important for expression of resistance (or sensitivity) to CS. In addition, deep-sequencing technologies are now being used to study potato microbial communities of endophytes, mycorrhizae, rhizosphere, and soil in order to gain a more complete picture of the effects of microbial communities on plant health and CS disease (Diallo et al. 2011; Manter et al. 2010; Sugiyama et al. 2010).
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Fig. 3

Overview of the current understanding of common scab induced by thaxtomin. Boxes lined with red emphasize what is still not known about the initiation and propagation of CS by Streptomyces species. Dotted lines indicate transfer of molecules presumed but unproven to play roles in pathogenicity

Summary: Knowledge Gaps Limit Efforts to Devise Better Strategies for Control

Recent research has been focused on two areas that may help in controlling CS: (1) developing rational, research-based measures based on understanding the pathogen, its distribution, and under what circumstances it causes disease; and (2) developing reliable disease-resistant cultivars. Factors that have hindered the development of CS-resistant potato cultivars include variable effects of environmental conditions, need for better sources of resistance (within S. tuberosum), genetic variation in pathogen populations, and the variability in CS severity from year to year and location to location. Traditional control measures are insufficient and often fail. No single measure is sufficient for managing CS. Integrated use of the available methods, especially planting cultivars with the best CS resistance for a region, is presently the best option for control.

Acknowledgments

Thanks to the helpful commentary of Dr. Jo Anne Crouch, Dr. Linda Kinkel, and an anonymous reviewer in editing the manuscript. This work was partially supported by USDA-ARS project number 1275-21220-250-0OD, the Research Council of Norway, the Foundation for Research Levy on Agricultural Products, the Agricultural Agreement Research Fund, and Norwegian food industries.

Copyright information

© EAPR (outside the USA) 2012