Dickeya solani
(black leg disease of potato)

Pictures

Picture	Title	Caption	Copyright
Title Field symptoms Caption Dickeya solani on potato (Solanum tuberosum) cv. Red Robin. Image is of field grown naturally infected potatoes from Scotland, UK in July 2009. Copyright Public Domain - ex. SASA ©Crown Copyright	Field symptoms	Dickeya solani on potato (Solanum tuberosum) cv. Red Robin. Image is of field grown naturally infected potatoes from Scotland, UK in July 2009.	Public Domain - ex. SASA ©Crown Copyright
Title Healthy vs. infected Caption Dickeya solani on potato (Solanum tuberosum) cv. Estima. Plant (b) was grown from a seed potato vacuum infiltrated with a suspension of Dickeya solani, resulting in stunting and curling, wilting of leaves. Plant (a) is the healthy control. Copyright Public Domain - ex. SASA ©Crown Copyright	Healthy vs. infected	Dickeya solani on potato (Solanum tuberosum) cv. Estima. Plant (b) was grown from a seed potato vacuum infiltrated with a suspension of Dickeya solani, resulting in stunting and curling, wilting of leaves. Plant (a) is the healthy control.	Public Domain - ex. SASA ©Crown Copyright
Title Symptoms Caption Tuber infection of potato (Solanum tuberosum) cv. Agria caused by Dickeya solani. Image is of an imported ware tuber intercepted in Scotland, UK in July 2009. Copyright Public Domain - ex. SASA ©Crown Copyright	Symptoms	Tuber infection of potato (Solanum tuberosum) cv. Agria caused by Dickeya solani. Image is of an imported ware tuber intercepted in Scotland, UK in July 2009.	Public Domain - ex. SASA ©Crown Copyright
Title Symptoms Caption Tuber infection of potato (Solanum tuberosum) on cv. 'Red Robin' caused by Dickeya solani. Image is of a tuber harvested from a field grown, naturally infected plant in Scotland, UK in 2009. Copyright Public Domain - ex. SASA ©Crown Copyright	Symptoms	Tuber infection of potato (Solanum tuberosum) on cv. 'Red Robin' caused by Dickeya solani. Image is of a tuber harvested from a field grown, naturally infected plant in Scotland, UK in 2009.	Public Domain - ex. SASA ©Crown Copyright
Title Dickeya solani colonies on Crystal Violet Pectate Medium (CVPM) Caption Dickeya solani colonies on Crystal Violet Pectate Medium (CVPM). CVPM is typically used to isolate the bacterium from infected plant material. D. solani produces pitted colonies on CVPM as a result of the actions of pectolytic enzymes. Copyright Public Domain - ex. SASA ©Crown Copyright	Dickeya solani colonies on Crystal Violet Pectate Medium (CVPM)	Dickeya solani colonies on Crystal Violet Pectate Medium (CVPM). CVPM is typically used to isolate the bacterium from infected plant material. D. solani produces pitted colonies on CVPM as a result of the actions of pectolytic enzymes.	Public Domain - ex. SASA ©Crown Copyright

Identity

Preferred Scientific Name

• Dickeya solani van der Wolf et al., 2014

Preferred Common Name

• black leg disease of potato

International Common Names

• English: blackleg; slow wilt; soft rot; stem rot; top wilt
• French: jambe noire

Local Common Names

• Netherlands: stengelnatrot; zwartbenigheid

Summary of Invasiveness

Dickeya solani is a bacterial pathogen of potato thought to have crossed from horticultural crops in Northern Europe in 2005-2006. The earliest reports of disease on potato are from Belgium and the Netherlands, though it is now present in most European countries and Israel. Symptoms range from blackleg to top wilt in the growing plant and soft rotting of tubers. Symptoms are indistinguishable from those caused by Pectobacterium atrosepticum, P. carotovorum, P. parmentieri (formerly P. wasabiae) (Khayi et al., 2016) and D. dianthicola and control is usually reliant on seed certification schemes to mitigate its worst effects. It should be noted that most losses are attributable to the certification process itself though losses as high as 30% have been recorded in crops grown in Israel. There is no evidence of varietal resistance in potato. D. solani is a highly clonal organism highlighting its recent emergence as a pathogen but also the vulnerability of Europe’s highly integrated potato production system.

Taxonomic Tree

• Domain: Bacteria
•     Phylum: Proteobacteria
•         Class: Gammaproteobacteria
•             Order: Enterobacteriales
•                 Family: Enterobacteriaceae
•                     Genus: Dickeya
•                         Species: Dickeya solani

Notes on Taxonomy and Nomenclature

Several attempts have been made to clarify the taxonomic position and circumscribe the diversity within the species formerly known as Erwinia chrysanthemi (Burkholder et al., 1953) either on the basis of differences in host range, pathovars (Young et al., 1978; Lelliott and Dickey, 1984) or biochemical profiles, biovars (Samson and Nassan-Agha, 1978; Ngwira and Samson, 1990). These studies culminated in the creation of the genus Dickeya and the elevation of infra-specific taxa to new species within it; D. chrysanthemi, D. dadantii, D. dianthicola, D. dieffenbachiae, D. paradisiaca and D. zeae (Samson et al., 2005) with subsequent revision reassigning D. dieffenbachiae as a subspecies of D. dadantii (Brady et al., 2012). With the exception of D. dadantii subsp. dieffenbachiae all are known to cause disease in potato (Czajkowski et al., 2011; Toth et al., 2011).

In 2005/2006 a growing number of cases of potato blackleg/top wilt in Northern Europe and Israel were found to be caused by a previously unrecognized Dickeya sp. (Laurila et al., 2008; Parkinson et al., 2009; Slawiak et al., 2009b), frequently referred to in early reports as Dickeya sp. biovar 3 (Slawiak et al., 2009a; Tsror et al., 2010, 2011; Czajkowski et al., 2012a). Detailed study of this pathogen highlighted a close relationship to Dickeya dadantii, but ultimately it was considered sufficiently distinct to merit description as a new species; D. solani (van der Wolf et al., 2014b).

Distribution

D. solani is widespread in Europe and also occurs in Israel and Republic of Georgia.

Distribution Table

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.

History of Introduction and Spread

The earliest known strains of D. solani were originally isolated from hyacinth, leading many to speculate that the pathogen crossed into potato production from horticulture (Parkinson et al., 2015). In December 2013, D. solani was intercepted at Ningbo Port, China, on diseased bulbs of Hyacinthus orientalis exported from the Netherlands (Chen et al., 2015).

Since 2004, D. solani has spread over much of Europe and to Israel in less than 5 years through trade in latently infected seed potatoes (Toth et al., 2011). It was probably first introduced to Israel in 2004 via infected seed potatoes imported from the Netherlands. It was intercepted in Israel in exported seed potatoes from France in 2009 and from Germany (Tsror et al., 2009).

D. solani was first reported in Poland in 2005 (Slawiak et al., 2009b). The most likely source was potatoes which were imported from the Netherlands. Large-scale survey for D. solani in seed potato fields and water sources in Poland indicated the presence of D. solani in potato fields in the years 2009-2013; the intensity of occurrence depends on the year, and is higher if the summer is hot and dry (Potrykus et al., 2016). In the same studies D. solani was not detected in waterways.

In Norway, it was first reported in 2012, again, in potatoes grown from imported seed (van der Wolf and Bergsma Vlami, 2013). In Spain, it was likely to have been first isolated from potatoes grown in Valencia in 2002, though the exact identity of this pathogen has yet to be clarified (Palacio-Bielsa et al., 2006). Most findings in Sweden, up to 2011, were in crops produced from imported seed potatoes from the Netherlands. However findings now found in Swedish, German and Finnish origin potatoes suggest the pathogen is becoming established in other production systems (Rölin and Nilsson, 2011). In Finland it was first noted in 2004, and the highest incidence was found in 2006 (Degefu et al., 2013). In Crete, Greece, it was first recorded in 2009.

D. solani was first found in England and Wales in 2007 and in Scotland in 2009 (Cahill et al., 2010). In 2010, seed potatoes of Scottish origin were reported to be free from Dickeya spp. thanks to a monitoring programme introduced to Scotland in 2006. However, D. solani was found in potatoes that had entered Scotland for processing and planting, and in one river (Cahill et al., 2010).

D. solani has become the dominant cause of blackleg in Belgium since 2005 (ILVO, 2010) and is also an important cause of blackleg in Switzerland (Keiser and de Werra, 2013).

D. solani was first confirmed in Georgia in 2008. Its likely source was imported seed potatoes from the Netherlands and Germany (Tsror et al., 2011). D. solani was first detected in Turkey in 2016 (Ozturk and Aksoy, 2017).

In addition, D. solani was detected in healthy potato rhizosphere in Germany in 2006 (Hauer et al., 2010; Potrykus et al., 2014).

In 2013, blackleg of potato was observed in a commercial field in Minas Gerais, Brazil. The pathogen was identified as D. solani (Cardoza et al., 2017).

Risk of Introduction

It is very likely that D. solani crossed into potato production from horticulture because the earliest known strains of D. solani were originally isolated from hyacinth. Movement of D. solani via infected hyacinth is therefore likely.

World-wide trade of latently infected potatoes has facilitated the spread of D. solani.

In Israel, D. solani is considered to be a quarantine organism (Tsror et al., 2009).

Habitat List

Hosts/Species Affected

Potato is the primary host for D. solani but it also causes disease in Hyacinthus orientalis (hyacinth) and has been found in association with the sedge Cyperus rotundus, a common weed in Israel (Tsror et al., 2010). The latter may serve as an alternative host in the absence of a host crop.

The vegetative growth, post-harvest, seedborne and storage stages of the host plant are most affected by D. solani.

Cultivar susceptibility studies have shown that all potato cultivars studied to date are, at least to some degree, susceptible. Roufflange et al. (2013) noted that cv. Agria was the most susceptible of six cultivars studied (cvs. Agria, Arinda, Charlotte, Innovator, Lady Claire and Victoria) when looking at aerial stem rots in greenhouse experiments. Gerardin et al. (2013) found similar results highlighting cv. Agria’s susceptibility to tuber soft rot caused by D. solani. However, it is clear that environmental factors, such as soil moisture, can have a dramatic effect on the severity of the disease in the field (Gill et al., 2014).

Host Plants and Other Plants Affected

Growth Stages

Symptoms

D. solani causes blackleg and top wilt of the growing potato plant and soft rot of tubers. The wilt may be rapid as the soft rot moves from the infected tuber through the vascular system of the plant (SASA, 2009). In some varieties, wilting may occur without any apparent blackleg (SASA, 2009). 

List of Symptoms/Signs

Biology and Ecology

Genetics

D. solani is closely related to D. dadantii on the basis of DNA-DNA hybridization data and average nucleotide identity (ANI) values and this has led some to speculate that it may be a subspecies of the latter (van Vaerenbergh et al., 2012). It can however, be readily distinguished from other members of the genus Dickeya on the basis of sequence data derived from the intergenic spacer region (IGS), dnaX, recA, dnaN, fusA, gapA, purA, rplB, rpoS and gyrA genes (van der Wolf et al., 2014b), the concatenated sequences of 23 conserved proteins (Naushad et al., 2014) and RFLP analysis of the recA gene (Waleron et al., 2013).

A recent study looking at differences between conserved signature idels (CSIs) and proteins (CSPs) amongst the plant pathogenic genera Brenneria, Dickeya, Pectobacterium and other members of the order Enterobacteriales showed that Brenneria and Pectobacterium shared a common ancestor exclusive from Dickeya (Naushad et al., 2014).

Genome sequence data from a variety of different D. solani isolates (Garlant et al., 2013; Pritchard et al., 2013; Khayi et al., 2014, 2015, 2016; Golanowska et al., 2015) and variable number tandem repeats analysis (Parkinson et al., 2015) demonstrate clearly that D. solani is a clonal organism; little variation exists between isolates from a wide variety of locations and environmental sources which adds weight to the view that this is a recently emerged pathogen. However there is some evidence to suggest that isolates obtained from hot countries, e.g., Israel, are more virulent that those obtained from the cooler north (Tsror et al., 2013) despite the lack of diversity in the genome. In studies of Golanowska et al. (2016) strains isolated in Poland indicated higher ability to macerate potato tuber tissue  than strains from Finland and Israel.

Comparative genomic analysis has identified the presence of three large polyketide/fatty acid/non-ribosomal peptide synthetase clusters (Garlant et al., 2013) not present in the closely related D. dadantii, which may be involved in the production of toxic secondary metabolites. Furthermore, D. solani contained several unique genes to the genus Dickeya which may confer advantages for adaptation to new environments, a finding largely backed-up by a subsequent, independent study (Pédron et al., 2014).

Physiology and Phenology

D. solani produces Gram-negative, motile, rods. It produces phosphatases and growth on α-methylglucoside results in indole and acid production. Arginine is not degraded under anaerobic conditions. Acid is produced from D-arabinose, mannitol, melibiose and raffinose but not from 5-ketogluconate or inulin. It is pectinolytic and can rapidly degrade potato tissue.

D. solani is less susceptible to attack from soil saprophytic bacteria and is a highly efficient as a colonizer of the growing potato plant, when compared against another member of the genus Dickeya pathogenic to potato in Northern Europe, D. dianthicola (Czajkowski et al., 2012c).

Environmental Requirements

D. solani does not survive well in soil in the absence of its host (Toth et al., 2011) and earlier studies have suggested it is unable to persist beyond 3 weeks, irrespective of soil type, temperature and humidity (van der Wolf et al., 2007) and may survive for as little as 7 days at 6°C and 50% field moisture capacity (van der Wolf et al., 2009).

Climate

Air Temperature

Natural enemies

Notes on Natural Enemies

Bacteriophages such as Bacteriophage LIMEstone 1 & 2 (Andriaenssens et al., 2012), ΦD3 Φ D5 (Czajkowski et al., 2014, 2015b), Φ D10.3 and Φ D23.1 (Cjakowski et al., 2015a) have shown some potential for biocontrol of D. solani.

Means of Movement and Dispersal

Accidental Introduction

D. solani is predominantly seedborne and almost all new findings can be traced back to the movement of latently infected seed (Slawiak et al., 2008; Tsror et al., 2009, 2011; Cahill et al., 2010; Elphinstone, 2012; Degefu et al., 2013; Dreo et al., 2013). However, D. solani has also been found in irrigation water in both Finland and the UK (Laurila et al., 2008; Cahill et al., 2010; Parkinson et al., 2015) with infected crops grown in the vicinity or the processing of infected potatoes with waste waters discharged into local rivers the likely source of these infestations. D. solani was not detected during a 4 year survey of waterways in Poland. Although this has not been conclusively proven, the possibility exists that D. solani may also be spread by the use of infested irrigation water.

D. solani was detected in healthy potato rhizosphere in Germany in 2006 (Hauer et al., 2010; Potrykus et al., 2014).

Trade in ware potatoes may also provide an additional route for long-distance infection as the bacterial ooze on the surface of transport/storage materials (boxes, sacks, etc.), machinery etc. can serve as a source of infection if seed tubers come into subsequent contact.  Liquid and solid waste from packing or processing of infected tubers may also serve as a route for further spread of the pathogen (Toth et al., 2011).

Pathway Causes

Pathway Vectors

Plant Trade

Impact Summary

Economic Impact

In Israel, potato yield reductions up to 30% have been recorded as a consequence of D. solani infection across a wide number of commercially produced cultivars (Tsror et al., 2009) and in more limited studies yield reductions of up to 50% from individual plants have been recorded in Finland (Laurila et al., 2010).

It should be stressed that most direct losses to potato production in Europe caused by D. solani have occurred as a result of downgrading or rejection of potatoes during seed certification (Toth et al., 2011). As national certification tolerances differ, the economic impact varies from country to country. Strict tolerance in the Netherlands has led to increased direct losses of up to €30M annually (Prins and Breukers, 2008), largely attributable to the actions of D. solani.

According to ILVO (2010), D. solani is an aggressive form of Dickeya causing macerative blackleg in seed potatoes from Flanders, Belgium and causing a major block to export.

Risk and Impact Factors

• Reproduces asexually

• Host damage
• Negatively impacts agriculture
• Negatively impacts livelihoods

• Pathogenic

• Highly likely to be transported internationally accidentally
• Difficult to identify/detect as a commodity contaminant
• Difficult to identify/detect in the field
• Difficult/costly to control

Similarities to Other Species/Conditions

Symptoms caused by D. solani on potato, specifically blackleg and top wilt of the growing potato plant and soft rot of tubers, are indistinguishable from those produced by other plant pathogenic bacteria, namely: Pectobacterium atrosepticum, P. carotovorum subsp. carotovorum, P. parmentieri (earlier classified as P. wasabiae), P. wasabiae, D. dianthicola, etc. Therefore, it is vital that a positive diagnosis is not reliant on visual inspection alone. A number of diagnostics protocols are available and have been recently reviewed (Czajkowski et al., 2015). Most are reliant on either conventional (Potrykus et al., 2014) or real-time PCR (Kelly et al., 2012; Pritchard et al., 2012; van der Wolf et al., 2014a; Humphris et al., 2015), with the latter work by Humphris and co-workers giving a step-by-step guide, methods and protocols for diagnosis.

Toth et al. (2010) noted characteristics which help distinguish Dickeya spp. from Pectobacterium spp.: "Dickeya spp. can initiate disease from lower inoculum levels, have a greater ability to spread through the plant’s vascular tissue, are considerably more aggressive, and have higher optimal temperatures for disease development (the latter potentially leading to increased disease problems as Europe’s climate warms). However, they also appear to be less hardy than Pectobacterium spp. in soil and other environments outside the plant."

Prevention and Control

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Prevention

Within the European Community (EC) D. solani is a regulated, non-quarantine pest and as such is controlled in the majority of Member States by their respective potato seed certification schemes. In general, potato seed production is initiated from pathogen-tested nuclear stock microplants and field production is limited to a restricted number of generations thus avoiding the build-up of pathogens, such as D. solani, with each field multiplication (Toth et al., 2011). All classification schemes are reliant on visual inspection of field crops and tubers in store and although there is generally a zero tolerance to blackleg and soft rot diseases in high grade material, latent infections exist and will obviously be overlooked, leading some to advocate the use of post-harvest testing to monitor seed stocks for the presence of D. solani (Czajkowski et al., 2011).

Scotland was the first country within the EC to enforce testing of all non-indigenous seed stocks prior to planting to ensure that they are free of D. solani (Kerr et al., 2010). It has also introduced a zero tolerance for blackleg caused by Dickeya spp. in its seed tuber classification scheme, using a system based on field inspection backed by laboratory testing, in which high-risk crops (non-Scottish origin) are targeted but 10% of indigenous production is also surveyed to ensure freedom from Dickeya spp.

As the movement of latently infected seed is the principal infection route, measures to assure seed health are gaining traction in some countries, such as the Safe Haven Scheme currently in operation within the UK (see http://www.potato.org.uk/growing/plant-health/safe-haven). This is an industry-led initiative that ensures that only disease-free microplants can enter the production chain and that field-grown generations can only be grown on agricultural units that cannot handle seed from outside the scheme. In this way, healthy planting material is passing through the production chain, with no possible avenue for the introduction of infection from other sources of seed tubers.

Control

Movement control

Once D. solani has become established there are a number of measures that can reduce its impact and the risk of spreading the pathogen further. Cleaning and disinfection of machinery, equipment and grading lines are very important and a range of disinfectants have shown efficacy in suppressing D. solani (Czajkowski et al., 2013). There are also a number of studies that have detected the presence of D. solani in irrigation water in both Finland and the UK (Laurila et al., 2008; Cahill et al., 2010; Parkinson et al., 2015) suggesting that monitoring sources of irrigation water, backed by restrictions on irrigation where the pathogen is found, may reduce contamination and disease in field-grown crops.

Biological control

Some preliminary studies are providing evidence that biological control may have benefit in reducing the impact of D. solani. Studies have explored the use of bacteriophage (Adriaenssens et al., 2012) and antagonistic bacteria such as Serratia plymuthica (Czajkowski et al., 2012b).

References

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Distribution References

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Laurila J, Ahola V, Lehtinen A, Joutsjoki T, Hannukkala A, Rahkonen A, Pirhonen M, 2008. Characterization of Dickeya strains isolated from potato and river water samples in Finland. European Journal of Plant Pathology. 122 (2), 213-225. http://springerlink.metapress.com/link.asp?id=100265 DOI:10.1007/s10658-008-9274-5

Ozturk M, Aksoy H M, 2017. First report of Dickeya solani associated with potato blackleg and soft rot in Turkey. Journal of Plant Pathology. 99 (1), 298. http://www.sipav.org/main/jpp/index.php/jpp/article/view/3807/2449

Palacio-Bielsa A, Cambra M A, López M M, 2006. Characterisation of potato isolates of Dickeya chrysanthemi in Spain by a microtitre system for biovar determination. Annals of Applied Biology. 148 (2), 157-164. http://www.blackwell-synergy.com/doi/abs/10.1111/j.1744-7348.2006.00045.x DOI:10.1111/j.1744-7348.2006.00045.x

Potrykus M, Golanowska M, Sledz W, Zoledowska S, Motyka A, Kolodziejska A, Butrymowicz J, Lojkowska E, 2016. Biodiversity of Dickeya spp. isolated from potato plants and water sources in temperate climate. Plant Disease. 100 (2), 408-417. http://apsjournals.apsnet.org/loi/pdis DOI:10.1094/PDIS-04-15-0439-RE

Rölin A, Nilsson ATS, 2011. Dickeya spp - occurrence in Swedish grown potato tubers., Sweden: Hushallnings Sallskapet. http://www.bioforsk.no/ikbViewer/Content/94215/PTDW_Dickeya_Rolin_PR.pdf

Sarris P F, Trantas E, Pagoulatou M, Stavrou D, Ververidis F, Goumas D E, 2011. First report of potato blackleg caused by biovar 3 Dickeya sp. (Pectobacterium chrysanthemi) in Greece. New Disease Reports. Article 21. http://www.ndrs.org.uk/article.php?id=024021

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Tsror L, Erlich O, Lebiush S, Hazanovsky M, Zig U, Slawiak M, Grabe G, Wolf J M van der, Haar J J van de, 2009. Assessment of recent outbreaks of Dickeya sp. (syn. Erwinia chrysanthemi) slow wilt in potato crops in Israel. European Journal of Plant Pathology. 123 (3), 311-320. http://springerlink.metapress.com/link.asp?id=100265 DOI:10.1007/s10658-008-9368-0

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Links to Websites

Organizations

Netherlands: Plant Research International, Wageningen (PRI), Postbus 69, 6700AB,, Wageningen, www.wageningenur.nl

UK: FERA (The Food and Environment Research Agency), Sand Hutton, York, Y0411LZ, http://www.fera.defra.gov.uk

UK: The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, http://www.hutton.ac.uk/

Scotland: Science and Advice for Scottish Agriculture (SASA), 1 Roddinglaw Road, Edinburgh, EH12 9FJ, http://www.sasa.gov.uk

Contributors

23/01/15 Original text by:

Gerry Saddler, Science and Advice for Scottish Agriculture, Edinburgh, UK

Distribution Maps