Dickeya solani
(black leg disease of potato)

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.

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

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).

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).

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).

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.

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."

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).

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

23/01/15 Original text by:

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