The authors of this content are Amy Charkowski, Kalpana Sharma, Monica L. Parker, Gary A. Secor, John Elphinstone
Blackleg and Soft Rot of Potato Caused by Dickeya
Taxonomy and Nomenclature
The genus Dickeya is a member of the ß-Proteobacteria in the family Pectobacteriaceae within the order Enterobacterales. The Pectobacteriaceae family also contains the genera Brenneria, Lonsdalea Pectobacterium, and Sodalis (Adeolu et al. 2016).
Members of the Dickeya genus originally belonged to the genus Erwinia represented by strains within species E. chrysanthemi (Burkholder et al. 1953).
Later this species was reclassified as Pectobacterium chrysanthemi (Hauben et al. 1998), until Samson et al. (2005) elevated the species to the genus Dickeya with six species.
There have since been some changes and additions to these species, which currently include D. aquatica, D. chrysanthemi, D. dadantii, D. dianthicola, D. fangzhongdai, D. paradisiaca, D. solani, and D. zeae (Brady et al. 2012; Parkinson et al. 2014; Samson et al. 2005; Tian et al. 2016).
The genus Dickeya is a member of the ß-Proteobacteria in the family Pectobacteriaceae within the order Enterobacterales. The Pectobacteriaceae family also contains the genera Brenneria, Lonsdalea Pectobacterium, and Sodalis (Adeolu et al. 2016).
Members of the Dickeya genus originally belonged to the genus Erwinia represented by strains within species E. chrysanthemi (Burkholder et al. 1953).
Later this species was reclassified as Pectobacterium chrysanthemi (Hauben et al. 1998), until Samson et al. (2005) elevated the species to the genus Dickeya with six species.
There have since been some changes and additions to these species, which currently include D. aquatica, D. chrysanthemi, D. dadantii, D. dianthicola, D. fangzhongdai, D. paradisiaca, D. solani, and D. zeae (Brady et al. 2012; Parkinson et al. 2014; Samson et al. 2005; Tian et al. 2016).
Host Range
Dickeya has a broad host range and can infect plant species in at least 12 dicot families in 10 orders and 10 monocot families in 5 orders, and include ornamentals such as chrysanthemum, carnation, dahlia, and calla lily as well as important crops including carrot, tomato, and, the most economically important, potato (Charkowski 2018; Ma et al. 2007a, b; Samson et al. 2005).
While all Dickeya species, with the exception of D. paradisiaca, have been found on ornamentals in Europe, only D. dianthicola and D. solani have caused significant economic losses on potato (Toth et al. 2011). In both cases, the lack of genetic diversity between isolates on potato and ornamental hosts suggests the organisms may have spread to potato from such a host (Parkinson et al. 2009; Slawiak et al. 2009).
Only D. aquatica, which was isolated from waterways in the UK (Parkinson et al. 2014) and Maine (J. Hao, personal communication), has not yet been associated with a plant disease.
Dickeya has a broad host range and can infect plant species in at least 12 dicot families in 10 orders and 10 monocot families in 5 orders, and include ornamentals such as chrysanthemum, carnation, dahlia, and calla lily as well as important crops including carrot, tomato, and, the most economically important, potato (Charkowski 2018; Ma et al. 2007a, b; Samson et al. 2005).
While all Dickeya species, with the exception of D. paradisiaca, have been found on ornamentals in Europe, only D. dianthicola and D. solani have caused significant economic losses on potato (Toth et al. 2011). In both cases, the lack of genetic diversity between isolates on potato and ornamental hosts suggests the organisms may have spread to potato from such a host (Parkinson et al. 2009; Slawiak et al. 2009).
Only D. aquatica, which was isolated from waterways in the UK (Parkinson et al. 2014) and Maine (J. Hao, personal communication), has not yet been associated with a plant disease.
Geographical Distribution
As with Pectobacterium, Dickeya species have been reported on a wide range of hosts in different countries around the world (Samson et al. 2005). While D. zeae, D. solani, and D. dianthicola have wide geographic distributions, D. paradisiaca appears to be restricted to Colombia (Samson et al. 2005; Toth et al. 2011).
D. dianthicola was the first Dickeya species to be associated with plant disease in Europe, occurring on Dianthus in the Netherlands, Denmark, and the UK and later spreading to other nations (Hellmers 1958). It was later associated with other ornamentals and crops in a number of European countries, including potato.
In some cases, D. dianthicola replaced P. atrosepticum as the dominant blackleg pathogen (Parkinson et al. 2009; Toth et al. 2011). D. solani was recognized independently as a new Dickeya pathogen on potato by several groups from 2004 through 2010 (Laurila et al. 2008; Parkinson et al. 2009; Slawiak et al. 2009).
Isolates of both D. dianthicola and D. solani show little genetic diversity compared to isolates from ornamentals, and within these species there is a high degree of genetic similarity. Therefore, it seems likely that these pathogens have independently jumped host from an ornamental onto potato (Toth et al. 2011).
As with Pectobacterium, Dickeya species have been reported on a wide range of hosts in different countries around the world (Samson et al. 2005). While D. zeae, D. solani, and D. dianthicola have wide geographic distributions, D. paradisiaca appears to be restricted to Colombia (Samson et al. 2005; Toth et al. 2011).
D. dianthicola was the first Dickeya species to be associated with plant disease in Europe, occurring on Dianthus in the Netherlands, Denmark, and the UK and later spreading to other nations (Hellmers 1958). It was later associated with other ornamentals and crops in a number of European countries, including potato.
In some cases, D. dianthicola replaced P. atrosepticum as the dominant blackleg pathogen (Parkinson et al. 2009; Toth et al. 2011). D. solani was recognized independently as a new Dickeya pathogen on potato by several groups from 2004 through 2010 (Laurila et al. 2008; Parkinson et al. 2009; Slawiak et al. 2009).
Isolates of both D. dianthicola and D. solani show little genetic diversity compared to isolates from ornamentals, and within these species there is a high degree of genetic similarity. Therefore, it seems likely that these pathogens have independently jumped host from an ornamental onto potato (Toth et al. 2011).
Symptoms
Although Dickeya can cause tuber soft rot, it primarily causes blackleg on potato. Blackleg symptoms include necrosis of the potato stem, originating from the mother tuber and spreading several centimeters above ground (image below).
Plant leaves will wilt and curl as the disease develops and the plant vascular system will become necrotic. The pith of the stem is often decayed. D. dianthicola can also cause severe seed decay and lack of plant emergence in severe cases.
Infected plants produce few or no tubers and any tubers produced may decay prior to harvest. Both Dickeya and Pectobacterium may be present together in diseased plants. In the United States, P. parmentieri is the most common species found together with Dickeya.
Although Dickeya can cause tuber soft rot, it primarily causes blackleg on potato. Blackleg symptoms include necrosis of the potato stem, originating from the mother tuber and spreading several centimeters above ground (image below).
Plant leaves will wilt and curl as the disease develops and the plant vascular system will become necrotic. The pith of the stem is often decayed. D. dianthicola can also cause severe seed decay and lack of plant emergence in severe cases.
Infected plants produce few or no tubers and any tubers produced may decay prior to harvest. Both Dickeya and Pectobacterium may be present together in diseased plants. In the United States, P. parmentieri is the most common species found together with Dickeya.
Foliar symptoms of Dickeya dianthicola on potato. Initial symptoms are either a lack of emergence or leaf curling (a). The base of the stem turns dark brown or black and this necrosis can extend several centimeters from the soil line (b). The pith inside symptomatic stems is often decayed and the xylem are necrotic for several centimeters above the external stem necrosis and the pith decay (c). Disease symptoms may only develop on one stem of a multi-stem plant (d).<br> (Courtesy: Amy O. Charkowski | Colorado State University)
Epidemiology
Initial seed potato production relies on pathogen-free micropropagated plantlets. These plantlets are grown in greenhouses or screenhouses to produce minitubers, which are used for field planting (Frost et al. 2013). Dickeya will kill micropropagated plants within a few days and is not typically found in greenhouses or screenhouses.
It appears to contaminate potatoes after they have been grown for at least one generation in the field, with the risk of contamination increasing with each generation in the field. Dickeya does not appear to survive in soil, but it can contaminate waterways and survive for long periods in surface water (Toth et al. 2011).
It may also survive in weeds (Fikowicz-Krosko and Czajkowski 2017) or volunteer potatoes and spread by insects (Rossmann et al. 2018). Like Pectobacterium, Dickeya appears to spread mainly at harvest, where it can spread from infected vines and tubers to previously uncontaminated tubers.
The bacteria are mainly found on tuber lenticels, but may also be present in the tuber stolon scar. Asymptomatic infestations are common, so it is not possible to visually assess seed potato lots for risk.
Blackleg development is highly dependent on the environment and it is unpredictable, even when a seed lot is known to be contaminated with Dickeya. Plants grown from infested seed lots planted in warm, humid areas tend to develop disease, while plants grown from the same infested seed lot planted in cooler, drier climates may remain healthy.
Temperatures above 30 °C during the growing season appear to be particularly conducive to disease development. Co-contamination with Pectobacterium and Dickeya appears to lead to disease development more frequently than when only Dickeya is present.
Initial seed potato production relies on pathogen-free micropropagated plantlets. These plantlets are grown in greenhouses or screenhouses to produce minitubers, which are used for field planting (Frost et al. 2013). Dickeya will kill micropropagated plants within a few days and is not typically found in greenhouses or screenhouses.
It appears to contaminate potatoes after they have been grown for at least one generation in the field, with the risk of contamination increasing with each generation in the field. Dickeya does not appear to survive in soil, but it can contaminate waterways and survive for long periods in surface water (Toth et al. 2011).
It may also survive in weeds (Fikowicz-Krosko and Czajkowski 2017) or volunteer potatoes and spread by insects (Rossmann et al. 2018). Like Pectobacterium, Dickeya appears to spread mainly at harvest, where it can spread from infected vines and tubers to previously uncontaminated tubers.
The bacteria are mainly found on tuber lenticels, but may also be present in the tuber stolon scar. Asymptomatic infestations are common, so it is not possible to visually assess seed potato lots for risk.
Blackleg development is highly dependent on the environment and it is unpredictable, even when a seed lot is known to be contaminated with Dickeya. Plants grown from infested seed lots planted in warm, humid areas tend to develop disease, while plants grown from the same infested seed lot planted in cooler, drier climates may remain healthy.
Temperatures above 30 °C during the growing season appear to be particularly conducive to disease development. Co-contamination with Pectobacterium and Dickeya appears to lead to disease development more frequently than when only Dickeya is present.
Pathogenicity Determinants and Resistance
Dickeya pathogenicity relies mainly on pectate lyases and other plant cell wall-degrading enzymes secreted by the bacterial cell, although several other virulence genes are known (Charkowski et al. 2012). Although both Pectobacterium and Dickeya use plant cell wall-degrading enzymes, there are some important differences in enzyme genes and gene regulation between the genera that may account for some of the differences in disease symptoms.
There are no examples of gene-for-gene resistance with Dickeya and the basis for resistance to Dickeya in wild potato species or for host range is poorly understood. There are no resistant commercial potato varieties, but varieties do differ in tolerance.
Dickeya pathogenicity relies mainly on pectate lyases and other plant cell wall-degrading enzymes secreted by the bacterial cell, although several other virulence genes are known (Charkowski et al. 2012). Although both Pectobacterium and Dickeya use plant cell wall-degrading enzymes, there are some important differences in enzyme genes and gene regulation between the genera that may account for some of the differences in disease symptoms.
There are no examples of gene-for-gene resistance with Dickeya and the basis for resistance to Dickeya in wild potato species or for host range is poorly understood. There are no resistant commercial potato varieties, but varieties do differ in tolerance.
Significance and Economic Loss
The relative importance of Dickeya as a potato pathogen appears to be increasing (Toth et al. 2011). D. solani caused severe losses in the early 2000s in multiple countries and in 2015 D. dianthicola was in up to 20% of seed potato lots in some states in the US. Recent development of species-specific PCR assays for Dickeya will likely reveal that it is widespread in potato. As with Pectobacterium, farmers lose millions annually to blackleg caused by Dickeya.
The relative importance of Dickeya as a potato pathogen appears to be increasing (Toth et al. 2011). D. solani caused severe losses in the early 2000s in multiple countries and in 2015 D. dianthicola was in up to 20% of seed potato lots in some states in the US. Recent development of species-specific PCR assays for Dickeya will likely reveal that it is widespread in potato. As with Pectobacterium, farmers lose millions annually to blackleg caused by Dickeya.
Management
Cultural practices are important for Dickeya management and the recommendations are essentially the same as for Pectobacterium (Czajkowski et al. 2011, 2013). Growers initiate potato production with micropropagated plantlets that are free of Dickeya, but tubers may become contaminated once they are planted in fields.
To reduce the risk of disease spread, growers should sanitize equipment thoroughly between seed fields, especially if blackleg is present. At planting, growers should fully suberize seed if they are using cut seed, and they should not plant seed that is too cold or into saturated ground.
During the growing season, they should irrigate with ground water if possible and not overfertilize with nitrogen. Rouging infected plants is likely to spread the pathogen if diseased plants are present. At harvest, the Dickeya may multiply on the vines as they senesce, so quickly killing potato vines may aid in reducing disease incidence the following year.
Tubers should be allowed to heal before cooling storages. Good airflow and high humidity in potato warehouses will also aid in reducing soft rot in storage. High levels of carbon dioxide in warehouses will promote soft rot development.
Seed potatoes may be tested for Dickeya prior to planting (Czajkowski et al. 2015; Humphris et al. 2015) and growers should avoid planting contaminated seed lots in areas where growing conditions are conducive to blackleg.
Cultural practices are important for Dickeya management and the recommendations are essentially the same as for Pectobacterium (Czajkowski et al. 2011, 2013). Growers initiate potato production with micropropagated plantlets that are free of Dickeya, but tubers may become contaminated once they are planted in fields.
To reduce the risk of disease spread, growers should sanitize equipment thoroughly between seed fields, especially if blackleg is present. At planting, growers should fully suberize seed if they are using cut seed, and they should not plant seed that is too cold or into saturated ground.
During the growing season, they should irrigate with ground water if possible and not overfertilize with nitrogen. Rouging infected plants is likely to spread the pathogen if diseased plants are present. At harvest, the Dickeya may multiply on the vines as they senesce, so quickly killing potato vines may aid in reducing disease incidence the following year.
Tubers should be allowed to heal before cooling storages. Good airflow and high humidity in potato warehouses will also aid in reducing soft rot in storage. High levels of carbon dioxide in warehouses will promote soft rot development.
Seed potatoes may be tested for Dickeya prior to planting (Czajkowski et al. 2015; Humphris et al. 2015) and growers should avoid planting contaminated seed lots in areas where growing conditions are conducive to blackleg.
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