Pectobacterium parmentieri
(black leg disease of potato)

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Identity

Preferred Scientific Name

• Pectobacterium parmentieri Khayi et al. 2016

Preferred Common Name

• black leg disease of potato

Other Scientific Names

• Erwinia carotovora subsp. wasabiae Goto and Matsumoto, 1987
• Pectobacterium carotovorum subsp. wasabiae (Goto and Matsumoto, 1987) Hauben et al. 1999
• Pectobacterium wasabiae Gardan et al. 2003

International Common Names

• English: soft rot; stem rot
• French: jambe noire

Summary of Invasiveness

Pectobacterium parmentieri is a bacterial pathogen of potato present in Europe since the 1960s. The bacterium was earlier classified as Pectobacterium carotovorum. After reclassification of P. carotovorum subsp. carotovorum SCC3193 to P. wasabiae and later on to P. parmentieri, several studies devoted to identification of pectinolytic bacteria in international collections and identification of the strains isolated from infected potato plants have indicated that this bacteria commonly occurs in several regions of Europe, Canada, USA, New Zealand and South Africa. P. parmentieri can cause symptoms of blackleg and soft rot on potato tubers. These diseases are usually a consequence of latent infection of seed potatoes. In the majority of countries pre-basic and basic seed tuber potatoes intended for the production of seed tuber crops should be free of Pectobacterium spp. and Dickeya spp. P. parmentieri is not present on any international or national alert lists.

Taxonomic Tree

• Domain: Bacteria
•     Phylum: Proteobacteria
•         Class: Gammaproteobacteria
•             Order: Enterobacteriales
•                 Family: Enterobacteriaceae
•                     Genus: Pectobacterium
•                         Species: Pectobacterium parmentieri

Notes on Taxonomy and Nomenclature

Erwinia carotovora subsp. wasabiae was isolated for the first time in the late 1980s from rotting Japanese horseradish (Goto and Matsumoto, 1987). Hauben et al. (1998) later established the genus Pectobacterium and all pectinolytic Erwinia were transferred to this new taxon. In this classification, the genus Pectobacterium included two species: Pectobacterium carotovorum and Pectobacterium chrysanthemum.P. carotovorum was divided into four species including Pectobacterium carotovorum subsp. wasabiae. Subsequently, subspecies P.carotovorum subsp. wasabiae was elevated to species level, namely: Pectobacterium wasabiae (Gardan et al., 2003). Neither the occurrence of P. wasabiae on potato, nor its presence outside of Japan was reported before 2009. Pitman et al. (2010) demonstrated that P. wasabiae was capable of causing disease symptoms on potato plants in New Zealand. In 2012 P. carotovorum subsp. carotovorum SCC3193, a bacterial strain widely used as a model in molecular studies (Eriksson et al., 1998; Koskinen et al., 2012) was reclassified as P. wasabiae SCC3193 (Nykyri et al., 2012). This reclassification was followed by further renaming of strains deposited in international collections as P. carotovorum subsp. carotovorum to P. wasabiae (de Boer et al., 2012; Nabhan et al., 2012a, b; Slawiak et al., 2013; Waleron et al., 2013). Recent comprehensive analysis based on DDH, gANI and ANI values calculated in silico on P. wasabiae genomes resulted in reclassification of all P. wasabiae potato-originating isolates into a newly established species P. parmentieri (Khayi et al., 2016).

Description

Strains of P. parmentieri are Gram-negative, rod-shaped necrotrophs which destroy plant tissue components through the activity of plant cell wall-degrading enzymes such as pectinases, cellulases and proteases secreted via Type I or II secretion systems (Chatterjee et al., 1995; Liu et al., 1999; Charkowski et al., 2012) but lack the Type III secretion system (Kim et al., 2009). Pectinases (pectate and pectine lyases, polygalacturonases, methyl- and acyl- ) and cellulases play a major role in the virulence of soft-rotting pathogens as they degrade the primary cell walls of infected plants. Proteases are also mentioned as they disrupt host plant protoplasts via degradation of transmembrane proteins (Marits et al., 1999). Effective spread of the pathogen through the plant's vascular system, often referred to as motility of the strain, is essential for the development of disease symptoms (Toth et al., 2003). The efficient production of iron scavenging molecules, siderophores, provides cofactors involved in almost all life-supporting processes (Ishimaru and Loper, 1992).

The Type strain is P. parmentieri CFBP 8475^T isolated from potato plants in France (Khayi et al., 2016)

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

P. parmentieri was formerly classified as Erwinia carotovora, Pectobacterium carotovorum and later as Pectobacterium wasabiae. Neither the occurrence of P. wasabiae on potato, nor its presence outside of Japan was reported before 2009. Pitman et al. (2010) demonstrated that P. wasabiae is capable of causing disease symptoms on potato plants in New Zealand. The presence in Europe of virulent strains of P. carotovorum subsp. carotovorum able to cause blackleg has been reported by Waleron et al. (2002; recA PCR-RFLP profile 3) and Haan et al. (2008; vPcc).

 In 2012, Nykyri et al. (2012) reported that P. carotovorum subsp. carotovorum SCC3193, a model strain widely used in molecular biology of phytopathogens, was in fact P. wasabiae SCC3193. This event was a milestone in the research of P. wasabiae and triggered reclassification events in all international collections. Several reports confirmed the presence of P. wasabiae in Finland, France, Germany, Norway, Poland, Scotland, Spain, Switzerland, USA, Canada, Turkey, Malaysia and South Africa (de Boer et al., 2012; Dung et al., 2012; Ngadze et al., 2012; Nykyri et al., 2012; Moleleki et al., 2013; Waleron et al., 2013; Werra et al., 2015; Ozturk et al., 2016; Rosenzweig et al., 2016; Dees et al., 2017; Suárez et al., 2017; Zoledowska et al., 2018). On the basis of additional studies and analysis of recA gene sequences, scientists concluded that P. carotovorum subsp. carotovorum strains indicated recA PCR-RFLP profile 3 (Waleron et al., 2002) and vPcc (Haan et al., 2008) belong to P. wasabiae (Slawiak et al., 2013). The presence of P. wasabiae was finally confirmed in Europe since the 1960s (Nabhan et al., 2012b; Waleron et al., 2013).

With the development of NGS techniques, Pritchard et al. (2016) suggested division within P. wasabiae on the basis of gANI values. Most recent comprehensive analysis based on DDH, gANI, and ANI values calculated in silico on P. wasabiae genomes has resulted in reclassification of all P. wasabiae potato-originating isolates into a newly established species P. parmentieri (Khayi et al., 2016).

Risk of Introduction

Increased international trade has played a major role in the spread of disease caused by P. parmentieri, while the distribution of seed potato tubers may be the main cause of its spread. There is no information about other plant hosts (particularly ornamentals) for P. parmentieri. There are also risks associated with unidentified pathways of accidental introduction of the organism to new areas.

Host Plants and Other Plants Affected

Growth Stages

Symptoms

Symptoms only appear on potato plants. Latent infection is common on potato tubers.

Potato blackleg mainly occurs from plants derived from latently infected seed potatoes. It is more severe when host resistance is impaired. Pathogenesis of P. parmentieri is also temperature dependent. Potato stem diseases generally develop under wet and partially aerobic conditions. Blackleg develops as a consequence of pathogen multiplication in rotting (or latently infected) mother tubers. Infection of seed tubers or stem invasion by P. parmentieri soon after emergence can result in blanking (rotting and death of the whole plant). Stunting, chlorosis and wilting symptoms, caused by restriction of water flow in the xylem vessels following infection, tend to develop at that stage under dry conditions (Pérombelon, 2002).

Potato soft rot during storage is usually a consequence of latent infection of potato crops. The bacteria are sited intracellularly, in lenticels and in wounds, typically beyond the phylloderm layer. Symptoms of soft rot exhibit as tissue maceration with intact skin of potato. A characteristic odor occurs when additional bacteria are present in infected tissue (Perombelon and Kelman, 1980; Pérombelon, 2000).

List of Symptoms/Signs

Biology and Ecology

Genetics

The genome of Pectobacterium parmentieri SCC3193 consists of a single, circular chromosome of 5.16 Mbp, with an overall G+C content of 50%, without any plasmids. The chromosomal genome contains 4,705 predicted protein-coding sequences, 76 tRNA genes, 7 rRNA operons, and 2 CRISPR loci. On the basis of the orthologous grouping, 772 (16%) of the SCC3193 CDSs have no detectable homologs in any of the complete Pectobacterium or Dickeya proteomes published to date (Koskinen et al., 2012). There is a high variability in genome sequence among P. parmentieri strains when genomic fingerprinting using repetitive sequences-based PCR are applied (Versalovic et al., 1994). They exhibited in at least 5 REP-PCR genomic profiles (Zoledowska et al., 2018).  In Poland, profile I (also characteristic for P. parmentieri SCC3193 isolated in Finland) is the most abundant (approx. 44% of isolated strains). The recA gene-based phylogenetic analysis divided P. parmentieri strains isolated in different countries into two distinct clades. Evaluation of the phenotypic traits such as: pectinase, cellulase and protease activities, siderophore production in addition to potato tissue maceration, swimming and swarming motility also indicated significant differences among the characterized strains (Zoledowska et al., 2018). Genomic overview of type strain of P. parmentieri 08.42.1A (CFBP 8475^T) indicated horizontal acquisition of quorum sensing genes (Khayi et al., 2015).

Physiology and phenology

P. parmentieri strains produce acids from (+)-raffinose, α-d(+)-α-lactose, d(+)-galactose and (+)-melibiose but not from methyl α-d-glycopyranoside, (+)-maltose or malonic acid. They are pectinolytic, form cavities on selective CVP medium and can rapidly macerate potato tissue.

Climate

Means of Movement and Dispersal

Natural dispersal

P. parmentieri can be dispersed by water, irrigation and aerosols.

Accidental introduction

P. parmentieri is associated with trade of infected or latently infected seed potatoes.

Seedborne Aspects

Incidence

P. parmentieri has been present on potato in Europe since the 1960s. Data presented by Waleron et al. (2013) and Zoledowska et al. (2018) indicate that it is quite common in Polish seed potato plantations (about 15% of the population of pectinolytic bacteria).

P. parmentieri has been reported in the USA, Canada, Africa and New Zealand (Pitman et al., 2010; de Boer et al., 2012; Ngadze et al., 2012; Moleleki et al., 2013) but no epidemiological data are available.

Effect on seed quality

Plants affected by P. parmentieri show wilting, stunting and chlorosis, also black soft rot at the stem base, extending upwards from the mother tuber. When disease occurs just after emergence, blanking is observed in the field. In low-temperature growing regions, infections often develop  with dark colouring, chlorosis and wilting. As the disease progresses, stems wilt and blackleg symptoms appear. Contamination of foliage can result in aerial stem rot. Infected plants rapidly develop internal stem rotting, but externally the stem base appears healthy. P. parmentieri commonly causes rotting of developing progeny tubers in the field and/or soft rot in storage.

Seed potatoes with soft rot symptoms are not accepted for trading. Latent infections are monitored via isolation of bacteria on selective CVP media (Hélias et al., 2012), Real-Time PCR (Humphris et al., 2015, van der Wolf et al., 2017), PCR with the use of plant homogenates and species specific primers (de Boer et al., 2012; Potrykus et al., 2014). Recently, Cigna et al. (2017) reported the application of the gapA gene sequencing assay for identification of different Dickeya and Pectobacterium species including P. parmentieri.

If pectinolytic bacteria (P. parmentieri) are detected, pre-basic and basic seed potatoes are rejected.

Pathogen transmission

The rise in international trade of seed potatoes has increased the risk of introduction and spread of P. parmentieri. According to Toth et al. (2011) higher risks of introduction arise from more intensive exchange of seed potatoes and the implementation of environmentally friendly methods of biodegradable waste disposal, such as composting and anaerobic digestion. These methods do not involve sterilization, and pectinolytic bacteria such as P. parmentieri can survive these treatments, thus spreading is intensified.

Seed treatments

No effective seed treatments have been described.

Seed health tests

In the majority of countries, seed potato fields are visually inspected for the presence of blackleg. However, the best method for the detection and identification of P. parmentieri is Real-Time PCR with specific primers ( Humphris et al., 2015; van der Wolf et al., 2017) or Multiplex PCR with three pairs of specific primers (simultaneous identification of Pectobacterium atrosepticum, Dickeya spp. and P. carotovorum together with P. parmentieri (Potrykus et al., 2014)), followed by a PCR reaction with primers specific to P. parmentieri (de Boer et al., 2012) performed on stolon ends of potato seed tubers.

Pathway Causes

Pathway Vectors

Plant Trade

Wood Packaging

Economic Impact

There have been no specific studies on the impact of P. parmentieri on economic losses; however losses in European and other countries connected with the appearance of blackleg and seed potato declassification are obvious.

Risk and Impact Factors

• Has high genetic variability

• Host damage
• Increases vulnerability to invasions
• Negatively impacts agriculture
• Damages animal/plant products
• Negatively impacts trade/international relations

• Pest and disease transmission
• Induces hypersensitivity
• Interaction with other invasive species
• Pathogenic
• Rapid growth
• Rooting

• 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

Uses List

General

• Laboratory use
• Research model

Diagnosis

Fields should be inspected by qualified inspectors to select infected plants. Detection and identification of P. parmentieri is performed using molecular diagnostic methods such as Real-Time PCR with specific primers (Humphris et al., 2015; van der Wolf et al., 2017) or Multiplex PCR with three pairs of specific primers (simultaneous identification of P. atrosepticum, Dickeya spp. and P. carotovorum together with P. parmentieri (Potrykus et al., 2014)), followed by a PCR reaction with primers specific to P. parmentieri (de Boer et al., 2012). Cigna et al. (2017) reported application of the gapA gene sequencing assay for identification of P. parmentieri. For a review of detection and identification methods for pectinolytic bacteria, see Czajkowski et al. (2015).

Similarities to Other Species/Conditions

P. parmentieri is a pathogen of potato. It can cause symptoms of blackleg and soft rot that are very similar to those caused by Pectobacterium carotovorum subsp. carotovorum, P. carotovorum subsp. brasiliense,P. atrosepticum, Dickeya solani and D. dianthicola. The best method for identification of P. parmentieri is Real-Time PCR with specific primers (Kim et al., 2012; Humphris et al., 2015; van der Wolf et al., 2017) or Multiplex PCR with three pairs of specific primers (simultaneous identification of P. atrosepticum, Dickeya spp. and P. carotovorum together with P. parmentieri (Potrykus et al., 2014) followed by a PCR reaction with primers specific to P. parmentieri (de Boer et al., 2012).

Prevention and Control

Within the European Community (EC) P. parmentieri is important but is not a quarantine pest. It is controlled in the majority of Member States by their respective potato seed certification schemes. When potato seed production is initiated from pathogen-free microplants/microtubers and field production is limited to a restricted number of generations, the occurrence of P. parmentieri is limited (Toth et al., 2011). Control is based on visual inspection of field crops and tubers. However, latent infections are quite common and cannot be detected using this method. The post-harvest testing of seed potatoes is necessary to monitor seed stocks for the presence of bacteria from genus Pectobacterium and Dickeya (Czajkowski et al., 2011b). Certified pathogen-free seed potatoes should be cultivated. Latently infected seed potatoes should be rejected.

Eradication

There are no commercial methods available for eradication of P. parmentieri.

Recent studies have indicated that P. parmentieri is susceptible to attack from soil saprophytic bacteria and specific bacteriophages (Krzyzanowska et al., 2012; Czajkowski et al., 2011a, b; Smolarska et al., 2018).

Movement control

There are some measures that can reduce the impact and risk of spread of P. parmentieri from latently infected seed potatoes. Cleaning and disinfection of machinery, equipment and grading lines is very important and a range of disinfectants have shown efficacy in suppressing Dickeya solani (Czajkowski et al., 2011b). P. parmentieri has not been reported in waterways. A 3-year survey of Polish waterways did not detect P. parmentieri, however, P. carotovorum was detected.

Biological control

Biological control may be beneficial in reducing the impact of P. parmentieri. Smolarska et al. (2018) described bacteriophages of family Podoviride and order Caudovirales that infect some strains of P. parmentieri but not strains of other species of Pectobacterium and Dickeya. Antagonistic bacteria such as Ochrobactrum A44 and some strains of Pseudomonas sp. can be used to limit the spread of infection by Pectobacetrium and Dickeya (Czajkowski et al., 2011a; Krzyzanowska et al., 2012).

Gaps in Knowledge/Research Needs

Further information is required on the geographical distribution of P. parmentieri. Research is also needed to investigate the survival of P. parmentieri in soil, water and air, its sensitivity to approved pesticides, and effective methods of eradication.

References

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Links to Websites

Organizations

Netherlands: EUPHRESCO ERA- NET, Dr. Jan van der Wolf, PO Box 16 6700AA WAGENINGEN

Principal Source

Draft datasheet under review.

Contributors

27/07/17 Original text by:

Ewa Lojkowska, Intercollegiate Faculty of Biotechnology, Univesity of Gdansk & Medical University of Gdansk, 80-307 Gdansk, Abrahama 58, Poland

Distribution Maps