Dickeya Plant Pathogens

Abstract

Bacteria of the genus Dickeya are phytopathogens characterised by a wide host range and large geographical distribution. The disease is named soft rot because the plant material is liquefied by bacterial enzymes. The massive production of pectate lyases is typical of Dickeya. Secretion by a specialised system named Out enables the export of pectinases that cause soft rot by cleaving pectin present in plant cell walls. The 10 species of the genus Dickeya were isolated from diseased plants or water. They attack a variety of crops and ornamental plants in tropical, subtropical and temperate climates. Dickeya solani and Dickeya dianthicola are the two main species responsible for potato diseases, leading to significant economic losses. Recent diseases on fruit trees are also due to Dickeya. These bacteria have developed different mechanisms to cope with adverse conditions and compete with other microorganisms. In addition, they use a complex regulatory network to adjust the production of pectate lyases during the successive phases of plant infection.

Key Concepts

  • Dickeya members are plant pathogens characterised by a broad‐host range and a large geographical distribution.
  • The genus Dickeya is subdivided into ten species, seven acting as phytopathogens and three found in water.
  • Dickeya species are ‘brute force’ pathogens as they use a set of plant cell wall degrading enzymes as their primary weapon.
  • Massive production of pectate lyases and accessory pectinases is the main virulence signature of the Dickeya species; they cause the symptom of rotting of the plant tissues.
  • Since antibiotics are not allowed in agriculture, there is currently no effective chemical control for Dickeya.
  • Dickeya has developed mechanisms to compete with other microorganisms and to cope with stressful conditions found in the environment or during plant colonisation.
  • The infectious process begins with an asymptomatic phase, corresponding to the asymptomatic presence of Dickeya in plant tissues, followed by the symptomatic phase corresponding to soft‐rot appearance.
  • The disease appears when environmental parameters, mainly temperatures and humidity, become favourable.
  • During the plant infection, the expression of pectate lyase genes is finely controlled by a complex regulatory network.
  • Besides pectate lyase secretion, many other functions favour the bacterial virulence, such as protein secretion systems, motility, chemotaxis, iron capture and envelope components.

Keywords: plant pathology; enterobacteria; phytopathogen; soft‐rot; pectinase; protein secretion; virulence regulation

Figure 1. Soft‐rot symptoms caused by Dickeya. Examples of maceration caused by D. dadantii on (a) chicory, (b) sweet potato, (c) potato and (d) the model plant Arabidopsis thaliana.
Figure 2. Dickeya in the environment. Dickeya species are found in a variety of environmental niches such as plants, water, insects and slugs.
Figure 3. The action of Dickeya pectinases. The linear regions of pectin are composed of long chains of polygalacturonate partially methylated at C6 carboxyl and acetylated at C2 or C3 hydroxyls. Pectin acetylesterase (PaeY) and methylesterase (PemA) pectin eliminate acetyl and methyl groups. Endo‐polygalacturonases (Peh) and endo‐pectate lyases (Pel) cleave the glycosidic bonds by either hydrolysis or β‐elimination, respectively. The generated oligogalacturonides cross the outer membrane via the specific porins KdgM and KdgN. In the periplasm, remaining esterifications are eliminated by PemB and PaeX and oligogalacturonides are further cleaved by the exo‐pectate lyase PelX and exo‐polygalacturonases PehV, PehW and PehX. The resulting dimers and trimers pass the inner membrane via the transporters TogMNAB and TogT. In the cytoplasm, they are cleaved by the exo‐pectate lyase PelW and oligogalacturonate lyase Ogl into saturated and unsaturated monomers which are further metabolised to KDG, the inducer of the pectin degradation regulator KdgR.
Figure 4. Regulation of pectate lyase genes during the Dickeya – plant interaction. The major actors controlling the pel gene expression during Dickeya infection are shown. The transcriptional activator CRP ensures a coupling of virulence and sugar metabolism. After the preferential utilisation of energetic sugars, the accumulation of cAMP activates CRP, allowing the activation of pel gene transcription. The transcriptional regulator PecS and the nucleoid‐associated protein FIS repress virulence factors that must be restrained in early infection stages. The repression exerted by KdgR is linked to pectin presence, as the inducer KDG formed during pectin degradation inactivates this transcriptional regulator. VfmE is the regulator associated to a quorum sensing regulation specific of the genus Dickeya. The PecT repression is exerted only at high temperature. The activation by GacA is linked to a post‐transcriptional regulation. The RNA‐binding protein RsmA binds directly to pel mRNAs, leading to their degradation. The regulatory RNA RsmB, whose production is increased by GacA, is able to sequester RsmA, avoiding pel mRNA degradation.
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Further Reading

Charkowski AO (2018) The changing face of bacterial soft‐rot diseases. Annual Review of Phytopathology 56: 269–288.

Leonard S, Hommais F, Nasser W and Reverchon S (2017) Plant‐phytopathogen interactions: bacterial responses to environmental and plant stimuli. Environmental Microbiology 19 (5): 1689–1716.

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Toth IK, Pritchard L and Birch PR (2006) Comparative genomics reveals what makes an enterobacterial plant pathogen. Annual Review of Phytopathology 44: 305–336.

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Hugouvieux‐Cotte‐Pattat, Nicole, Condemine, Guy, Gueguen, Erwan, and Shevchik, Vladimir E(Mar 2020) Dickeya Plant Pathogens. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028932]