Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

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Pseudomonas cichorii
(bacterial blight of endive)

Osdaghi E, 2020. Pseudomonas cichorii (bacterial blight of endive). Invasive Species Compendium. Wallingford, UK: CABI. DOI:10.1079/ISC.44942.20210200740

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Pseudomonas cichorii (bacterial blight of endive)

Pictures

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PictureTitleCaptionCopyright
Pseudomonas cichorii (bacterial blight of endive); symptoms on sage (Salvia spp). Virginia, USA.
TitleSymptoms
CaptionPseudomonas cichorii (bacterial blight of endive); symptoms on sage (Salvia spp). Virginia, USA.
Copyright©Mary Ann Hansen/Virginia Polytechnic Institute and State University/Bugwood.org - CC BY 3.0 US
Pseudomonas cichorii (bacterial blight of endive); symptoms on sage (Salvia spp). Virginia, USA.
SymptomsPseudomonas cichorii (bacterial blight of endive); symptoms on sage (Salvia spp). Virginia, USA.©Mary Ann Hansen/Virginia Polytechnic Institute and State University/Bugwood.org - CC BY 3.0 US
Pseudomonas cichorii (bacterial blight of endive); symptoms, showing leaf spot and blight  on tickseed (Coreopsis spp). Virginia, USA.
TitleSymptoms
CaptionPseudomonas cichorii (bacterial blight of endive); symptoms, showing leaf spot and blight on tickseed (Coreopsis spp). Virginia, USA.
Copyright©Mary Ann Hansen/Virginia Polytechnic Institute and State University/Bugwood.org - CC BY 3.0 US
Pseudomonas cichorii (bacterial blight of endive); symptoms, showing leaf spot and blight  on tickseed (Coreopsis spp). Virginia, USA.
SymptomsPseudomonas cichorii (bacterial blight of endive); symptoms, showing leaf spot and blight on tickseed (Coreopsis spp). Virginia, USA.©Mary Ann Hansen/Virginia Polytechnic Institute and State University/Bugwood.org - CC BY 3.0 US

Identity

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Preferred Scientific Name

  • Pseudomonas cichorii (Swingle 1925) Stapp 1928

Preferred Common Name

  • bacterial blight of endive

Other Scientific Names

  • Bacterium cichorii (Swingle) Elliott 1930
  • Bacterium endiviae Kotte 1930
  • Bacterium formosanum Okabe 1935
  • Chlorobacter cichorii (Swingle 1925) Patel & Kulkarni 1951
  • Phytomonas cichorii Swingle 1925
  • Phytomonas endiviae (Kotte) Clara 1934
  • Pseudomonas endiviae Kotte 1930
  • Pseudomonas formosanum (Okabe) Krasil'nikov 1949
  • Pseudomonas papaveris (Takimoto) Okabe & Goto 1955
  • Pseudomonas papaveris Lelliott & Wallace 1955

International Common Names

  • English: bacterial blight of celery; bacterial blight of eggplant; bacterial leaf spot of sweet basil; bacterial leaf spot of tomato; bacterial rot of lettuce; bacterial spot of ornamentals; bacterial: celery blight; bacterial: endive blight; bacterial: ornamentals spot; brown stem of celery; bud blight of chrysanthemum; celery: bacterial blight; celery: brown stem; chrysanthemum: bud blight; chrysanthemum: leaf spot; chrysanthemum: stem necrosis; drippy gill of mushrooms; endive bacterial blight; leaf rot of pepper; leaf spot of stevia; leaf spot of chrysanthemum; leaf spot of Geranium spp.; leaf spot of ornamentals; leaf spot of soybean; leaf spot of vegetables; lettuce varnish spot; midrib rot of lettuce; ornamentals: bacterial spot; varnish spot of lettuce; varnish spot of lettuce
  • Spanish: corazon negro de la endivia; veta negra de la escarola
  • French: coeur noir de la chicoree; graisse du celeri; pourriture bacterienne de la laitue
  • Portuguese: mancha-bacteriana; podridão-das-hastes

Local Common Names

  • Italy: marciume batterico della lattuga

EPPO code

  • PSDMCI (Pseudomonas cichorii)

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Proteobacteria
  •         Class: Gammaproteobacteria
  •             Order: Pseudomonadales
  •                 Family: Pseudomonadaceae
  •                     Genus: Pseudomonas
  •                         Species: Pseudomonas cichorii

Notes on Taxonomy and Nomenclature

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Pseudomonas cichorii was accepted in the Approved Lists of Bacterial Names (Skerman et al., 1980). There have been no revisions of the name since then. Phylogenetic investigations showed that the genus Pseudomonas belongs to the gamma subclass of Proteobacteria (Moore et al., 1996). P. cichorii belongs to the ‘Pseudomonas syringae group’ of the genus using the 16S rRNA sequence analyses (Anzai et al., 2000), while it belongs to the ‘P. syringae subgroup’ of Palleroni rRNA group I based on the rRNA-DNA hybridization analyses (Palleroni, 1984). Recently, multilocus sequence analysis (MLSA) revealed high genetic diversity among the P. cichorii strains isolated from various host plants in different geographical areas. It has been shown that the species consists of a cluster of closely related phylogroups that significantly differ from the type strain in their phenotypic and genotypic characteristics (Trantas et al., 2013; Timilsina et al., 2017).

Description

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P. cichorii is a Gram-negative rod, about 0.8-1.3 µm, with one to several polar flagella. Colonies on nutrient agar are round, white, slightly raised, translucent, with slightly irregular margins; on King's medium B, a fluorescent greenish pigment diffuses into the medium (Bradbury, 1981). Typical differentiative phenotypic characteristics for the identification of P. cichorii based on the LOPAT scheme consisted of negative levan, positive oxidase, negative potato soft rot, negative arginine dihydrolase and positive hypersensitive reaction features (Schaad et al., 2001).

Distribution

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P. cichorii is probably ubiquitous. It causes serious diseases in all regions characterized by mild temperatures and high humidity or in protected environments. It is widespread in France, Germany, Italy, Russia, UK, Japan, Taiwan, South Africa, Tanzania, Barbados, Brazil, Cuba and New Zealand. In the USA, it occurs most frequently in Florida.

Distribution Table

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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.

Last updated: 17 Feb 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

BurundiPresent
EgyptPresent
South AfricaPresent, Widespread
TanzaniaPresent, Widespread

Asia

ChinaPresent
-FujianPresent
-GuangdongPresent
-HainanPresent
-HebeiPresent
-Inner MongoliaPresent
-SichuanPresent
IndiaPresent, Localized
-DelhiPresent
IranPresent
JapanPresent, Widespread
-HokkaidoPresent
-ShikokuPresent
South KoreaPresent
TaiwanPresent, Widespread
TurkeyPresent

Europe

BelgiumPresent
BulgariaPresent
FrancePresent, Widespread
GermanyPresent, Widespread
GreeceAbsent, Intercepted only
-CretePresent
ItalyPresent, Widespread
North MacedoniaPresent
PortugalPresentOriginal citation: Ferreira Pinto & Oliveira, 1993
RussiaPresent, Widespread
SerbiaPresent
Serbia and MontenegroPresent
SpainPresentOriginal citation: Garcia Morato et al., 1984
UkrainePresent
United KingdomPresent, Widespread
-EnglandPresent, Widespread

North America

BarbadosPresent, Widespread
CanadaPresent, Widespread
-AlbertaPresent
-British ColumbiaPresent
-New BrunswickPresent
-Nova ScotiaPresent, Few occurrences
-OntarioPresent
-Prince Edward IslandPresent
-QuebecPresent
-SaskatchewanPresent, Few occurrences
CubaPresent, Widespread
MexicoPresent
Puerto RicoPresent
United StatesPresent, Localized
-AlabamaPresent
-CaliforniaPresent
-FloridaPresent
-GeorgiaPresent
-HawaiiPresent
-IllinoisPresent
-IndianaPresentGreenhouse finding.
-LouisianaPresent
-MississippiPresent
-MontanaPresent
-New JerseyPresent
-New YorkPresent
-North CarolinaPresent
-PennsylvaniaPresent
-TennesseePresent
-WashingtonPresent

Oceania

AustraliaPresent, Localized
-New South WalesPresent
-QueenslandPresent
New CaledoniaPresent
New ZealandPresent, Widespread

South America

ArgentinaPresent
BrazilPresent, Widespread
-BahiaPresent
-Distrito FederalPresent
-Minas GeraisPresent
-ParanaPresent
-Rio de JaneiroPresent
-Rio Grande do SulPresent
-Sao PauloPresent
ChilePresentOriginal citation: Pinto de Torres & Carreno Ibanez, 1983
ColombiaPresent

Risk of Introduction

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P. cichorii is included in the EPPO list of pathogens associated with the import of tomato fruit (EPPO 2015).

Hosts/Species Affected

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P. cichorii has a wide host range and can incite disease in a large number of plant species. Under favourable environmental conditions, the bacterium can cause severe disease in almost all the crops in which it has been described. Some crops have been more widely investigated because of their economic importance and/or the frequent or yearly occurrence of the disease. These hosts include vegetables such as borage (Borago officinalis) (Cambra et al., 2004), celery (Pernezny et al., 1994), endive and lettuce (Grogan et al., 1977); flowering ornamentals such as chrysanthemum (Chrysanthemum x morifolium) (Strider and Jones, 1977; Jones et al., 1983), African daisy (Gerbera jamesonii) (Miller and Knauss, 1973), geranium (Pelargonium spp.) (Engelhard et al., 1983); and foliage ornamentals belonging to the Araceae and Araliaceae (Chase, 1987a). Other hosts from Bradbury (1986) and more recent reports include okra (Mariano et al., 1994), garlic (Stefanova et al., 1992), Peruvian carrot (Arracacia xanthorrhiza) (Beriam et al., 1998), Chinese cabbage (Brassica pekinensis) (Sun et al., 1993), safflower (Carthamus tinctorius) and cornflower (Centaurea cyanus) (Young et al., 1987), Ficus lyrata (Chase 1987b), soyabean (Nishiyama et al., 1986), Hedera helix (Hassanzadeh, 1993), Helianthus (Robbs and Almeida, 1981), Hibiscus helatus (Rodriguez and Hinojosa, 1986), H. rosa-sinensis (Chase, 1986), Hyoscyamus muticus (Sattar et al., 1986), Lagascea mollis (Cruz and Stefanova (1992), Lobelia ricardii (Putnam, 1999), Mentha arvensis (Maia et al., 1996), Musa (Choi et al., 1988), Ocimum basilicum (Miller and Burgess, 1987), Thai basil (Ocimum basilicum var. thyrsiflora) (Luiz et al., 2018), Panax pseudoginseng (Gvozdyak and Pendus, 1988), Phaseolus vulgaris (Cruz and Stefanova, 1992), Plectranthus australis (Miller, 1991), Ranunculus acris (Young et al., 1987), Rhododendron catawbiense (Uddin and McCarter, 1996), turmeric (Curcuma longa) (Maringoni et al., 2003), muskmelon (Cucumis melo), watermelon (Citrullus vulgaris) (Obradovic and Arsenijevic, 2002) and Xanthosoma brasilense (Romeiro et al., 1988).

The experimental host range includes an even larger number of hosts from various botanical families (Bradbury, 1986).

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
Abelmoschus esculentus (okra)MalvaceaeOther
    AgaricusAgaricaceaeOther
      Allium sativum (garlic)LiliaceaeOther
        Apium graveolens (celery)ApiaceaeMain
          Arracacia xanthorrhiza (arracacha)ApiaceaeOther
            Barleria cristata (Philippine violet)AcanthaceaeOther
              Borago officinalis (Borage)BoraginaceaeOther
                Brassica napus var. napus (rape)BrassicaceaeOther
                  Brassica oleracea var. botrytis (cauliflower)BrassicaceaeOther
                    Brassica oleracea var. capitata (cabbage)BrassicaceaeOther
                      Brassica rapa subsp. chinensis (Chinese cabbage)BrassicaceaeOther
                        Brassica rapa subsp. oleifera (turnip rape)BrassicaceaeOther
                          Brassica rapa subsp. pekinensisBrassicaceaeOther
                            Calendula officinalis (Pot marigold)AsteraceaeOther
                              CamelliaTheaceaeOther
                                Capsicum (peppers)SolanaceaeOther
                                  Capsicum annuum (bell pepper)SolanaceaeOther
                                    Carthamus tinctorius (safflower)AsteraceaeOther
                                      Centaurea cyanus (cornflower)AsteraceaeOther
                                        Chrysanthemum (daisy)AsteraceaeMain
                                          Chrysanthemum coronarium (garland chrysanthemum)AsteraceaeMain
                                            Chrysanthemum morifolium (chrysanthemum (florists'))AsteraceaeMain
                                              Chrysanthemum vestitumAsteraceaeMain
                                                Cichorium endivia (endives)AsteraceaeMain
                                                  Cichorium endivia subsp. endivia (endives)AsteraceaeMain
                                                    Cichorium endivia var. crispum (Winter endive)AsteraceaeMain
                                                      Cichorium intybus (chicory)AsteraceaeMain
                                                        Citrullus lanatus (watermelon)CucurbitaceaeOther
                                                          Coffea arabica (arabica coffee)RubiaceaeOther
                                                            Coreopsis lanceolataAsteraceaeOther
                                                              Cucumis melo (melon)CucurbitaceaeOther
                                                                Cucumis sativus (cucumber)CucurbitaceaeOther
                                                                  Cucurbita pepo (marrow)CucurbitaceaeOther
                                                                    CyclamenPrimulaceaeOther
                                                                      Daucus carota (carrot)ApiaceaeOther
                                                                        Duranta erecta (golden dewdrop)VerbenaceaeOther
                                                                          Ficus lyrata (fiddle-leaf fig)MoraceaeOther
                                                                            Gerbera (Barbeton daisy)AsteraceaeMain
                                                                              Gerbera jamesonii (African daisy)AsteraceaeMain
                                                                                Glycine max (soyabean)FabaceaeOther
                                                                                  Hedera helix (ivy)AraliaceaeOther
                                                                                    Helianthus (sunflower)AsteraceaeOther
                                                                                      Hibiscus rosa-sinensis (China-rose)MalvaceaeMain
                                                                                        Hydrangea (hydrangeas)HydrangeaceaeOther
                                                                                          Lactuca sativa (lettuce)AsteraceaeMain
                                                                                            Luffa aegyptiaca (loofah)CucurbitaceaeOther
                                                                                              Magnolia grandiflora (Southern magnolia)MagnoliaceaeOther
                                                                                                Malus domestica (apple)RosaceaeOther
                                                                                                  Mentha arvensis (Corn mint)LamiaceaeOther
                                                                                                    Monstera deliciosa (ceriman)AraceaeOther
                                                                                                      Musa (banana)MusaceaeOther
                                                                                                        Nicotiana tabacum (tobacco)SolanaceaeOther
                                                                                                          Ocimum basilicum (basil)LamiaceaeOther
                                                                                                            Panax ginseng (Asiatic ginseng)AraliaceaeOther
                                                                                                              Papaver nudicaule (Iceland poppy)PapaveraceaeOther
                                                                                                                Papaver orientale (Oriental poppy)PapaveraceaeOther
                                                                                                                  Pelargonium (pelargoniums)GeraniaceaeMain
                                                                                                                    Pernettya mucronata (prickly heath (UK))EricaceaeOther
                                                                                                                      Phaseolus vulgaris (common bean)FabaceaeOther
                                                                                                                        Phlox paniculata (summer perennial phlox)PolemoniaceaeOther
                                                                                                                          Plumeria pudicaApocynaceaeOther
                                                                                                                            Potentilla (Cinquefoil)RosaceaeOther
                                                                                                                              Primula polyanthaPrimulaceaeOther
                                                                                                                                Prunus persica (peach)RosaceaeOther
                                                                                                                                  Pyracantha (Firethorn)RosaceaeOther
                                                                                                                                    Pyrus communis (European pear)RosaceaeOther
                                                                                                                                      Ranunculus acris (Meadow buttercup)RanunculaceaeOther
                                                                                                                                        Rhododendron catawbienseEricaceaeOther
                                                                                                                                          ScindapsusAraceaeOther
                                                                                                                                            Solanum lycopersicum (tomato)SolanaceaeOther
                                                                                                                                              Solanum melongena (aubergine)SolanaceaeOther
                                                                                                                                                SpathiphyllumAraceaeOther
                                                                                                                                                  Stevia rebaudianaAsteraceaeOther
                                                                                                                                                    Triticum aestivum (wheat)PoaceaeOther
                                                                                                                                                      ViburnumCaprifoliaceaeOther
                                                                                                                                                        Vigna angularis (adzuki bean)FabaceaeMain
                                                                                                                                                          Xanthosoma brasiliense (Tahitian spinach)AraceaeOther

                                                                                                                                                            Growth Stages

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                                                                                                                                                            Flowering stage, Fruiting stage, Post-harvest, Seedling stage, Vegetative growing stage

                                                                                                                                                            Symptoms

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                                                                                                                                                            Symptoms caused by P. cichorii may vary depending on the host and the infected part of the plant. Symptoms usually start with the appearance of water-soaked lesions that develop either at the leaf margin, near the midvein and/or are randomly distributed as leaf spots. Developing lesions are roughly circular and are rarely confined to the inter-veinal areas. The lesions enlarge and turn dark brown or black. Lesions are sometimes surrounded by bright yellow halos. Lesions may coalesce to form very large necrotic areas and may affect the whole leaf. In some hosts symptoms may also be present on petioles, pedicels and/or stems (celery, chrysanthemum, coffee, aubergine, geranium and tomato) and flower buds (chrysanthemum, aubergine and geranium). The size of the lesions varies depending on the environmental conditions; in high humidity conditions larger lesions and rotting of infected tissues are observed, whereas in low humidity conditions lesions may only be a few millimetres diameter and the disease may eventually cease development. Abscission of severely infected leaves (dwarf schefflera (Schefflera arboricola), mint, Ficus lyrata and geranium) and, rarely, the death of the plant (ginseng, chrysantemum, celery seedlings and F. lyrata) have also been reported.

                                                                                                                                                            Host-specific symptoms have also been described on a number of plant species. For instance, 'varnish spot of lettuce' affects the blades and petioles of the inner leaves of head lettuce varieties, and is characterized by shiny, dark-brown, necrotic lesions. Lesions range in size from a few millimetres to very large and are not delimited by veins (Grogan et al., 1977). Vein blackening of the outer leaves is possible on lettuce grown in severely infested soils.

                                                                                                                                                            Disease on field-grown lettuce is frequently reported as lettuce rot or varnish spot, while it is called midrib rot when infects greenhouse-grown lettuce plants (Cottyn et al., 2009). In the latter case, symptoms consist of small, brown spots that coalesce and expand into moist, dark brown to greenish black rotted lesions along the midrib of inner head leaves (Cottyn et al., 2011).

                                                                                                                                                            On celery, P. cichorii causes 'bacterial blight' (leaf and petiole lesions) and 'brown stem of celery'. Most of the symptoms occur on leaves. Leaf lesions are at first circular to angular, dark green, water-soaked spots 1-2 mm diameter, while in the large number of spots, the whole leaf becomes chlorotic. Symptoms on stem and petiole appear as elongated, rusty brown lesions 1-2 mm wide by 2-5 mm long (Wilkie and Dye, 1974; Pernezny et al., 1994).

                                                                                                                                                            'Leaf rot of pepper' causes watery spots on the leaves, stem and apical regions resulting in complete decay (Rivera et al., 1981). 'Stem melanosis of spring wheat' is characterized by bleached, empty heads and blackening of the rachis, peduncle and stem immediately beneath the nodes (Piening and McPherson, 1985). Chrysanthemum leaf spot and bud blight (McFadden, 1961) produces symptoms on the leaves, buds or stem. Irregular, dark brown to black necrotic lesions develop on the leaves. The bacterium moves from the leaf through the petiole and causes a dark-brown stem necrosis. Flower buds turn dark brown and die prematurely. On chrysanthemum, P. cichorii causes 'stem necrosis', characterized by dark blue to black, water-soaked lesions along the stem, without lesions on the leaves; severely affected plants may die (Jones et al., 1983). 'Leaf spot of geranium' (Engelhard et al., 1983) causes irregularly-shaped, water-soaked spots that become dark brown to black. Yellowing of adjacent tissues invariably occurs a few days after the lesion appears and infected leaves die. Flower buds turn black and fail to open and the necrosis extends down the peduncle. Basal rot of geranium cuttings has been reported as softening and blackening of stems. The leaf margins of affected cuttings develop chlorosis and wilting symptoms (Semer and Raju, 1984).

                                                                                                                                                            On gerbera (Miller and Knauss, 1973), circular to irregular, brownish-black spots with or without a concentric ring are usually observed. The lesions extending from the margins become narrow as they reach the midvein. On Hibiscus rosa-sinensis, symptoms consist of tan spots with purple or black margins (Chase, 1986). The disease is called pith necrosis on tomato when infects the inner parts of the stems. Initial symptoms of pith necrosis consist of yellowing and wilting of young leaves, while serious infection can lead to dark green to dark brown, irregular blotches on the leaf blades and elongated streaks along the stem (Wilkie and Dye, 1974). Longitudinal cut of the symptomatic stems will reveal extensive discoloration of the centre of the stem (pith). Infected stems may crack or collapse due to the destruction of the tissues (Trantas et al., 2013).

                                                                                                                                                            On Mentha arvensis, small, water-soaked, yellow spots on the leaf edges are observed, which cause leaf abscission at the advanced stages of disease. On ginseng, small, dark-brown spots on the central vein of the leaf that spread across the surface, while leaves lose turgor and wilt. On F. lyrata (Chase, 1987b), angular, black lesions with purplish margins on leaves, frequently initiated at the junction of the blade and petiole, expanding along the veins into the leaf blade. The leaves may abscise and, in severe cases, the stem rots and the plant dies. On nectarines, gummy and corky spots on fruits are observed (Pinto de Torres and Carreno Ibanez, 1983). A disease of mushrooms called oozing gills and brown blotch, which is similar to drippy gill caused by Pseudomonas agarici, is caused by strains with biochemical characteristics similar to P. cichorii (Bateson et al., 1972). P. cichorii has been also isolated from rots of bananas, carrot, cauliflower, lettuce, in mixed infections with other pseudomonads and/or Pectobacterium species. P. cichorii is associated with the postharvest bacterial rot of lettuce together with other fluorescent pseudomonads.

                                                                                                                                                            List of Symptoms/Signs

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                                                                                                                                                            SignLife StagesType
                                                                                                                                                            Inflorescence / blight; necrosis
                                                                                                                                                            Leaves / abnormal colours
                                                                                                                                                            Leaves / abnormal leaf fall
                                                                                                                                                            Leaves / necrotic areas
                                                                                                                                                            Stems / discoloration of bark
                                                                                                                                                            Stems / internal discoloration
                                                                                                                                                            Whole plant / plant dead; dieback

                                                                                                                                                            Biology and Ecology

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                                                                                                                                                            Until recently, the genomic data of P. cichorii has rarely been available (Ramkumar et al. 2015), hence, most of the pathogen-plant interaction mechanisms remain undetermined. P. cichorii has a broad host range and low host specificity. Under favourable environmental conditions, this constitutes a high potential for the development of epidemics. Infection occurs through stomata or wounds. Wounding is not required for infection of most hosts when plants are subject to high levels of free moisture, such as under misting, while inoculum of P. cichorii is present. Under environmental conditions that favour the pathogen, lettuce may be infected through epidermal hairs (Shirata et al., 1982). Wounds caused by the feeding and oviposition of Lyriomiza trifolii provide entry sites for P. cichorii in chrysanthemum (Matteoni and Broadbent, 1988). The bacterium multiplies in the intercellular spaces of the epidermis and then colonizes the intercellular spaces of the mesophyll (Hikichi et al., 1996a). Browning of the tissue develops after bacterial multiplication. Extracts of a phytotoxin, isolated from several P. cichorii strains and partially characterized (Hu et al., 1998), has been shown to induce lesions when injected into lettuce tissues, similar to those induced by the bacterium, and may be responsible for disease symptoms (Shirakawa et al., 1998).

                                                                                                                                                            Huang et al. (2015) showed that P. cichorii strain SF1-54 causing lettuce midrib rot disease, produces seven bioactive compounds with biosurfactant properties among which two phytotoxic compounds 'cichopeptin A and B' contribute to virulence of the pathogen on lettuce. Although the cipA-mutant strain (lacking cichopeptin A and B) exhibited significantly less virulence and rotten midribs than the wild type strain, the two strains showed the same level of leaf multiplication on lettuce (Huang et al., 2015). Furthermore, it has been shown that the gene hrpW is involved in the virulence of P. cichorii and it contributes in the induction of hypersensitivity reaction in tobacco (Kajihara et al., 2012). On the other hand, it has been shown that induction of apoptotic cell death by P. cichorii within the infected lettuce tissues initiates the development of rotting symptoms on the plant (Kiba et al., 2006).

                                                                                                                                                            Periods of high humidity and leaf wetness are necessary for infection and disease development. The longer the period of moisture the greater is the incidence of the disease (Jones et al., 1984). Lesions cease to expand in low moisture conditions. Thus, plants grown in polyethylene-covered greenhouses or tunnels, in nurseries as well as plants subjected to rainfall or sprinkle-irrigation tend to develop the most severe symptoms. The greenhouse is an ideal environment for disease development because of the dense plant canopy and high humidity.

                                                                                                                                                            Disease develops over a wide temperature range, while the optimum temperature is 20-28°C. At higher temperatures, lesion expansion declines and ceases at temperatures above 36°C (Jones et al., 1984).

                                                                                                                                                            Experiments on the effect of host nutrition showed that high fertilizer application, stimulating rapid and succulent plant growth, results in an increased number of lesions after inoculation with P. cichorii (Jones et al., 1984). Contrasting results have been obtained on dwarf schefflera (Schefflera arboricola) (Chase, 1987a). Different host species (chrysanthemum, lettuce and coffee) are known to carry epiphytic populations of P. cichorii. On lettuce, the bacterial population increased on the outer and head leaves in the early and middle stages of head formation, respectively (Hikichi et al., 1996b). The bacterium may also be present in apparently healthy chrysanthemum buds (Jones et al., 1990). It has been shown that infections occur only when the pathogen reaches populations on leaves that are greater than 100,000 CFU/g of fresh weight (Hikichi, 1996b). Disease incidence is also correlated with the population level of the bacterium on lettuce leaves (Hikichi et al., 1996b).

                                                                                                                                                            P. cichorii can survive in soil for short periods, while it survives for up to 6 months in buried infected debris, but this is not the case under conditions where they are subject to rapid decay (Ohata et al., 1982; Bazzi et al., 1984). The bacterium is frequently associated with other fluorescent pseudomonads in soils and in the rhizosphere of vegetables and weeds (Grogan et al., 1977). It has also been isolated from dried, diseased lettuce leaves that had overwintered for 4 months in a vinyl house, from rotted leaves of Senecio vulgaris and Capsella bursa-pastoris growing in lettuce fields affected by the disease and from their root surfaces, and from those of lettuce and Artemisia princeps (Ohata et al., 1982). P. cichorii which survives within an infected field is able to colonize new plants in the following year. Populations of the pathogen may be present but the disease does not always occur unless environmental conditions favour bacterial multiplication in the host. The bacterium has been isolated from artificially inoculated seeds stored at 23 and 5°C after 50 and 93 days, respectively.

                                                                                                                                                            Climate

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                                                                                                                                                            ClimateStatusDescriptionRemark
                                                                                                                                                            A - Tropical/Megathermal climate Average temp. of coolest month > 18°C, > 1500mm precipitation annually
                                                                                                                                                            C - Temperate/Mesothermal climate Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C
                                                                                                                                                            Cf - Warm temperate climate, wet all year Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year

                                                                                                                                                            Air Temperature

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                                                                                                                                                            Parameter Lower limit Upper limit
                                                                                                                                                            Mean annual temperature (ºC) 20 28

                                                                                                                                                            Means of Movement and Dispersal

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                                                                                                                                                            Natural Dispersal

                                                                                                                                                            Splashing water (rain, sprinkler irrigation, water dripping from the roof of greenhouses, etc.) results in dispersal of P. cichorii within the crop, from soil to plant or from plant to plant. It is likely that this pathogen can be dispersed between adjacent crops by aerosols. The very wide host range of P. cichorii suggests that there may exist many weed plants that act as alternative hosts. Prevention of infection of crops when adjacent plants are hosts to the pathogen may be impossible.

                                                                                                                                                            Vector Transmission

                                                                                                                                                            Adults of Liriomyza trifolii are able to acquire and transmit P. cichorii from infected to non-infected chrysanthemums (Broadbent and Matteoni, 1991).

                                                                                                                                                            Seedborne Spread

                                                                                                                                                            P. cichorii has been shown to survive on artificially inoculated lettuce seeds (Ohata et al., 1982). Many authors have reported P. cichorii as seed transmitted but, despite field observation of early infections in the crop and in the nursery that support this suggestion, there is no experimental data on transmission by seed.

                                                                                                                                                            Agricultural Practices

                                                                                                                                                            Sprinkler irrigation provides dispersal of inoculum within the crop.

                                                                                                                                                            Movement in Trade

                                                                                                                                                            The exchange of propagative material can distribute P. cichorii over long distances as the bacterium may be carried in commodities either in tissue lesions (symptomatic plants) or epiphytically on asymptomatic plants.

                                                                                                                                                            Pathway Causes

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                                                                                                                                                            CauseNotesLong DistanceLocalReferences
                                                                                                                                                            Botanical gardens and zoos Yes Yes
                                                                                                                                                            Breeding and propagation Yes Yes
                                                                                                                                                            Crop production Yes Yes
                                                                                                                                                            Cut flower trade Yes Yes
                                                                                                                                                            Food Yes Yes
                                                                                                                                                            Horticulture Yes Yes
                                                                                                                                                            Seed trade Yes Yes

                                                                                                                                                            Pathway Vectors

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                                                                                                                                                            VectorNotesLong DistanceLocalReferences
                                                                                                                                                            Host and vector organisms Yes Yes
                                                                                                                                                            Plants or parts of plants Yes Yes

                                                                                                                                                            Plant Trade

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                                                                                                                                                            Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
                                                                                                                                                            Flowers/Inflorescences/Cones/Calyx Yes Yes Pest or symptoms usually invisible
                                                                                                                                                            Fruits (inc. pods) Yes Yes Pest or symptoms usually invisible
                                                                                                                                                            Leaves Yes Yes Pest or symptoms usually invisible
                                                                                                                                                            Roots Yes Pest or symptoms usually invisible
                                                                                                                                                            Seedlings/Micropropagated plants Yes Yes Pest or symptoms usually invisible
                                                                                                                                                            Stems (above ground)/Shoots/Trunks/Branches Yes Yes Pest or symptoms usually invisible
                                                                                                                                                            Plant parts not known to carry the pest in trade/transport
                                                                                                                                                            Bulbs/Tubers/Corms/Rhizomes

                                                                                                                                                            Impact Summary

                                                                                                                                                            Top of page
                                                                                                                                                            CategoryImpact
                                                                                                                                                            Cultural/amenity Negative
                                                                                                                                                            Economic/livelihood Negative

                                                                                                                                                            Impact

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                                                                                                                                                            Under environmental conditions favourable to the pathogen, diseases incited by P. cichorii cause severe damage to the host and can result in outbreaks. Outbreaks in the nursery or in the field during warm winters in Florida, USA, can lead to widespread disease affecting thousands of plants (Jones et al., 1983; Chase and Brunk, 1984; Uddin and McCarter, 1996). Diseases caused by P. cichorii can appear sporadically over a number of years then cause severe outbreaks such as the outbreak of 'varnish spot of lettuce' in California (Grogan et al. 1977) and 'brown stem of celery' in Florida, USA (Pernezny et al., 1994). Severe disease outbreaks on lettuce leading to losses of up to 100% have been reported in California (Grogan et al., 1977), Italy (Bazzi and Mazzucchi, 1979) and Portugal (Ferreira-Pinto and Oliveira, 1993). In Italy and France, P. cichorii is a recurring problem on endive and lettuce (Allex and Rat 1990; D'Ascenzo et al., 1997). In Florida, brown stem of chrysanthemum only occurs about every 5 to 6 years whereas leaf spot occurs annually (Pernezny et al., 1994).

                                                                                                                                                            Risk and Impact Factors

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                                                                                                                                                            Invasiveness
                                                                                                                                                            • Invasive in its native range
                                                                                                                                                            • Has a broad native range
                                                                                                                                                            • Abundant in its native range
                                                                                                                                                            • Fast growing
                                                                                                                                                            • Has high reproductive potential
                                                                                                                                                            • Reproduces asexually
                                                                                                                                                            • Has high genetic variability
                                                                                                                                                            Impact outcomes
                                                                                                                                                            • Host damage
                                                                                                                                                            • Negatively impacts agriculture
                                                                                                                                                            • Negatively impacts trade/international relations
                                                                                                                                                            Impact mechanisms
                                                                                                                                                            • Pathogenic
                                                                                                                                                            Likelihood of entry/control
                                                                                                                                                            • Highly likely to be transported internationally accidentally
                                                                                                                                                            • Highly likely to be transported internationally deliberately
                                                                                                                                                            • Difficult to identify/detect as a commodity contaminant
                                                                                                                                                            • Difficult to identify/detect in the field
                                                                                                                                                            • Difficult/costly to control

                                                                                                                                                            Uses List

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                                                                                                                                                            General

                                                                                                                                                            • Laboratory use

                                                                                                                                                            Diagnosis

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                                                                                                                                                            Isolation is made from early infection stages, small pieces of tissue being excised from the margins preferably of the youngest lesions. These are comminuted in small quantities of sterile water and streaked on plates of surface-dried King's medium B and incubated at 25-27°C for 2 days. The development of largely unmixed colonies, green fluorescent under UV light, is a good indication that the pathogen has been isolated. Single colonies are sub-cultured onto nutrient agar for storage and confirmation of the identity of the pathogen using LOPAT tests (Lelliott and Stead, 1987; Schaad et al., 2001). Presumptive diagnosis of the pathogen can be made if green fluorescent bacteria with the LOPAT Group III characteristics are obtained (being levan negative, oxidase positive, potato rot negative, arginine dihydrolase negative, hypersensitivity on tobacco positive). However, variable results for the LOPAT scheme were reported for the Pseudomonas strains designated as P. cichorii (Aysan et al., 2003; Cottyn et al., 2009). Culturally, P. cichorii most resembles the common plant saprophytes, P. fluorescens and P. putida. These are distinguished from P. cichorii because they are positive in the test for arginine dihydrolase and negative in the test for tobacco hypersensitivity. Further biochemical analysis can be performed according to Schaad et al. (2001) or by mean of galleries for biochemical characterization and identification. Pathogenicity tests could be performed on the host of isolation and preferably on one known host (e.g., lettuce or chrysanthemum). A bacterial suspension of no more than 10,000,000 CFU/ml is sprayed on plants until run off. Wounding is not necessary for leaf infection but high humidity levels (for example, enclosing plants in polyethylene bags) are essential until 24 h post inoculation. The plants are incubated at 26°C, being maintained for 3 days after inoculation in high humidity conditions, either by being enclosed with a polythene bag or, preferably, held in a mist cabinet. Plants may also be inoculated on stems using a needle laden with inoculum.

                                                                                                                                                            Two semi-selective media containing fungal and bacterial inhibitors have been developed for ecological studies on P. cichorii (Jones et al., 1990).

                                                                                                                                                            An ELISA procedure has been evaluated to detect P. cichorii in lettuce leaves (Ogiso et al., 1997). Polyclonal antibodies are commercially available for the identification of P. cichorii by immunofluorescence and ELISA. Any unusual report or diagnosis on plants or plant parts moving in trade should be confirmed by a pathogenicity test. Highly specific and sensitive molecular probes based on unique DNA sequences obtained by DNA subtraction methods can readily be developed to confirm the identity of the pathogen including strains obtained from symptomless plants. These methods are only used when a high level of confidence in identification is necessary to support eradication programmes or quarantine restrictions that may involve compensation.

                                                                                                                                                            Recently, a sensitive real‐time PCR assay was developed for the specific detection of P. cichorii using a Taqman Minor Groove Binding probe based on a 90‐bp amplicon from the pathogenicity gene cluster hrcRST. The method was shown to be capable of detecting 1 CFU/mL of irrigation water, which is well below the concentration needed for lettuce midrib rot infection in commercial lettuce greenhouses (Cottyn et al., 2011).

                                                                                                                                                            Detection and Inspection

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                                                                                                                                                            Inspect the plants or plant parts (e.g. cuttings) for the presence of leaf and/or stem lesions. Water-soaked lesions and bright-yellow halos at the margin of the lesions are indicative of P. cichorii. Symptoms on lettuce in the field are not always visible because the bacterium infects the inner leaves of mature heads but are evident when the heads are cut open (Grogan et al., 1977). Diseased specimens must be collected and analysed for the presence of the bacterium by isolation in culture and confirmation of identity.

                                                                                                                                                            Similarities to Other Species/Conditions

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                                                                                                                                                            Symptoms induced by P. cichorii can be confused with those caused by other bacterial pathogens that cause leaf spot or blight on vegetables and ornamentals. In tomato for instance, initial field symptoms caused by P. cichorii could be confused with the symptoms caused by P. syringae pv. tomato, P. corrugata as well as the leaf spot pathogen Xanthomonas euvesicatoria (Jones et al., 2016). In the laboratory, fluorescence of colonies on King's B medium restricts the investigation to fluorescent pseudomonads that can be identified by LOPAT tests (see Diagnosis).

                                                                                                                                                            Prevention and Control

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                                                                                                                                                            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.

                                                                                                                                                            Control of disease caused by P. cichorii is difficult to achieve when conditions favour the pathogen. For greenhouse operations, the ability to regulate free water on plant surfaces offers some chance of success. Soil irrigation, rather than overhead watering, will reduce the likelihood of infection and disease development (Pauwelyn et al., 2011). Greenhouse ventilation is beneficial. Planting material should be from sources free of the pathogen. Plants with symptoms should be isolated if of high value, or discarded. The spread of the bacterium may be reduced by decontaminating tools and hands after handling diseased plants. High plant densities and over-fertilization, especially with nitrogen fertilizers, should be avoided. Inoculum in the field may be reduced by ploughing, removing and burning infected plant debris, removing weeds near growing areas. Different cultivar susceptibility has been observed in chrysanthemum (Strider and Jones, 1986), basil (Holcomb and Cox, 1998), endive, lettuce and chicory (Matta and Garibaldi, 1970). Chemical control using copper compounds or antibiotics has been demonstrated in trials, but success in commercial practice, especially in the field, is problematic. Spray costs and the variability of efficacy may mean that applications are often not cost effective.

                                                                                                                                                            Furthermore, resistance to streptomycin and copper-based chemicals was reported within the P. cichorii strains isolated from celery seedbeds in Florida, USA.

                                                                                                                                                            It has been shown that tomato seedlings inoculated with P. cichorii strain JBC1 and exposed to green or red light showed a significant reduction in disease incidence compared to the seedlings grown under white light or dark conditions. Inoculated seedlings grown under green or red light showed significant up-regulation in the defense-related genes, phenylalanine ammonia-lyase (PAL) and pathogenesis-related protein 1a (PR-1a) (Nagendran and Lee, 2015). Furthermore, Rajalingam and Lee (2018) showed that the expression of genes involved in the production of phytotoxic lipopeptides and siderophores were significantly decreased under green light in comparison to the dark conditions.

                                                                                                                                                            References

                                                                                                                                                            Top of page

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                                                                                                                                                            Contributors

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                                                                                                                                                            16/03/20 Reviewed by:

                                                                                                                                                            Ebrahim Osdaghi, Department of Plant Protection, College of Agriculture, Bajgah, Shiraz University, 71441-65186, Shiraz, Iran.

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