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Candidatus Phytoplasma ulmi
(elm yellows)

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Datasheet

Candidatus Phytoplasma ulmi (elm yellows)

Summary

  • Last modified
  • 05 June 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Candidatus Phytoplasma ulmi
  • Preferred Common Name
  • elm yellows
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Firmicutes
  •     Class: Mollicutes
  •       Order: Acholeplasmatales
  •         Family: Acholeplasmataceae
  • Summary of Invasiveness
  • Elm yellows develops in sporadic epidemics after introduction of 'Ca. Phytoplasma ulmi' to areas where vectors are abundant.

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Pictures

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PictureTitleCaptionCopyright
Candidatus Phytoplasma ulmi (elm yellows); yellowing foliage of Ulmus rubra.
TitleSymptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); yellowing foliage of Ulmus rubra.
Copyright©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); yellowing foliage of Ulmus rubra.
SymptomsCandidatus Phytoplasma ulmi (elm yellows); yellowing foliage of Ulmus rubra.©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); Epinasty on Ulmus americana leaves caused by elm phloem necrosis phytoplasma; healthy (left) and diseased (right) branches, showing epinasty of leaves.
TitleEarly foliar symptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); Epinasty on Ulmus americana leaves caused by elm phloem necrosis phytoplasma; healthy (left) and diseased (right) branches, showing epinasty of leaves.
Copyright©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); Epinasty on Ulmus americana leaves caused by elm phloem necrosis phytoplasma; healthy (left) and diseased (right) branches, showing epinasty of leaves.
Early foliar symptomsCandidatus Phytoplasma ulmi (elm yellows); Epinasty on Ulmus americana leaves caused by elm phloem necrosis phytoplasma; healthy (left) and diseased (right) branches, showing epinasty of leaves.©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); symptoms in field on Ulmus americana.
TitleSymptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); symptoms in field on Ulmus americana.
Copyright©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); symptoms in field on Ulmus americana.
SymptomsCandidatus Phytoplasma ulmi (elm yellows); symptoms in field on Ulmus americana.©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); phloem necrosis on Ulmus americana.
TitleSymptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); phloem necrosis on Ulmus americana.
Copyright©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); phloem necrosis on Ulmus americana.
SymptomsCandidatus Phytoplasma ulmi (elm yellows); phloem necrosis on Ulmus americana.©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); phloem necrosis on Ulmus americana.
TitleSymptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); phloem necrosis on Ulmus americana.
Copyright©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); phloem necrosis on Ulmus americana.
SymptomsCandidatus Phytoplasma ulmi (elm yellows); phloem necrosis on Ulmus americana.©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); Phloem discoloration in Ulmus americana caused by elm phloem necrosis phytoplasma infection; healthy (top) and diseased (bottom).
TitleStem symptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); Phloem discoloration in Ulmus americana caused by elm phloem necrosis phytoplasma infection; healthy (top) and diseased (bottom).
Copyright©Wayne A. Sinclair, Cornell University/via Bugwood.org - CC BY-NC 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); Phloem discoloration in Ulmus americana caused by elm phloem necrosis phytoplasma infection; healthy (top) and diseased (bottom).
Stem symptomsCandidatus Phytoplasma ulmi (elm yellows); Phloem discoloration in Ulmus americana caused by elm phloem necrosis phytoplasma infection; healthy (top) and diseased (bottom).©Wayne A. Sinclair, Cornell University/via Bugwood.org - CC BY-NC 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); Foliar symptoms on Ulmus spp.
TitleFoliar symptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); Foliar symptoms on Ulmus spp.
Copyright©Pennsylvania Department of Conservation and Natural Resources - Forestry/via Bugwood.org - CC BY 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); Foliar symptoms on Ulmus spp.
Foliar symptomsCandidatus Phytoplasma ulmi (elm yellows); Foliar symptoms on Ulmus spp.©Pennsylvania Department of Conservation and Natural Resources - Forestry/via Bugwood.org - CC BY 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); Field symptoms on Ulmus spp.
TitleField symptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); Field symptoms on Ulmus spp.
Copyright©Pennsylvania Department of Conservation and Natural Resources - Forestry/via Bugwood.org - CC BY 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); Field symptoms on Ulmus spp.
Field symptomsCandidatus Phytoplasma ulmi (elm yellows); Field symptoms on Ulmus spp.©Pennsylvania Department of Conservation and Natural Resources - Forestry/via Bugwood.org - CC BY 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); brooms growing on Ulmus parvifolia.
TitleSymptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); brooms growing on Ulmus parvifolia.
Copyright©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); brooms growing on Ulmus parvifolia.
SymptomsCandidatus Phytoplasma ulmi (elm yellows); brooms growing on Ulmus parvifolia.©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); rootlet necrosis on Ulmus americana.
TitleSymptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); rootlet necrosis on Ulmus americana.
Copyright©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); rootlet necrosis on Ulmus americana.
SymptomsCandidatus Phytoplasma ulmi (elm yellows); rootlet necrosis on Ulmus americana.©Dept. of Plant Pathology/Cornell University, Ithaca, New York
Candidatus Phytoplasma ulmi (elm yellows); Phloem discoloration on Ulmus spp.
TitleSymptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); Phloem discoloration on Ulmus spp.
Copyright©Pennsylvania Department of Conservation and Natural Resources - Forestry/via Bugwood.org - CC BY 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); Phloem discoloration on Ulmus spp.
SymptomsCandidatus Phytoplasma ulmi (elm yellows); Phloem discoloration on Ulmus spp.©Pennsylvania Department of Conservation and Natural Resources - Forestry/via Bugwood.org - CC BY 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); Elm phloem necrosis, stem symptoms.
TitleStem symptoms
CaptionCandidatus Phytoplasma ulmi (elm yellows); Elm phloem necrosis, stem symptoms.
Copyright©USDA Forest Service - Region 8 - Southern, USDA Forest Service/via Bugwood.org - CC BY 3.0 US
Candidatus Phytoplasma ulmi (elm yellows); Elm phloem necrosis, stem symptoms.
Stem symptomsCandidatus Phytoplasma ulmi (elm yellows); Elm phloem necrosis, stem symptoms.©USDA Forest Service - Region 8 - Southern, USDA Forest Service/via Bugwood.org - CC BY 3.0 US

Identity

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Preferred Scientific Name

  • Candidatus Phytoplasma ulmi Lee, Martini, Marcone & Zhu

Preferred Common Name

  • elm yellows

Other Scientific Names

  • elm yellows phytoplasma
  • Phytoplasma ulmi

International Common Names

  • English: elm phloem necrosis; elm witches'-broom; little leaf and bunchy top of Tossa jute; phloem necrosis of elm; rose balsam phyllody
  • French: nécrose du liber de l'orme
  • Portuguese: fitoplasma dos amarelos do ulmeiro

EPPO code

  • PHYPUL

Summary of Invasiveness

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Elm yellows develops in sporadic epidemics after introduction of 'Ca. Phytoplasma ulmi' to areas where vectors are abundant.

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Firmicutes
  •         Class: Mollicutes
  •             Order: Acholeplasmatales
  •                 Family: Acholeplasmataceae
  •                     Genus: Phytoplasma
  •                         Species: Candidatus Phytoplasma ulmi

Notes on Taxonomy and Nomenclature

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Elm yellows phytoplasmas belong to a phylogenetically discrete group of plant- and insect-inhabiting wall-less, pleomorphic bacteria, unculturable heretofore, that are provisionally classified as a genus, 'Candidatus Phytoplasma,' in the class Mollicutes (Firrao et al., 2004). Infrageneric classification is based primarily on nucleotide sequences in the 16S rRNA genes and secondarily on other molecular and biological criteria. Numerous taxa, classified in more than 30 groups (Zhao and Davis, 2016) have been delineated within 'Ca. Phytoplasma’. The so-called elm yellows group, also designated as 16S rRNA group V, or 16SrV, comprises several subgroups of which only one (subgroup A, or 16SrV-A) is associated with a disease syndrome in elms. This taxon is provisionally named 'Ca. Phytoplasma ulmi' (Lee et al., 2004). Phytoplasmas assignable to this taxon have been detected in elms and/or leafhoppers in multiple localities in France (Mäurer et al., 1993; Boudon-Padieu et al., 2004), Italy (Lee et al., 1993; Marcone et al., 1997; Mittempergher, 2000; Carraro et al., 2004) and the USA (Lee et al., 1993; Griffiths et al., 1999). Many references to the elm yellows group of phytoplasmas sensu lato are not specifically relevant to 'Ca. Phytoplasma ulmi' or to the disease elm yellows.

Ca. Phytoplasma trifolii’-related strains of the clover proliferation group (16S rRNA group VI, subgroup C; Hiruki and Wang, 2004) were found associated with an elm yellows outbreak in Ulmus americana that began near Chicago, Illinois, USA in the 1990s (Jacobs et al., 2003). 'Ca. Phytoplasma ulmi' was not found in the affected trees. Thus, elm yellows can be caused by either of two phytoplasmas. This datasheet focuses only on diseases associated with 'Ca. Phytoplasma ulmi' infection.

Distribution

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In Europe, elm yellows disease incidences have been reported most often from Italy. The disease has occurred in scattered localities in France and Germany as well as in former Czechoslovakia. This disease is relatively unimportant in Europe (Mittempergher, 2000) but devastating outbreaks have occurred in native elms in the USA (Swingle, 1942; Carter and Carter, 1974; Sinclair, 2000). In the USA, elm yellows has occurred in eastern and central parts of the country from approximately 32 to 46°N (latitude) and from 71 to 97°W (longitude). It has been suggested that 'Ca. Phytoplasma ulmi' may be native to Europe and was introduced into the USA, causing damage in the intolerant North American elms beginning in the 1880s (Garman, 1893; Sinclair, 2000).

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: 10 Jan 2020
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Europe

CzechiaPresent, Localized
FrancePresent, Localized
GermanyPresent, Localized
ItalyPresent, Widespread
SerbiaPresent, Few occurrences
United KingdomAbsent, Formerly presentFound on elm trees imported from Italy. Plants destroyed. No further reports.

North America

CanadaPresent, LocalizedIntroducedFirst reported: 1983 or earlier
-OntarioPresent, LocalizedIntroducedFirst reported: 1983 or earlier
United StatesPresent, WidespreadIntroducedInvasiveFirst reported: 1880s or earlier
-AlabamaPresent, LocalizedIntroduced
-ArkansasPresent, LocalizedIntroduced
-GeorgiaPresent, LocalizedIntroduced
-IllinoisPresent, WidespreadIntroducedInvasive
-IndianaPresent, WidespreadIntroducedInvasive
-IowaPresent, LocalizedIntroduced
-KansasPresent, LocalizedIntroduced
-KentuckyPresent, WidespreadIntroducedInvasive
-MarylandPresent, LocalizedIntroducedOriginal citation: USDA Forest Service (1999)
-MassachusettsPresent, LocalizedIntroduced
-MichiganPresent, LocalizedIntroduced
-MinnesotaPresent, LocalizedIntroduced
-MississippiPresent, LocalizedIntroduced
-MissouriPresent, WidespreadIntroducedInvasive
-MontanaPresent
-NebraskaPresent, LocalizedIntroduced
-New JerseyPresent, LocalizedIntroduced
-New YorkPresent, WidespreadIntroducedInvasive
-North DakotaPresent, LocalizedIntroduced
-OhioPresent, WidespreadIntroducedInvasive
-OklahomaPresent, LocalizedIntroduced
-PennsylvaniaPresent, WidespreadIntroduced
-TennesseePresent, WidespreadIntroducedInvasive
-VirginiaPresent, LocalizedIntroducedOriginal citation: USDA Forest Service (1999)
-West VirginiaPresent, LocalizedIntroducedInvasive

Risk of Introduction

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Ca. Phytoplasma ulmi’ (under the name elm phloem necrosis phytoplasma) is regulated by the European Union (EU, 2000) and by other EPPO countries (Turkey). 'Elm phloem necrosis phytoplasma' also appears on a list of recommended quarantine pests for southern Africa. Biological variability among strains of 'Ca. Phytoplasma ulmi' is undetermined, but variability in DNA sequences has been detected in both European and North American populations (Lee et al., 1993; Griffiths et al., 1999; Boudon-Padieu et al., 2004). Severe epidemics have occurred in the USA and Italy, but elm yellows has not caused much damage in France, which is the only other country where it is known to occur commonly up to 2006. As American elms are not often planted in Europe or Asia, the main risk there is to native Ulmus spp., some of which are quite susceptible (Mittempergher, 2000).

Elm hybrids bred for resistance to fungal diseases caused by Ophiostoma spp. involve Ulmus parents from all regions across Eurasia. Tolerance of such elm hybrids to elm yellows remains to be determined, but experience in Italy indicated it would largely reflect that of the parents, with Ulmus parvifolia, U. villosa and U. wallichiana in particular, exhibiting intolerance to infection (Mittempergher, 2000). Sinclair et al. (2000) reported that five out of six Eurasian cultivars showed symptoms (suppressed growth, size reduction of apical shoots and leaves, chlorosis or reddening, witches' broom, dieback) after graft-inoculation with an American strain of 'Ca. Phytoplasma ulmi.' Clones of U. americana selected for resistance to Ophiostoma spp. are very intolerant of elm yellows (Sinclair et al., 2001).

Phytosanitary Measures

EPPO recommends prohibition of import of elm plants from infested countries (OEPP/EPPO, 1990). If material is imported with a permit, it would be advisable to fumigate it, or treat it with insecticide, to destroy eggs and other stages of vectors. An adequate quarantine period (at least 12 months) for all elms and molecular testing of elm species known to be tolerant of elm yellows phytoplasmas would safeguard against the introduction of phytoplasmas with the elm material.

Hosts/Species Affected

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In addition to the hosts listed, other species in Ulmus are probably susceptible. Non-Ulmus hosts probably occur, as other phytoplasmas have been detected in plants that are not their usual hosts. For further information on hosts, see Mittempergher (2000) and Sinclair (2000).

Experimental Host Range

'Ca. Phytoplasma ulmi' is graft- and vector-transmissible (Baker, 1949, 1951; Braun and Sinclair, 1979; Sinclair et al., 2000; Carraro et al., 2004), although interspecies incompatibility is sometimes a problem in grafting. Symptoms appear 3-12 months after graft-inoculation, usually after inoculated plants have undergone dormancy. The only non-elm plant to which the phytoplasma has been transmitted is Catharanthus roseus, effected using Cuscuta epithymum (Braun and Sinclair, 1979).

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
Ulmus alata (Winged elm)UlmaceaeWild host
Ulmus americana (American elm)UlmaceaeWild host
Ulmus chenmouiUlmaceaeWild host
Ulmus crassifolia (Cedar elm)UlmaceaeWild host
Ulmus davidiana (japanese elm)UlmaceaeWild host
Ulmus glabra (mountain elm)UlmaceaeWild host
Ulmus laciniataUlmaceaeWild host
Ulmus laevis (Russian white elm)UlmaceaeWild host
Ulmus minor (European field elm)UlmaceaeWild host
Ulmus parvifolia (lacebark elm)UlmaceaeWild host
Ulmus pumila (dwarf elm)UlmaceaeWild host
Ulmus rubra (slippery elm)UlmaceaeWild host
Ulmus serotina (red elm)UlmaceaeWild host
Ulmus villosaUlmaceaeWild host
Ulmus wallichianaUlmaceaeWild host

Growth Stages

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Vegetative growing stage

Symptoms

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Symptoms in Eurasian elm species

Tolerant Ulmus spp. (European and Asian species), naturally infected or graft-inoculated, produce witches' brooms (at branch tips and/or along branches) and grow slowly or decline, but phloem necrosis does not develop. Foliage and twigs may be undersized or dwarfed, and foliar yellowing and/or reddening are common. Symptoms may develop on scattered branches (with progressively shorter internodes) or entire plants. Epinasty often accompanies yellowing, and yellow leaves tend to drop prematurely. Several Eurasian elm species and hybrids were found to be susceptible to North American strains of 'Ca. Phytoplasma ulmi' when inoculated by grafting (Braun and Sinclair, 1979; Sinclair et al., 2000), but natural infection of an Eurasian species in North America is recorded only for Ulmus parvifolia (Lee et al., 1993). For more symptomology, see Marcone et al. (1994), Mittempergher (2000), Sinclair (1981, 2000) and Swingle (1942).

Symptoms in North American elms that develop phloem necrosis

Rootlet necrosis and phloem necrosis in roots usually precede foliar symptoms. Fibrous roots and then larger roots die. Hyperplasia, hypertrophy and discoloration may be evident in the phloem of roots and the lower parts of trunks. Current year's phloem becomes yellow to butterscotch before turning brown. The first foliar symptoms usually appear from mid-July to mid-September in the northern USA and include yellowing, epinasty (drooping or downward bending of turgid leaves) and premature casting. Usually, all branches show symptoms at once, but sometimes yellowing begins on one branch. Both yellow and green leaves may occur on a single small branch, but more often all leaves on a branch have the same yellowish-green to yellow colour. Trees visibly affected in June-July usually die during the same year or in the year following first symptoms. Large trees and those somewhat tolerant of infection (notably Ulmus rubra but also U. americana) sometimes decline over several years. U. rubra may display chlorotic undersized foliage and witches'-brooms near branch tips.

Foliar symptoms that first appear after midsummer resemble those or normal leaf senescence and are indistinguishable from symptoms caused by water stress. Trees with late-season symptoms may fail to produce leaves the next spring or may produce dwarfed leaves that wilt or turn yellow and drop. If leaves develop normally on a tree that had symptoms in the previous year, rapid wilting and death may occur in late spring or summer. Shrivelled brown leaves may adhere for several weeks.

Phloem discoloration accompanies and may precede foliar symptoms but does not extend into branches far above ground. In large stems, the discoloration tends to occur in vertical bands with diffuse margins, associated with the positions of buttress roots. The cambial region and the surface of the wood may also be discoloured but the abnormal colour does not extend more than about 1 mm into the wood. If dark discoloration of the outer wood is seen, in addition to phloem discoloration, this may indicate that the tree is infected by both Ophiostomanovo-ulmi and a phytoplasma. Oxidative browning of freshly exposed inner phloem is much more rapid in infected than in healthy trees.

List of Symptoms/Signs

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SignLife StagesType
Leaves / abnormal forms
Leaves / abnormal leaf fall
Leaves / wilting
Leaves / yellowed or dead
Roots / reduced root system
Stems / internal discoloration
Stems / witches broom
Whole plant / early senescence
Whole plant / plant dead; dieback

Biology and Ecology

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In northern Italy the leafhopper Macropsis mendax is a vector of elm yellows (Carraro et al., 2004), and additional insect species that are known vectors of other phytoplasmas have been trapped on elms (Pavan, 2000). The cercopid Philaenus spumarius and the cicadellid Allygus atomarius, implicated as possible secondary vectors in the USA (Matteoni and Sinclair, 1988), have also been trapped on elms in Italy (Pavan, 2000).

In North America the only confirmed vector of an elm yellows phytoplasma is the cicadellid leafhopper Scaphoideus luteolus (Baker, 1948, 1949). Other vectors may exist, since many species of leafhoppers and planthoppers in genera that include phytoplasma vectors have been found on elms (Gibson, 1973; Bentz and Townsend, 2005). S. luteolus was sought without success in an elm yellows outbreak area in New York State (Lanier et al., 1988; Matteoni and Sinclair, 1988). Single transmissions of elm yellows were recorded for the Allygus atomarius and Philaenus spumarius in cage tests (Matteoni and Sinclair, 1988), but vector roles of these insects are unproven. Elm yellows phytoplasmas may also be transmitted by root grafts and bark patch grafts (Swingle, 1938; Sinclair et al., 2000, 2001).

Epidemics in North America occur where annual minimum temperatures are above -23°C, but the disease has been found in scattered localities where average temperatures fall below -26°C. Epidemics, although spectacularly destructive, are usually localized, and spread into contiguous localities is neither quick nor certain. In the state of New York, USA, observations suggested an annual rate of spread of 5-8 km in some places and disappearance in others. The disease may persist at a low level for many years between epidemics. Within an affected tree, phytoplasmas can be visualized by electron microscopy in phloem sieve tubes, where they induce callose deposition and (in species subject to phloem necrosis) collapse of sieve tubes and companion cells (Braun and Sinclair, 1976). Phytoplasmal DNA can be detected in all organs (Lee et al., 1993; Bertelli et al., 2002); leaf midribs are preferred for molecular diagnosis. Phytoplasmas are thought to overwinter in uncollapsed sieve elements (in the roots of plants in which above-ground sieve tubes collapse in winter) and then move throughout a tree after new phloem develops in spring (Braun and Sinclair, 1976). Similar behaviour has been documented for fruit-tree-infecting phytoplasmas (Seemüller et al., 1984).

Means of Movement and Dispersal

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Vector transmission

Elm yellows phytoplasmas are dispersed primarily by their insect hosts, in which they are presumed to reproduce, as demonstrated for other phytoplasmas. Nymphs and adults of vector species can transmit phytoplasmas; the adults are more important because they fly. Instances of elm yellows in single trees far from the main range of the disease in the USA (e.g., in Massachusetts (Holmes and Chater, 1977) and North Dakota (Stack and Freeman, 1988) are presumed to result from long-distance transport of vectors by wind. Vector species include the cicadellid leafhoppers Macropsis mendax in Italy (Carraro et al., 2004) and Scaphoideus luteolus in the USA (Baker, 1948, 1949). Additional vectors probably occur, as elm yellows phytoplasmas have been detected in several species of leafhoppers and planthoppers (Boudon-Padieu et al., 2004).

The vector Scaphoideus luteolus can only transmit locally, and the disease has a restricted distribution within the USA. No instance of human transport of elm yellows phytoplasmas in commerce is known. Infected plants or vegetative propagules of Ulmus can theoretically carry elm yellows phytoplasmas in international trade. Infected plants would not have symptoms while dormant or during the incubation period of the disease, and symptoms remain mild in some tolerant elms. There is a slight possibility that infective vector nymphs or adults could accompany plants in foliage. Eggs are more likely to be carried. Transovarial transmission of a phytoplasma of the aster yellows group has been demonstrated (Alma et al., 1997) but is untested for vectors of elm yellows phytoplasmas. Elm seeds can harbour elm yellows phytoplasmas (Bertelli et al., 2002), but seedlings grown from diseased seeds remained healthy, and no anecdotal reports of apparent seed transmission have appeared.

Plant Trade

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

Wood Packaging

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Wood Packaging not known to carry the pest in trade/transport
Loose wood packing material
Non-wood
Processed or treated wood
Solid wood packing material with bark
Solid wood packing material without bark

Vectors and Intermediate Hosts

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VectorSourceReferenceGroupDistribution
Macropsis mendaxCarraro et al. (2004)InsectItaly
Scaphoideus luteolusBaker (1948)InsectUSA

Impact Summary

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CategoryImpact
Animal/plant collections None
Animal/plant products None
Biodiversity (generally) None
Crop production None
Environment (generally) Negative
Fisheries / aquaculture None
Forestry production None
Human health None
Livestock production None
Native fauna None
Native flora Negative
Rare/protected species None
Tourism None
Trade/international relations None
Transport/travel None

Impact

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Elm yellows has little economic impact in Europe. It is prominent only in parts of Italy. In the USA, it has killed hundreds of thousands of elm trees from the Great Plains eastward to New York and south to Mississippi (Swingle, 1942; Sinclair, 2000), but its impact is overshadowed by that of Dutch elm disease (e.g., Carter and Carter, 1974). Several devastating epidemics of elm yellows occurred in Midwestern states in the 1930s and 1940s before Dutch elm disease occurred there. A 10-year study in New York State (Lanier et al., 1988) showed that elm yellows can cause the failure of Dutch elm disease suppression programmes. In recent decades, elm yellows epidemics have occurred in parts of Mississippi, New Jersey, New York, Pennsylvania, and the region around the northern Shenandoah Valley, comprising parts of Maryland, Virginia and West Virginia (Sinclair, 2000; USDA Forest Service, 1999). In New York State, Ulmus americana clones selected for resistance to Ophiostoma spp. have been killed by elm yellows after being planted to replace trees lost to Dutch elm disease. It should be noted that, based on the instance in Arlington Heights, Illinois, USA, elm yellows disease could also be induced by infection of ‘Ca. Phytoplasma trifolii’ (Jacobs et al., 2003), a pathogen that is dealt with in a separate datasheet.

Diagnosis

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Specific diagnosis of 'Ca. Phytoplasma ulmi' requires analysis of the 16S rRNA gene sequence after amplification of a suitable DNA fragment by polymerase chain reaction (PCR). Because these phytoplasmas, and others that may yet be detected in elms, differ in 16S rDNA sequence, diagnosis should begin with nonspecific phytoplasma detection (e.g. see Ferrini et al., 2004; Jarausch et al., 2001). This is accomplished by amplification of a fragment of the 16S rRNA genes using so-called universal primers that bind to 16S rDNA of any phytoplasma but not to that of other prokaryotes (Lee et al., 1998). Nested PCR reactions are often needed to detect low concentrations of phytoplasma DNA. The analysis can then be completed by direct sequencing or by restriction fragment length profile (RFLP) analysis (Griffiths et al., 1999; Marcone et al., 1997; Sinclair, 2000).

Detection and Inspection

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In elms of Eurasian species, look for foliar discoloration and growth abnormalities as described above. Witches'-brooms are diagnostic, so far as is known. If molecular diagnosis is needed, collect living leaves for DNA extraction from midribs.

In North American elms, look for foliar yellowing and sparse foliage, usually involving all branches. If yellowing is present, then remove a sample of the inner bark including the cambial region from the lower trunk or buttress area. The cambial face of the sample, if the bark is still alive and the tree has elm yellows, should have yellow to butterscotch or brown discoloration. For U. americana, U. alata, U. crassifolia or U. serotina, put a fresh sample of living discoloured inner bark into a small closed container for a few minutes; then open and sniff. If the sample is moist, wintergreen odour (methyl salicylate) can be detected (Swingle, 1942). Ulmus rubra does not produce the wintergreen odour, and the reaction of U. thomasii to elm yellows infection is unknown. Foliar yellowing accompanied by phloem discoloration (and wintergreen odour in some species) is diagnostic. Ophiostoma spp. can also cause yellow discoloration of the inner phloem surface, but no wintergreen odour comes from that discoloration. If molecular diagnosis is needed, collect living leaves for DNA extraction from midribs.

Similarities to Other Species/Conditions

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Phytoplasmas of the elm yellows group sensu lato (16S rRNA group V) affect various plants in Europe, Asia, and North America (Alnus, Apocynum, Celtis, Eucalyptus, Lycopersicon, Olea, Parthenocissus, Prunus, Rubus, Spartium, Ulmus, Vitis and Ziziphus) and tend to be named (at least provisionally) for the host plants in which they are found. Ribosomal RNA and ribosomal protein gene sequences, other molecular data, and vector relationships for some strains, indicate that those from different host genera are distinct from one another (Lee et al., 2004). Phytoplasmas of more than one group (e.g., group V and group I, the aster yellows group, in Italy, or group VI and group I in Illinois, USA) have sometimes been detected in elms using nested PCR techniques, but no symptoms have been consistently associated with phytoplasmas other than 'Ca. Phytoplasma ulmi' or the Illinois elm yellows phytoplasma (Lee et al., 1995; Jacobs et al., 2003).

Some symptoms of elm yellows in North American elms can be confused with those of Dutch elm disease (DED). In Ulmus americana, foliar yellowing caused by elm yellows phytoplasmas sometimes begins on one limb, as does yellowing in DED. Young U. americana and U. rubra dying of elm yellows sometimes wilt and die suddenly. This wilting can be confused with that due to DED. Both diseases sometimes develop in the same tree.

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.

There is no practical method for prevention or cure. However, tolerant Ulmus species and cultivars are available. Tolerant species include Ulmus glabra, U. laevis, U. macrocarpa, U. minor, U. pumila and U. wilsoniana (Mittempergher, 2000). Tolerant or resistant cultivars include 'Frontier' (Townsend et al., 1991a), 'Homestead' (Townsend and Masters, 1984) and 'Prospector' (Townsend et al., 1991b). The severity of symptoms in elms that are somewhat tolerant is related to their size when first infected, small trees developing more severe symptoms (Mittempergher, 2000). For more information, see Mittempergher (2000) and Sinclair et al. (2000).

References

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Alma A, Bosco D, Danielli A, Bertaccini A, Vibio M, Arzone A, 1997. Identification of phytoplasmas in eggs, nymphs and adults of Scaphoideus titanus Ball reared on healthy plants. Insect Molecular Biology, 6(2):115-121; 32 ref

Baker WL, 1948. Transmission by leafhoppers of the virus causing phloem necrosis of American elm. Science, 108:307-308

Baker WL, 1949. Studies on the transmission of the virus causing phloem necrosis of American elm with notes on the biology of its insect vector. Journal of Economic Entomology, 42:729-732

Baker WL, May C, 1951. Phloem necrosis of elm. Plants and Gardens, 7:129-130

Barnett DE, 1977. A revision of the nearctic species of the genus Scaphoideus (Homoptera: Cicadellidae). Transactions of the American Entomological Society, 102:485-593

Bentz JA, Townsend AM, 2005. Variation in leafhopper species abundance and diversity among elm seedlings and cultivars. HortScience, 40:1389-1393

Bertelli E, Tegli S, Sfalanga A, Surico G, 2002. Detection of phytoplasmal DNA in flowers and seeds from elm trees infected with Elm Yellows. Phytopathologia Mediterranea, 41(3):259-265; 27 ref

Bojansky V, 1969. Elm witches’-brooms - a new disease in Czechoslovakia. Proceedings of the 6th Conference of the Czechoslovak Plant Virologists, Olomouc, 1967:211-213

Bojansky V, Uzanova J, 1973. Morphological and histological changes caused by elm witches’-broom virus. Proceedings of the 7th Conference of the Czechoslovak Plant Virologists, High Tatras, 1971:177-183

Boudon-Padieu E, Larrue J, Clair D, Hourdel J, Jeanneau A, Sforza R, Collin E, 2004. Detection and prophylaxis of elm yellows phytoplasma in France. Investigacion Agraria Sistemas y Recursos Forestales, 13:71-80

Braun EJ, Sinclair WA, 1976. Histopathology of phloem necrosis in Ulmus americana. Phytopathology, 66(5):598-607

Braun EJ, Sinclair WA, 1979. Phloem necrosis of elms: symptoms and histopathological observations in tolerant hosts. Phytopathology, 69(4):354-358

Bretz TW, 1944. Phloem necrosis of elms in Missouri. Plant Disease Reporter, 28:929-931

Bretz TW, Swingle RU, 1946. Known distribution of phloem necrosis of the American elm. Plant Disease Reporter, 30:156-159

Carraro L, Ferrini F, Ermacora P, Loi N, Martin M, Osler R, 2004. Macropsis mendax as a vector of elm yellows phytoplasma of Ulmus species. Plant Pathology, 53(1):90-95

Carter JC, Carter LR, 1974. An urban epiphytotic of phloem necrosis and Dutch elm diseases, 1944-1972. Bulletin of the Illinois State Natural History Survey, 31:113-143

Ciferri R, 1961. Le virosi di piante varie: forestali e da frutto. Agricoltura, 10:48-52

Conti M, D'Agostino G, Mittembergher L, 1987. A recent epiphytotic of elm yellows in Italy. Proceedings of the 7th Congress of the Mediterranean Phytopathological Union. Granada, Spain: Consejeria de Agricultura y Pesca de la Junta de Andalucia, 208-209

Curl EA, Hyche LL, Marshall NL, 1959. An outbreak of phloem necrosis in Alabama. Plant Disease Reporter, 43:1245-1246

Dorst HE, Davis EW, 1937. Tracing long-distance movements of beet leafhopper in the desert. Journal of Economic Entomology, 30:948-954

EPPO, 1990. Specific quarantine requirements. EPPO Technical Documents, No. 1008. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2013. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

EU, 2000. Council Directive 2000/29/EC of 8 July 2000 on protective measures against the introduction into the Member States of organisms harmful to plant or plant products. Official Journal of the European Communities, No L169, 1-112

Ferrini F, Ermacora P, Marin C, Carraro L, 2004. Occurrence, spread and epidemiology of elm yellows in the Friuli Venezia Giulia. Notiziario-ERSA, 17(1):12-15

Firrao G, et al. [26 authors], 2004. ’Candidatus Phytoplasma’, a taxon for the wall-less, non-helical prokaryotes that colonize plant phloem and insects. International Journal of Systematic and Evolutionary Microbiology, 54:1243-1255

Fletcher J, 1983. Brittle root of horseradish in Illinois and the distribution of Spiroplasma citri in the United States. Phytopathology, 73(2):354-357

Garman H, 1893. The pests of shade and ornamental trees. 1. Kentucky Agricultural Experiment Station Bulletin, 47:88-181

Ghauri MSK, 1983. A case of long-distance dispersal of a leafhopper. In: Knight WJ, Pant NC, Robertson TS, Wilson MR, ed. Proceedings of the 1st International Workshop on Biotaxonomy, Classification and Biology of Leafhoppers and Planthoppers (Auchenorrhyncha) of Economic Importance, London, 4-7 October 1982 Commonwealth Institute of Entomology London UK, 249-255

Gibson LP, 1973. An annotated list of the Cicadellidae and Fulgoridae of elm. Research Paper, Northeastern Forest Experiment Station, USDA Forest Service, No.NE-278:5pp

Gibson LP, 1977. Distribution of elm phloem necrosis in the United States. Plant Disease Reporter, 61(5):402-403

Goidanich G, 1951. Gli scopazzi dell’olmo. Informatore Fitopatologico, 14:8

Griffiths HM, Sinclair WA, Boudon-Padieu E, Daire X, Lee IM, Sfalanga A, Bertaccini A, 1999. Phytoplasmas associated with elm yellows: molecular variability and differentiation from related organisms. Plant Disease, 83(12):1101-1104; 24 ref

Gualaccini F, 1963. Primi risultati di esperienze su scopazzi, foglie ad imbuto ed altre anomalie dell’olmo campestre (Ulmus campestris L.). Bolletino della Stazione di Patologia Vegetale di Roma, 21:25-44

Hart JH, 1978. Occurrence of elm phloem necrosis in Michigan. Plant Disease Reporter, 62(10):872-873

Hiruki C, Wang K, 2004. Clover proliferation phytoplasma: ’Candidatus Phytoplasma trifolii’. International Journal of Systematic and Evolutionary Microbiology, 54:1349-1353

Hodgetts J, Flint LJ, Fox A, 2015. First report of 'Candidatus phytoplasma ulmi' (16SrV-A) associated with Ulmus cultivar Morfeo (elm) in the United Kingdom. New Disease Reports, 32:26. http://www.ndrs.org.uk/article.php?id=032026

Holmes FW, Chater CS, 1977. Elm phloem necrosis in Eastern Massachusetts. Plant Disease Reporter, 61(8):626-628

Jacobs KA, Lee IM, Griffiths HM, Miller FDJr, Bottner KD, 2003. A new member of the clover proliferation phytoplasma group (16SrVI) associated with elm yellows in Illinois. Plant Disease, 87(3):241-246; 24 ref

Jarausch W, Jarausch-Wehrheim B, Danet JL, Broquaire JM, Dosba F, Saillard C, Garnier M, 2001. Detection and identification of European stone fruit yellows and other phytoplasmas in wild plants in the surroundings of apricot chlorotic leaf roll-affected orchards in southern France. European Journal of Plant Pathology, 107(2):209-217; 30 ref

Lanier GN, Schubert DC, Manion PD, 1988. Dutch elm disease and elm yellows in central New York: out of the frying pan into the fire. Plant Disease, 72(3):189-194

Larsh HW, 1945. Elm phloem necrosis in Arkansas and Oklahoma. Plant Disease Reporter, 29:699-700

Leach J G, Valleau W D, 1939. Two reports of phloem necrosis of elm. Plant Disease Reporter, 23:300-301

Lee IM, Bertaccini A, Vibio M, Gundersen DE, Davis RE, Mittempergher L, Conti M, Gennari F, 1995. Detection and characterization of phytoplasmas associated with diseases in Ulmus and Rubus in northern and central Italy. Phytopathologia Mediterranea, 34(3):174-183; 25 ref

Lee IM, Davis RE, Sinclair WA, DeWitt ND, Conti M, 1993. Genetic relatedness of mycoplasmalike organisms detected in Ulmus spp. in the United States and Italy by means of DNA probes and polymerase chain reactions. Phytopathology, 83(8):829-833

Lee IM, Martini M, Marcone C, Zhu SF, 2004. Classification of phytoplasma strains in the elm yellows group (16SrV) and proposal of ’Candidatus Phytoplasma ulmi’ for the phytoplasma associated with elm yellows. International Journal of Systematic and Evolutionary Microbiology, 54:337-347

Lee IngMing, Gundersen-Rindal DE, Davis RE, Bartoszyk IM, 1998. Revised classification scheme of phytoplasmas based on RFLP analyses of 16S rRNA and ribosomal protein gene sequences. International Journal of Systematic Bacteriology, 48(4):1153-1169; 145 ref

Livingston JE, 1947. Phloem necrosis of American elm found at in Lincoln, Nebraska. Plant Disease Reporter, 31:328

Marcone C, Ragozzino A, Firrao G, Locci R, 1994. Detection of elm witches' broom agent in Basilicata, Southern Italy. Phytopathologia Mediterranea, 33(3):194-199

Marcone C, Ragozzino A, Seemüller E, 1997. Identification and characterization of the phytoplasma associated with elm yellows in southern Italy and its relatedness to other phytoplasmas of the elm yellows group. European Journal of Forest Pathology, 27(1):45-54

Matteoni JA, Sinclair WA, 1983. Stomatal closure in plants infected with mycoplasmalike organisms. Phytopathology, 73(3):398-402

Matteoni JA, Sinclair WA, 1989. A note on the presence of elm yellows in the Niagara Peninsula. Phytoprotection, 70(3):137-139

Maurer R, Seemuller E, Sinclair WA, 1993. Genetic relatedness of mycoplasmalike organisms affecting elm, alder, and ash in Europe and North America. Phytopathology, 83(9):971-976

Mittempergher L, 2000. Elm yellows in Europe. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 103-120

Murray RGE, Stackebrandt E, 1995. Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. International Journal of Systematic Bacteriology 45:186-187

OEPP/EPPO, 2004. PQR EPPO plant quarantine information retrieval system. Version 4.3. Paris, France: EPPO

Pavan F, 2000. Occurrence on elm and phenology of Auchenorrhyncha potential vectors of the phytoplasma associated with elm yellows disease. Bollettino di Zoologia Agraria e di Bachicoltura, 32(1):59-68; 38 ref

Pisi A, Marani F, Bertaccini A, 1981. Mycoplasma-like organisms associated with elm witches' broom symptoms. Phytopathologia Mediterranea, 20(2/3):189-191

Seemuller E, 1992. Mycoplasma diseases of broadleaved trees in Europe. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes, 44(7):145-148

Seemüller E, Schaper U, Zimbelmann F, 1984. Seasonal variation in the colonisation patterns of mycoplasma-like organisms associated with apple proliferation and pear decline. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz, 91:371-382

Sfalanga A, Martini M, Surico G, Bertaccini A, 2002. Involvement of phytoplasmas in a decline of Ulmus chenmoui in Central Italy. Forest Pathology, 32(4/5):265-275; 30 ref

Sinclair WA, 1972. Phloem necrosis of American and slippery elms in New York. Plant Disease Reporter, 56:159-161

Sinclair WA, 2000. Elm Yellows in North America. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 121-136

Sinclair WA, Braun EJ, Larsen AO, 1976. Update on phloem necrosis of Elms. Journal of Arboriculture, 2(6):106-113

Sinclair WA, Campana RJ, Manion PD, Fry WE, Merrill W, Nichols LP, 1971. Elm phloem necrosis in Pennsylvania. Plant Disease Reporter, 55:1085

Sinclair WA, Filer TH, 1974. Diagnostic features of elm phloem necrosis. Arborist's News, 39:145-149

Sinclair WA, Townsend AM, Griffiths HM, Whitlow TH, 2000. Responses of six Eurasian Ulmus cultivars to a North American elm yellows phytoplasma. Plant Disease, 84(12):1266-1270; 32 ref

Sinclair WA, Townsend AM, Sherald JL, 2001. Elm yellows phytoplasma lethal to Dutch elm disease-resistant Ulmus americana cultivars. Plant Disease, 85(5):560; 4 ref

Slagg CM, 1944. Phloem necrosis found on elm in Kansas. Plant Disease Reporter, 28:1053

Smart CD, Schneider B, Blomquist CL, Guerra LJ, Harrison NA, Ahrens U, Lorenz KH, Seemller E, Kirkpatrick BC, 1996. Phytoplasma-specific PCR primers based on sequences of the 16S-23S rRNA spacer region. Applied and Environmental Microbiology, 62(8):2988-2993; 33 ref

Smith IM, McNamara DG, Scott PR, Holderness M, 1997. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization., Ed. 2:vii + 1425 pp.; many ref

Stack RW, Freeman TP, 1988. First report of elm yellows in North Dakota. Plant Disease, 72(10):912

Swingle RU, 1938. A phloem necrosis of elm. Phytopathology, 28:757-759

Swingle RU, 1942. Phloem necrosis, a virus disease of the American elm. Circular, US Department of Agriculture No. 640

Townsend AM, Masters WO, 1984. ’Homestead’ elm. HortScience, 19:897-898

Townsend AM, Schreiber LR, Masters WO, Bentz SE, 1991. 'Frontier' elm. HortScience, 26(1):80-81; 8 ref

Townsend AM, Schreiber LR, Masters WO, Bentz SE, 1991. 'Prospector' elm. HortScience, 26(1):81-82; 4 ref

USDA Forest Service Northeastern Area State and Private Forestry, 1999. West Virginia Forest Health Highlights-1998. Online at http://www.fs.fed.us/na/morgantown/fhp/fhh/fhh99/wv/wv.htm

Weber PVV, Sinclair WA, Peterson JL, Davis SH Jr, 1974. New in New Jersey: elm phloem necrosis. Plant Disease Reporter, 58(5):387-388

Wilson CL, Seliskar CE, Krause CR, 1972. Mycoplasma-like bodies associated with elm phloem necrosis. Phytopathology, 62:140-143

Zhao Yan, Davis, R. E., 2016. Criteria for phytoplasma 16Sr group/subgroup delineation and the need of a platform for proper registration of new groups and subgroups. International Journal of Systematic and Evolutionary Microbiology, 66(5), 2121-2123. http://ijs.sgmjournals.org

Distribution References

BAKER W L, MAY C, 1951. Phloem necrosis of elm. Plants and Gardens. 129-30.

Bojansky V, 1969. Elm witches'-brooms - a new disease in Czechoslovakia. [Proceedings of the 6th Conference of the Czechoslovak Plant Virologists, Olomouc], 1967 211-213.

Bretz T W , Swingle E U, 1946. Known distribution of phloem necrosis of the American Elm. Plant Disease Reporter. 30 (5), 156-159 pp.

Bretz T W, 1944. Phloem necrosis of Elms in Missouri. Plant Disease Reporter. 28 (30), 929-931 pp.

CABI, Undated. Compendium record. Wallingford, UK: CABI

CABI, Undated a. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

Carter J C, Carter L R, 1974. An urban epiphytotic of phloem necrosis and Dutch elm diseases, 1944-1972. Bulletin, Illinois Natural History Survey. 113-143.

Ciferri R, 1961. (Le virosi di piante varie: forestali e da frutto). In: Agricoltura, 10 48-52.

Conti M, D'Agostino G, Mittembergher L, 1987. A recent epiphytotic of elm yellows in Italy. [Proceedings of the 7th Congress of the Mediterranean Phytopathological Union], Granada, Spain: Consejeria de Agricultura y Pesca de la Junta de Andalucia. 208-209.

Curl EA, Hyche LL, Marshall NL, 1959. An outbreak of phloem necrosis in Alabama. In: Plant Disease Reporter, 43 1245-1246.

EPPO, 2013. PQR database - version 5.0. In: PQR database - version 5.0, Paris, France: European and Mediterranean Plant Protection Organization. unpaginated. http://www.eppo.int/DATABASES/pqr/pqr.htm

Gibson L P, 1977. Distribution of elm phloem necrosis in the United States. Plant Disease Reporter. 61 (5), 402-403.

Goidanich G, 1951. (Gli scopazzi dell'olmo). In: Informatore Fitopatologico, 14 8.

Gualaccini F, 1963. First results of experiments on witches' broom, cowl-forming leaves, and other abnormalities of the English Elm (U. campestris). (Primi risultati di esperienze su scopazzi, foglie ad imbiito ed altre anomalie dell'Olmo Cam pest re (Ulimis campestris L.).). Bollettino della Stazione di Patologia Vegetale. 21 (1), 25-43.

Hart J H, 1978. Occurrence of elm phloem necrosis in Michigan. Plant Disease Reporter. 62 (10), 872-873.

Hodgetts J, Flint L J, Fox A, 2015. First report of 'Candidatus phytoplasma ulmi' (16SrV-A) associated with Ulmus cultivar Morfeo (elm) in the United Kingdom. New Disease Reports. 26. http://www.ndrs.org.uk/article.php?id=032026

Holmes F W, Chater C S, 1977. Elm phloem necrosis in Eastern Massachusetts. Plant Disease Reporter. 61 (8), 626-628.

Larsh H W, 1945. Elm phloem necrosis in Arkansas and Oklahoma. Plant Disease Reporter. 699-700.

Leach J G , Valleau W D, 1939. Two reports on phloem necrosis of Elm. Plant Disease Reporter. 23 (18), 300-301 pp.

Lee I M, Bertaccini A, Vibio M, Gundersen D E, Davis R E, Mittempergher L, Conti M, Gennari F, 1995. Detection and characterization of phytoplasmas associated with diseases in Ulmus and Rubus in northern and central Italy. Phytopathologia Mediterranea. 34 (3), 174-183.

Lee I M, Davis R E, Sinclair W A, DeWitt N D, Conti M, 1993. Genetic relatedness of mycoplasmalike organisms detected in Ulmus spp. in the United States and Italy by means of DNA probes and polymerase chain reactions. Phytopathology. 83 (8), 829-833. DOI:10.1094/Phyto-83-829

Livingston J E, 1947. Phloem necrosis of American elm found at in Lincoln, Nebraska. Plant Disease Reporter. 328.

Marcone C, Ragozzino A, Firrao G, Locci R, 1994. Detection of elm witches' broom agent in Basilicata, Southern Italy. Phytopathologia Mediterranea. 33 (3), 194-199.

Matteoni J A, Sinclair W A, 1989. A note on the presence of elm yellows in the Niagara Peninsula. Phytoprotection. 70 (3), 137-139.

Mittempergher L, 2000. Elm yellows in Europe. In: The elms - Breeding, Conservation and Disease management, [ed. by Dunn CP]. Boston, USA: Kluwer Academic Publishers. 103-120.

Pisi A, Marani F, Bertaccini A, 1981. Mycoplasma-like organisms associated with elm witches' broom symptoms. Phytopathologie Mediterranea. 20 (2/3), 189-191.

Seemüller E, 1992. Mycoplasma diseases of broadleaved trees in Europe. (Laubgehölzmykoplasmosen in Europa.). Nachrichtenblatt des Deutschen Pflanzenschutzdienstes. 44 (7), 145-148.

Sfalanga A, Martini M, Surico G, Bertaccini A, 2002. Involvement of phytoplasmas in a decline of Ulmus chenmoui in Central Italy. Forest Pathology. 32 (4/5), 265-275. DOI:10.1046/j.1439-0329.2002.00290.x

SINCLAIR W A, 1972. Phloem necrosis of American and Slippery Elms in New York. Plant Disease Reporter. 56 (2), 159-161.

Sinclair W A, Campana RJ et al, 1971. Elm phloem necrosis in Pennsylvania. Plant Disease Reporter. 55 (12), 1085.

Sinclair WA, 2000. Elm Yellows in North America. In: The elms - Breeding, Conservation and Disease management, [ed. by Dunn CP]. Boston, USA: Kluwer Academic Publishers. 121-136.

Slagg C M, 1944. Phloem necrosis found on elm in Kansas. Plant Disease Reporter. 1053.

Stack R W, Freeman T P, 1988. First report of elm yellows in North Dakota. Plant Disease. 72 (10), 912. DOI:10.1094/PD-72-0912B

Swingle R U, 1938. A phloem necrosis of Elm. Phytopathology. 28 (10), 757-759 pp.

Swingle R U, 1942. Phloem necrosis, a virus disease of the American elm. In: Circular, US Department of Agriculture,

Weber P V V, Sinclair W A, Peterson J L, Davis S H Jr, 1974. New in New Jersey: elm phloem necrosis. Plant Disease Reporter. 58 (5), 387-388.

Contributors

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03/03/20 Review by:

Yan Zhao, Molecular Plant Pathology Laboratory, Agricultural Research Service-USDA, Beltsville, MD 20705, USA.

Wei Wei, Molecular Plant Pathology Laboratory, Agricultural Research Service-USDA, Beltsville, MD 20705, USA.

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