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Candidatus Phytoplasma phoenicium

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Candidatus Phytoplasma phoenicium

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PictureTitleCaptionCopyright
Candidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: shoot proliferation on the main trunk, with the witches’-broom appearance.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: shoot proliferation on the main trunk, with the witches’-broom appearance.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: shoot proliferation on the main trunk, with the witches’-broom appearance.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: shoot proliferation on the main trunk, with the witches’-broom appearance.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: perpendicular development of auxiliary buds on the branches, with smaller and yellowish leaves.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: perpendicular development of auxiliary buds on the branches, with smaller and yellowish leaves.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: perpendicular development of auxiliary buds on the branches, with smaller and yellowish leaves.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: perpendicular development of auxiliary buds on the branches, with smaller and yellowish leaves.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: general decline of the tree with final dieback.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: general decline of the tree with final dieback.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: general decline of the tree with final dieback.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by AlmWB on almond trees: general decline of the tree with final dieback.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: early flowering and development of all the buds of the infected branches.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: early flowering and development of all the buds of the infected branches.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: early flowering and development of all the buds of the infected branches.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: early flowering and development of all the buds of the infected branches.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: phyllody at the flowering period.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: phyllody at the flowering period.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: phyllody at the flowering period.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: phyllody at the flowering period.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: abnormal fruit development.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: abnormal fruit development.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: abnormal fruit development.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: abnormal fruit development.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: serrate, slim, light green leaves.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: serrate, slim, light green leaves.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: serrate, slim, light green leaves.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: serrate, slim, light green leaves.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: witches’-brooms from the trunk.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: witches’-brooms from the trunk.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: witches’-brooms from the trunk.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: witches’-brooms from the trunk.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: witches’-brooms from the crown.
TitleSymptoms
CaptionCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: witches’-brooms from the crown.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: witches’-brooms from the crown.
SymptomsCandidatus Phytoplasma phoenicium; main symptoms caused by Ca. P. phoenicium on peach and nectarine trees: witches’-brooms from the crown.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy

Identity

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Preferred Scientific Name

  • Candidatus Phytoplasma phoenicium Verdin et al., 2003

Other Scientific Names

  • Phytoplasma phoenicium

International Common Names

  • English: Almond witches’-broom phytoplasma

Summary of Invasiveness

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Phytoplasmas are wall-less parasitic bacteria living exclusively in plant phloem as consequence of transmission by sap-sucking insect vectors (Lee et al., 2000); they have been associated with several hundred plant diseases. ‘Candidatus Phytoplasma phoenicium’ (CaPphoe), subgroup 16SrIX-B, is the aetiological agent of almond witches’-broom (AlmWB), a severe disease affecting almond, peach and nectarine trees in Lebanon and Iran. The first epidemics of AlmWB occurred in almond trees in Lebanon in the early 1990s and in Iran in 1995. In Lebanon, the disease rapidly spread from coastal to high mountainous areas, killing almost 150,000 trees over a period of 15 years. CaPphoe was first added to the EPPO Alert List in 2001 and removed from the list in 2006. The more recent rapid spread of CaPphoe in peach and nectarine orchards and in other plant hosts, along with the identification of efficient insect vectors, increased the alarm about the risk it poses for stone fruit production in the Middle East and in all the countries of the Mediterranean basin. Thus it was re-inserted in the EPPO Alert List in 2015.

Taxonomic Tree

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

Notes on Taxonomy and Nomenclature

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Phytoplasmas are cell-wall-less plant pathogenic bacteria of the class Mollicutes, with a small genome size which ranges from 530 to 1350 kilobases (Marcone, 2014). They have been associated with several hundred diseases affecting economically important crops, such as ornamentals, vegetables, fruit trees and grapevines (Bertaccini et al., 2014). They live in the phloem sieve tubes of their host plants and are transmitted between plants by phloem-sap-feeding leafhoppers, planthoppers or psyllids in a persistent manner (Weintraub and Beanland, 2006).

Based on unique molecular and biological features, phytoplasmas have been classified into 40 species within the provisional genus ‘Candidatus Phytoplasma’ (International Research Programme for Comparative Mycoplasmology Phytoplasma/Spiroplasma Working Team - Phytoplasma Taxonomy Group, 2004; Marcone, 2014); also, taxonomic groupings have been delimited according to the similarity coefficients derived from the comparison of collective restriction profiles of the 16S rRNA gene sequence digested with a selected pool of endonucleases (Lee et al., 1998; Wei et al., 2008; Zhao et al., 2009).

Phytoplasmas of taxonomic group 16SrIX (pigeon pea witches’-broom group) are associated with diseases affecting crop and wild plants in different geographic areas worldwide. Almond witches’-broom disease (AlmWB) is associated with infection by ‘Candidatus Phytoplasma (Ca. P.) phoenicium’, taxonomic subgroup 16SrIX-B (Abou-Jawdah et al., 2002; Verdin et al., 2003; Lee et al., 2012). The reference strain of ‘Ca. P. phoenicium’ (strain A4) is associated with the 16S rRNA gene sequence accession number AF515636, with the unique signature sequence 5’-CCTTTTTCGGAAGGTATG-3’ (Verdin et al., 2003). Other 'Ca. P. phoenicium’ strains, formerly classified in distinct 16SrIX subgroups -F and -G (Molino Lova et al., 2011), are now considered as genetic variants of subgroup 16SrIX-B due to their common biological traits (Casati et al., 2016).

Based on the taxonomic rules, strains can be classified as 'Ca. P. phoenicium' strains if they share with the reference strain of the species (strain A4, accession number AF515636): (i) 16S rDNA sequence identity > 97.5%; (ii) the unique species-specific signature sequence 5’-CCTTTTTCGGAAGGTATG-3’ (Verdin et al., 2003); and (iii) biological features (plant and insect host range) and molecular features (similarity in other genes). Within group 16SrIX, only strains of subgroup 16SrIX-B and its variants (formerly classified in subgroups 16SrIX-D, -F and -G) share all these features with the reference strain; thus, these strains can be defined properly as 'Ca. P. phoenicium' strains. Strains classified in other 16SrIX subgroups share with the 'Ca. P. phoenicium' reference strain A4 only a 16S rDNA sequence identity > 97.5% (i); they do not have an identical signature sequence (ii) or biological/molecular features (iii). For this reason, such strains can be defined as 'Ca. P. phoenicium'-related strains but not as 'Ca. P. phoenicium'.

An AlmWB-like disease reported in Iran (Verdin et al., 2003) was associated with 'Ca. P. phoenicium'-related strains close to those responsible for Knautia arvensis phyllody (KAP), in subgroup 16SrIX-C (Salehi et al., 2006b).

Description

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Phytoplasmas (formerly mycoplasma-like organisms, MLOs) are pleomorphic, cell wall-less bacteria of the class Mollicutes that exist as obligate plant pathogens.

Distribution

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According to the small amount of information available in the scientific literature, almond witches’-broom appeared in Lebanon and Iran at the same time. No information is available on the presence of the disease in any other countries, including the two located between Lebanon and Iran, namely Syria (where almonds are intensively cultivated), and Iraq. However, as underlined by Verdin et al. (2004), the disease might be present and spreading in additional areas of the Middle East.

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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

IranWidespreadIntroduced1995 Invasive Salehi et al., 2006a; Salehi et al., 2006b; Salehi and Izadpanah, 1995; Salehi et al., 2005; Salehi et al., 2011; Pourali and Salehi, 2012; EPPO, 2014; CABI/EPPO, 2015; Salehi et al., 2015
LebanonWidespread Invasive Choueiri et al., 2001; Abou-Jawdah et al., 2002; Abou-Jawdah et al., 2003; Abou-Jawdah et al., 2009; Molino Lova et al., 2011; EPPO, 2014; Molino Lova et al., 2014; CABI/EPPO, 2015

History of Introduction and Spread

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The first epidemic of a lethal devastating almond (Prunus dulcis) disease, named almond witches’-broom (AlmWB), occurred in the south of Lebanon in the early 1990s; it was reported in north Lebanon and in Iran starting in 1995 (Salehi and Izadpanah, 1995; Abou-Jawdah et al., 2002; Molino Lova et al., 2011). During the last two decades, the outbreak of AlmWB has led to a rapid decline of almond trees in northern regions and in the Bekaa valley in Lebanon (Choueiri et al., 2001; Abou-Jawdah et al., 2002), and in Fars province and other southern provinces in Iran (Salehi et al., 2006a). In Lebanon the disease rapidly spread and killed almost 100,000 trees over a period of 10 years. AlmWB was found to infect properly managed orchards, abandoned orchards and isolated wild trees. The disease epidemic spreads from coastal areas to high mountainous areas (> 1200 m) encompassing several ecological niches. Based on observation of both symptoms and the spread of the epidemic, it was hypothesized that the aetiological agent of AlmWB could be a phytoplasma transmitted by an efficient aerial vector or vectors. In 2009, ‘Ca. P. phoenicium’ was identified in association with a severe disease of peach (P. persica) and nectarine (P. persica var. nucipersica) in southern Lebanon (Abou-Jawdah et al., 2009) and more than 40,000 newly diseased almond trees were observed in 2010 throughout the country, in 16 out of 24 Lebanese districts (Molino Lova et al., 2011). According to the small amount of information provided by the scientific literature (Verdin et al., 2004; Zirak et al., 2009) AlmWB appeared in both countries in the same period and, due to the distance between Lebanon and Iran, it is unlikely that transmission from one to the other took place through insect vectors. Unfortunately, no information is available on the presence of the disease in the two countries located between Lebanon and Iran, namely Syria (where almonds are intensively cultivated) and Iraq. It seems likely that humans played a role in the spread of the disease, even if trade of plants or seedlings from Lebanon and Iran is not reported. However, as underlined by Verdin et al. (2004), the disease might be present and spreading in additional areas of the Middle East.

Risk of Introduction

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The rapid spread of ‘Ca. P. phoenicium’ in peach and nectarine orchards and in other plant hosts causes concern about the risk it poses for stone fruit production in the Middle East and in all the countries of the Mediterranean basin, although grafting experiments and molecular analyses have revealed that it does not affect plum (Prunus domestica) or cherry (P. avium) trees (Abou-Jawdah et al., 2003).

Habitat

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In Lebanon AlmWB was found to infect properly managed orchards, abandoned orchards and isolated wild trees. The disease spreads from coastal areas to high mountainous areas (> 1200 m) encompassing several ecological niches (Abou-Jawdah et al., 2002; Molino Lova et al., 2014).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Other
Host Present, no further details Harmful (pest or invasive)
Vector Present, no further details Natural
Terrestrial
Terrestrial – ManagedCultivated / agricultural land Principal habitat Harmful (pest or invasive)
Managed forests, plantations and orchards Principal habitat Harmful (pest or invasive)
Terrestrial ‑ Natural / Semi-naturalNatural forests Principal habitat Natural
Rocky areas / lava flows Present, no further details Natural
Scrub / shrublands Present, no further details Natural
Arid regions Present, no further details Natural
Littoral
Coastal areas Present, no further details Natural
Coastal dunes Present, no further details Natural

Hosts/Species Affected

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All almond (Prunus dulcis) varieties in the almond growing areas of Iran and Lebanon have been affected by AlmWB disease, but some varieties (e.g. Alwani and Awja in Lebanon and Sangi in Iran) are highly susceptible and develop severe witches’-brooms, leading to rapid death of the tree, while other varieties (e.g. Kachabi) are less affected (Verdin et al., 2003; Choueiri et al., 2001). Grafting experiments and molecular analyses indicate that AlmWB does not affect plum (P. domestica) or cherry (P. avium) trees (Abou-Jawdah et al., 2003). Nevertheless, its rapid spread on almond, peach (P. persica) and nectarine (P. persica var. nucipersica) orchards indicate a risk for epidemics in Lebanon and in the other countries of the Mediterranean area.

In Iran, ‘Ca. P. phoenicium’ has not been identified in peach and nectarine but rather in other plant hosts, such as GF-677 (P. amygdalus × P. persica) and wild almond (Prunus scoparia) (Salehi et al., 2015), and more recently in apricots (P. armeniaca), in which it has been found to cause apricot yellows (Salehi et al., 2018).

Smilax aspera L. and Anthemis sp. are plant hosts preferred by the cixiid insect vectors Tachycixius viperinus (T. viperina) and T. cf. cypricus (T. cypricus) (Tedeschi et al., 2015). The leafhopper vector Asymmetrasca decedens was found feeding on Prunus scoparia (Salehi et al., 2015).

Host Plants and Other Plants Affected

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Plant nameFamilyContext
Anthemis (chamomile)AsteraceaeWild host
Prunus amygdalus x Prunus persicaOther
Prunus armeniaca (apricot)RosaceaeMain
Prunus dulcis (almond)RosaceaeMain
Prunus persica (peach)RosaceaeMain
Prunus scopariaRosaceaeWild host
Smilax asperaSmilacaceaeWild host

Growth Stages

Top of page Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

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The most characteristic symptoms caused by AlmWB on almond trees are (i) shoot proliferation on the main trunk with the appearance of a witches’-broom, (ii) the perpendicular development of many auxiliary buds on the branches, with smaller and yellowish leaves, and (iii) the general decline of the tree with final dieback. A total loss of production happens 1-2 years after the initial appearance of the symptoms (Abou-Jawdah et al., 2002).

In the case of peach and nectarine trees, the first symptom observed is early flowering (15 to 20 days earlier than normal), followed by the earlier development of all the buds of the infected branches. In addition, phyllody at the flowering period and serrate, slim, light green leaves and witches’-brooms developing several months later from the trunk and the crown of the trees are observed (Abou-Jawdah et al., 2009). Even if the presence of witches’-broom is more common in almond trees than in peach/nectarine, the most important difference between peach/nectarine and almond symptoms is the development, in peach/nectarine trees, of phyllodies, never recorded on almond (Molino Lova et al., 2011).

List of Symptoms/Signs

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SignLife StagesType
Fruit / abnormal patterns
Fruit / abnormal shape
Fruit / reduced size
Growing point / dieback
Growing point / dwarfing; stunting
Inflorescence / abnormal leaves (phyllody)
Inflorescence / premature ripening
Leaves / abnormal colours
Leaves / abnormal forms
Leaves / yellowed or dead
Stems / discoloration
Stems / stunting or rosetting
Stems / witches broom
Whole plant / discoloration
Whole plant / plant dead; dieback

Biology and Ecology

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Genetics

Phytoplasmas have reduced genomes, ranging in size from 530 to 1350 kilobases; as they lack genes encoding various metabolic pathways, their cultivation in axenic culture is still not completely successful. A draft genome sequence of 'Ca. P. phoenicium' strain SA213, representative of phytoplasma strain populations from different host plants, was recently generated. Analyses of the available genome features allowed the identification of candidate determinants of pathogenicity and highlighted the coding of the conserved ATP-providing pathway of phytoplasmas, based on MleP/CitS mediated malate uptake and subsequent formation of acetate. Two putative secreted effector proteins containing the SVM sequence (SAP05- and SAP11-like), and one predicted haemolysin, containing a CBS domain, were identified within the predicted secreted proteins and can be proposed as pathogenicity determinants. One of the integral membrane proteins was predicted as BI-1, an inhibitor of apoptosis-promoting Bax factor. Its identification within genomes of other ‘Ca. Phytoplasma’ species suggested its potential role as a phytoplasma fitness-increasing factor that works by modification of the host-defense response.

Multiple gene typing analyses (genes 16S rRNA, rplV-rpsC, secY, tufB, groEL, inmp) of ‘Ca. P. phoenicium’ strains infecting almond, peach and nectarine in Lebanon (i) revealed a substantial genetic homogeneity within the analyzed phytoplasma populations based on housekeeping gene sequence analyses, and (ii) allowed the identification of distinct AlmWB-associated phytoplasma strains from diverse host plants based on inmp (integral membrane protein) gene sequence analysis. This evidence, along with prior reports of multiple insect vectors of AlmWB phytoplasma, suggests that AlmWB could be associated with phytoplasma strains derived from the adaptation of an original strain to diverse hosts (Lee et al., 2012; Quaglino et al., 2015).

Climate

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ClimateStatusDescriptionRemark
BS - Steppe climate Tolerated > 430mm and < 860mm annual precipitation
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
38.63 25.65

Air Temperature

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Parameter Lower limit Upper limit
Absolute minimum temperature (ºC) -2
Mean annual temperature (ºC) 5 37
Mean maximum temperature of hottest month (ºC) 22 37
Mean minimum temperature of coldest month (ºC) -2 7

Means of Movement and Dispersal

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The presence and rapid spread of AlmWB in Lebanon entail the activity of one or more vectors. In nature phytoplasmas are mainly transmitted by sap-sucking insects, mainly Hemiptera, suborders Auchenorrhyncha (families Cicadellidae and Cixiidae) and Sternorrhyncha (Psyllidae) (Weber and Maixner, 1998; Weintraub and Beanland, 2006). During field surveys of the epidemiological cycle of AlmWB in Lebanon, conducted in AlmWB-infested almond and peach orchards and surroundings, 'Ca. P. phoenicium' was detected in the leafhopper Asymmetrasca decedens (prevalent on almond) and in the cixiids Cixius sp., Tachycixius spp., and Eumecurus spp. (prevalent on Smilax aspera L. and Anthemis sp.); it was also detected in crops and wild plants where the insects were collected. Transmission trials under controlled conditions demonstrated that A. decedens, T.viperinus and T. cf. cypricus are able to transmit 'Ca. P. phoenicium' to plants. These studies revealed a complex epidemiological cycle, in which A. decedens may be responsible for transmission from almond to almond and Tachycixius spp.for transmission from weeds to almonds (Abou-Jawdah et al., 2014; Tedeschi et al., 2015).

AlmWB appeared in Lebanon and Iran in the same period and, due to the distance between the two countries, it is unlikely that transmission between them took place through insect vectors. Unfortunately, no information is available on the distribution of the disease in the two countries located between Lebanon and Iran, namely Syria, where almonds are intensively cultivated, and Iraq; as underlined by Verdin et al. (2004), the disease might be present and spreading in additional areas of the Middle East. It seems likely that humans played a role in the diffusion of the disease, even if trade of plants or seedlings from Lebanon and Iran is not reported.

Considering the hosts of 'Ca. P. phoenicium', possible pathways for the phytoplasma are plants for planting (except seeds), cut branches, and fresh almonds with shells. Fruit of other known hosts would generally not carry a peduncle or plant part that would carry the phytoplasma.

Infectious vectors may also be found on plants for planting, cut flowers and branches, leaf vegetables. In addition, A. decedens has been found to be associated with Citrus fruit; for other hosts, it is not associated with the fruit itself, only with leaves or stems if these are present.

Some commodities may carry only the phytoplasma, some the phytoplasma and infectious vectors, and some only infectious vectors.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Breeding and propagationGrafting activities (probably) Yes Yes Abou-Jawdah et al., 2003
Crop productionTrade in plants or seedlings (probably) Yes Verdin et al., 2004

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Host and vector organismsAsymmetrasca decedens, Tachycixius viperina and T. cypricus. May be involved in long-distance transmission as well. Yes Dakhil et al., 2011
Plants or parts of plantsPlant trade (probably) Yes Yes Verdin et al., 2004

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
Seedlings/Micropropagated plants
Stems (above ground)/Shoots/Trunks/Branches

Vectors and Intermediate Hosts

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VectorSourceReferenceGroupDistribution
Asymmetrasca decedensAbou-Jawdah et al., 2014. Insect
Tachycixius cypricusTedeschi et al., 2015. Insect
Tachycixius viperinaTedeschi et al., 2015. InsectBulgaria

Impact Summary

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CategoryImpact
Cultural/amenity Negative
Economic/livelihood Negative
Environment (generally) Negative

Economic Impact

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Ca. P. phoenicium’ causes yield reduction in almonds, peaches and nectarines, with either unmarketable fruit or no fruit. On infected almond trees, total loss of production happens 1-2 years after the first symptoms (Molino Lova et al., 2011). Where trees still produce fruit, these are fewer and deformed, resulting in practically 100% marketable yield loss (Abou-Jawdah et al., 2002). In the case of peaches, most infected trees do not produce fruit; some produce a limited number of deformed fruits. In the case of nectarines, infected trees produce deformed fruit in the first two years, and fruit production stops from the third year. ‘Ca. P. phoenicium’ causes the death of almond trees within 3-4 years. In highly susceptible cultivars, dieback may occur in all trees of an affected orchard (Verdin et al., 2003).

Iran: Iran was a leader in almond production. In recent years, however, production of this crop has been seriously affected by almond witches’-broom disease in the region of Fars, in certain other provinces in the south of the country, and in the central regions of Iran, in Isfahan and Chaharmahal-and-Bakhtiari provinces. These regions contribute considerably to the Iranian agricultural economy -- 20,930 ha of almonds were cultivated with a production of 12,187 tonnes of nuts annually (AREEO, 2008). Over four years of observation, the infected trees declined and died within 3–4 years of initiation of symptoms. All almond varieties seem to be affected, with different degrees of susceptibility. Molino Lova et al. (2011) mention that AlmWB in Iran has caused severe losses on almond trees since 1995, i.e. at the same time as in Lebanon, and that the production has been seriously affected in some provinces. The disease has generated extensive research.

Lebanon: In Lebanon stone fruits, and almonds in particular, represent the major fruit crops grown, in terms of income generated, compared with grapes, olives, pome fruits and citrus. Within the stone fruits, almonds rank first compared to cherries, peaches and nectarines, apricots and plums. In the 1980s and 1990s, the area devoted to almond production in Lebanon increased remarkably when some growers in the Bekaa Valley preferred growing almonds instead of grape, cherry, and apricot. However, during the last decade the outbreak of AlmWB has led to a rapid decline of almond trees in the major almond production regions. ‘Ca. P. phoenicium’ has killed over 150,000 trees within two decades (Abou-Jawdah et al., 2014). In the regions of Koura and Tripoli, most almond trees have died or are dying (over 65,000 trees). In the major stone fruit production area of the Bekaa, the disease is still restricted. It has not spread to adjacent cherry trees in the same region, but it has spread to peaches and nectarines (Abou-Jawdah et al., 2002). Its rapid spread in the almond growing regions, together with the lack of any action taken by the farmers or by the local/national offices of the Ministry of Agriculture to stop it, has resulted in a devastating impact on the economy of the almond producers. It has reached very high frequency of infection and severity in the almond orchards, for example reaching 96% in the Koura district which is entirely cultivated with almonds.

Environmental Impact

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Since the disease is spreading in Lebanon and is not still clearly known by the growers, quick and reliable identification of infected trees is necessary to plan adequate strategies for its containment. When such information is not available, excessive numbers of insecticide treatments are applied, often suggested by technicians or agricultural engineers. The impact on the environment is detrimental, and such arbitrary practices have often facilitated the spread of the disease when infected plants are left on the fields (Molino Lova et al., 2014).

Risk and Impact Factors

Top of page Invasiveness
  • Invasive in its native range
  • Abundant in its native range
  • Highly adaptable to different environments
  • Highly mobile locally
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts cultural/traditional practices
  • Negatively impacts livelihoods
  • Damages animal/plant products
  • Negatively impacts trade/international relations
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult/costly to control

Diagnosis

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Phytoplasmas can be seen by microscopic observation of phloem tissues, but protocols for their detection and identification are based on PCR amplification of DNA target sequences. In addition, biological indexing may also be used for phytoplasma detection in certification or quarantine programs (Marcone, 2014). Sampling and extraction techniques are important as phytoplasmas may be distributed unevenly in the plant. ‘Ca. P. phoenicium’ may be present in the absence of symptoms, as it can have a long incubation period and some trees or cultivars are asymptomatic (Abou-Jawdah et al., 2002).

Identification requires molecular methods, which are available. Phytoplasmas can first be identified to the level of the 16SrIX group (so the presence of other groups can be ruled out), or to the level of the subgroups (allowing differentiation of 'Ca. P. phoenicium' from related phytoplasmas). PCR-based identification to the 16SrIX group level utilizes the primer pair AlWF2/AlWR2, while identification to the subgroup level relies on RFLP (restriction fragment length polymorphism) analyses on R16F2n/R16R2 amplicons (Molino Lova et al., 2011). Details for ‘Ca. P. phoenicium’ are given in various publications including Verdin et al. (2003), Abou-Jawdah et al. (2002, 2003), Molino Lova et al. (2011) and Salehi et al. (2006a). Recently, PCR and qPCR protocols that could be used on plants and insects have been developed (Jawhari et al., 2015).

Detection and Inspection

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Phyllody and flower malformation appear usually in April/May and are easy to recognize in the field. Over the season, farmers can observe shoot proliferation or light green leaf development, but they normally do not associate such symptoms with a disease that cannot be controlled by using pesticides, and frequently treat the phytoplasma-infected trees with ineffective pesticides.

Similarities to Other Species/Conditions

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A form of AlmWB reported in Iran (Verdin et al., 2003) was found to be associated with phytoplasmas related to ‘Ca. Phytoplasma phoenicium’ (subgroup 16SrIX-C), close to the Knautia arvensis phyllody (KAP) phytoplasma belonging to 16SrIX-C (Salehi et al., 2006b). Nucleotide sequence identity, the presence of species-specific signature sequences, and phylogenetic analysis of the 16S rRNA gene allowed the distinction of ‘Ca. Phytoplasma phoenicium’ strains (subgroup 16SrIX-B) and ‘Ca. Phytoplasma phoenicium’-related strains (subgroup 16SrIX-C). Moreover, such ‘Ca. Phytoplasma phoenicium’-related strains are not transmitted by insect vectors of ‘Ca. Phytoplasma phoenicium’ (16SrIX-B) strains and have not been found in the natural plant hosts of those vectors (Prunus scoparia, Smilax aspera, Anthemis spp.). Thus, ‘Ca. Phytoplasma phoenicium’ (16SrIX-B) strains are clearly distinct from strains of other 16SrIX subgroups at both the molecular and the biological level. Based on such evidence, several species have recently been determined (Davis et al., 2013; Quaglino et al., 2013). Although even strains of other 16SrIX subgroups share a 16S rDNA sequence identity > 97.5% in comparison with strain A4 (the reference strain of the species ‘Ca. P. phoenicium’), it appears improper to refer to all 16SrIX phytoplasma strains as ‘Ca. P. phoenicium’ strains.

Ca. Phytoplasma phoenicium’-related strains (subgroup 16SrIX-C) represent another threat to agriculture. These strains are associated with important crop diseases (e.g sesame phyllody) and are hosted worldwide by a large range of natural wild host plants (Casati et al., 2016).

Furthermore, almond trees showing different symptoms, such as small and yellow leaves, have been found to be infected by 'Ca. P. aurantifolia', 'Ca. P. solani' and 'Ca. P. trifolii' in Iran (Zirak et al., 2009). Nucleotide sequence identity, presence of species-specific signature sequences, and 16Sr-specific RFLP patterns clearly distinguish ‘Ca. Phytoplasma phoenicium’ strains from these phytoplasma species.

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 phytoplasma diseases is difficult in the field, and in the case of epidemics usually relies on the control of insect vectors, the use of phytoplasma-free planting material and the use of resistant cultivars. Early detection and eradication of phytoplasma sources, and quick and reliable identification of the infected trees, are important for successful control. The accurate description of the symptoms of a new or unknown disease provides a sound basis for locating the infected trees during the most suitable period to monitor the orchards. Effective disease control depends primarily on early, accurate identification of the disease and its causal agents.

  Al-Achi and Choueiri (2015) outline the following control measures against ‘Ca. P. phoenicium’:

  • use of certified plants and healthy buds.
  • several tissue culture techniques coupled with thermotherapy produce phytoplasma-free almond plantlets, and thus might be used as a sanitation technique for the production of healthy planting material (e.g. in the framework certification schemes). Stem cutting culture combined with thermotherapy appeared to be the most practical and effective (Chalak et al., 2005). Subsequent studies showed that shoot tip and stem cutting cultures associated with heat treatment were all suitable for phytoplasma elimination from regenerated shootlets (Chalak and Choueiri, 2015).
  • avoiding grafting from infected trees
  • removing weeds that might be hosts
  • destroying infected trees
  • not replacing infected trees by vulnerable species. Abou-Jawdah et al. (2011) note that apricot is one possible replacement crop, since it proved to be resistant to 'Ca. P. phoenicium'; however it is attacked by other phytoplasmas, and may also be a natural host of some strains in Iran.

There do not seem to be any known cultivars that are fully resistant to the disease. It is noted that breeding of resistant cultivars may be the only way to control the disease (Zamharir, 2011).

There is no chemical control method against phytoplasmas. Tetracycline antibiotics are somewhat effective but are problematic in fruit trees as they persist in plants for several months and only cause a temporary remission of symptoms (Zamharir, 2011). They are not allowed in crop production in the EU. In the absence of quick and reliable identification of infected trees, farmers often apply excessive quantities of insecticides, with a detrimental effect on the environment, or attempt to treat the disease with ineffective substances such as fosetyl–aluminium, copper or winter oil. Such practices can facilitate the spread of the disease by leaving infected plants in the fields (Molino Lova et al., 2014).

Management of vectors has relied on chemical control, but Molino Lova et al. (2011) note that this is slowly shifting to integrate a) habitat management to reduce the pest incidence and b) genetically modified crops. However, the knowledge of vectors is still very incomplete.

In Lebanon, both participatory approaches and farmer field schools have been used to develop science based knowledge and to increase farmer knowledge and awareness of IPM. Impact evaluations have shown that such approaches can significantly improve farmers' knowledge (Rola et al., 2002, Hashemi et al., 2008).

Gaps in Knowledge/Research Needs

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Future research should focus on the following aspects to allow the development of more efficient AlmWB management and prevention of its spread: (i) determination of the host range of ‘Ca. P. phoenicium’, including alternative hosts and the role of weeds as a reservoir; (ii) investigation on the epidemiology of the disease, including the life cycles of known and potential vectors in Lebanon, Iran and countries in the Mediterranean basin; and (iii) evaluation of the resistance to infection by ‘Ca. P. phoenicium’ in almond, peach and nectarine cultivars.

References

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Links to Websites

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WebsiteURLComment
COST action FA 0807: Integrated Management of Phytoplasma Epidemics in Different Crop Systemshttp://www.costphytoplasma.ipwgnet.org/
European and Mediterranean Plant Protection Organizationhttps://www.eppo.int
International Phytoplasmologist Working Group (IPWG)http://www.ipwgnet.org/

Organizations

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Lebanon: AVSI Foundation, Rue St. Fawka, Centre Jean Paul II, , 1200 Jounieh Ghadir, https://www.avsi.org/en/country/lebanon/1/

Contributors

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30/09/17 Original text by:

Fabio Quaglino, Department of Agricultural and Environmental Sciences, University of Milan, Milan, Italy

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