Candidatus Phytoplasma pruni

California Pest Rating for

(= Peach X-disease, Peach Rosette, Peach Red Suture, and Little Peach Phytoplasmas)

Pest Rating: C

PEST RATING PROFILE

Initiating Event:

CDFA regulations require imported peach nursery stock to be certified free from Peach Rosette, Peach Yellows, Little Peach and Red Suture Diseases. These diseases are caused by phytoplasmas which are named accordingly. Presently, all four phytoplasmas are A-rated pathogens in California. However, research has shown that these phytoplasmas are actually strains of Candidatus Phytoplasma pruni. Therefore, the status of the four phytoplasmas and their current rating in California are reviewed herein and a new permanent rating is proposed.

History & Status:

Background: In 1933, a disease of peach was discovered in Connecticut and called the “X-disease of Peach” because of its unknown cause and mysterious nature. For several years following its discovery, X-disease was believed to be caused by a virus that was mainly vectored by insects from nearby forests to peach orchards and seldom passed from tree to tree in the eastern USA. Wild chokecherry (Prunus virginiana), growing in forests, was found to be an important natural host of the pathogen. By the early 1950s, X-disease was also discovered in several US north eastern states and western states, including California, as well as in Canada (Stoddard, et al., 1951). Subsequently, based on slightly different symptoms, two forms of peach X-disease were initially distinguished in the USA, namely, eastern X-disease and western X-disease, however, based on serological, nucleic acid and graft-transmission studies the eastern and western forms were found to be similar and recognized as strains of the pathogen. The pathogen was soon discovered to be widely distributed in fruit trees in the USA and can be transmitted by species of leafhopper. X-disease is now known to be caused by a phytoplasma (formerly, mycoplasma-like organism or MLO). In Eastern USA, peach rosette, peach yellows (also called little peach) and peach red suture were associated with the presence of peach X-disease phytoplasma. Cherry albino disease, once found in the Rogue River Valley of Oregon in 1937 but now no longer found, was suspected to be caused by a strain of peach X-disease phytoplasma. In California, Cherry buckskin disease on cherry had been known since the early 1920s and later the pathogen that caused this disease was also discovered to cause lethal decline disease of peach or “lethal casting yellows’. Both diseases were later considered to be caused by strains of peach X-disease. Also in California, peach yellow leaf roll disease is caused by several genetically unrelated phytoplasmas of which only one is similar to, and a strain of peach X-disease phytoplasma (CABI, 2016; Davis et al., 2013; Kirkpatrick, 1995; Larson & Waterworth, 1995; 1995 Kirkpatrick et al., 1995).

Based on gene analysis, namely, restriction fragment length polymorphism (RFLP) analysis of 16S rRNA gene sequences, strains of peach X-disease phytoplasma from eastern and western USA and eastern Canada were classified in phytoplasma 16S rRNA gene RFLP group 16 SrIII, subgroup A. Davis et al., (2013) found gene sequences of peach X-disease phytoplasma strains to be distinct from other previously described Candidatus Phytoplasma species and therefore, formally described Candidatus Phytoplasma pruni (Ca. Phytoplasma pruni) as a new species group or taxon of phytoplasma associated with X-disease of stone fruits to include geographically diverse X-disease phytoplasma strains that shared similar nucleotide sequence (16S rRNA gene sequences) alignments. These strains include X-disease phytoplasma (cause of peach yellows disease), peach rosette, peach red suture, and little peach phytoplasmas.

Hosts: Peach (Prunus persica) is the principal host of the pathogen. Other hosts include species of the genus Prunus, including, cherry (P. avium and P. cerasus), Japanese plum (P. salicina), almond (P. dulcis), apricot (P. armeniaca), nectarine (P. persica var. nectarine), Chinese bushcherry (P. japonica), Bessey cherry (P. besseyi), wild American plum (P. americana), wildgoose plum (P. munsoniana) and European plum (P. domestica). Common chokecherry (P. virginiana) is a wild host species that serves as an important natural reservoir of peach X-disease phytoplasma in many states of USA. Bur clover (Medicago polymorpha) is also a wild host of the pathogen. Also, switch sorrel (Dodonaea viscosa) and lucerne (Medicago sativa) (CABI, 2016; EPPO, 2014; Davis et al., 2013; Douglas, 1986; Stoddard et al., 1951).

Symptoms: Symptoms of X-disease on peach (Ca. Phytoplasma pruni) include: tattered, shot-holed leaves, chlorosis, loss of severely affected leaves leaving a cluster of leaves at the terminal tips of shoots (rosettes), dieback of branches and death of trees (Davis, et al., 2013; Douglas, 1986; Stoddard, et al., 1951). Younger peach trees die within 1-3 years after the first appearance of symptoms. The first symptoms of X-disease in peach on leaves of some or all branches appear as reddish purple spots which later die and fall out (shot-holes). The leaves turn reddish and curl upwards. Older trees may survive longer but bear little or no fruit. Fruit usually shrivel and drop, but those remaining on the trees ripen prematurely, have an off-taste and are not marketable. No seeds develop in infected fruit. The phytoplasma can be irregularly distributed in the trees therefore fruit on healthy-appearing parts of a tree do not show signs of disease (Agrios, 2005; CABI, 2014). Infected cherry trees on resistant Prunus mahaleb rootstock die rapidly due to hypersensitive reaction that occurs at the graft union. Other rootstocks die slower (Kirkpatrick et al., 1995).

Damage Potential: Peach X-disease is one of the most important diseases of peach. Infected trees become commercially useless in 2-4 years (Agrios, 2005). The degree of damage depends on the strain of the pathogen and development stage of the infected host. Also, it can cause serious losses to cherry production.

Transmission: The pathogen is transmitted by several species of leafhopper, including Colladonas clitellarius, C. montanus, C. geminatus, Euscelidius variegates, Fieberiella florii, Graphocephala confluens, Gyponana lamina, Keonella confluens, Norvellina seminude, Osbornellus borealis, Paraphlepsius irroratus, and Scaphytopius delongi (S. acutus) (CABI, 2014; Davis, et al., 2013). The leafhopper vectors overwinter on herbaceous weeds that act as reservoir of the pathogen in orchards, and infect trees in spring and summer. The latency period, or the time between when a vector acquires the pathogen while feeding on an infected host and when the vector is able to inoculate the pathogen into a non-infected, susceptible host, is 22-35 days for Colladonas geminatus and 45 days for Scaphytopius delongi (S. acutus) (CABI, 2016).

The pathogen is also transmitted over long distances through infected plant materials that were propagated by budding and grafting of infected plant material. Infected plant parts at risk of spreading the phytoplasma include all plant parts with the exception of fruit (CABI, 2016).

Worldwide Distribution: Asia: India (EPPO, 2016); North America: Canada, USA (California, Colorado, Connecticut, Georgia, Hawaii, Massachusetts, Michigan, Minnesota, Missouri, Nebraska, New York, North Dakota, Oregon, Pennsylvania, South Carolina, South Dakota, Utah, Virginia, Washington, West Virginia) (CABI, 2016; EPPO, 2016; Thakur et al., 1998).

Official Control: Currently, the listed diseases and strains of Ca. Phytoplasma pruni are on the ‘Harmful Organism Lists’ for the respective countries. Peach X-disease phytoplasma: Argentina, Brazil, Canada, Chile, China, Colombia, Guatemala, Japan, Jordan, Republic of Korea, Mexico, Morocco, Norway, Paraguay, Peru, and Turkey; Peach X-disease mycoplasma: European Union, Holy See (Vatican City State), Monaco, San Marino, and Serbia; Peach X phytoplasma: Israel and Japan; Peach rosette mycoplasma: European Union, Holy See (Vatican City State), Monaco, San Marino, and Serbia; Peach rosette phytoplasma: Argentina, Brazil, Guatemala, Israel, Japan, Mexico, Morocco, Paraguay, and Turkey; Peach yellow MLO: Mexico; Peach yellows mycoplasma: European Union, Holy See (Vatican City State), Madagascar, Monaco, San Marino, Serbia, and Ukraine; Peach yellows phytoplasma: Brazil, Chile, Colombia, Israel, Japan, Jordan, Republic of Korea, Mexico, Morocco, Paraguay, Peru, and Turkey (PCIT, 2016).

Ca. Phytoplasma pruni is an EPPO A1 quarantine pest. It is a quarantine pest in Israel, and Norway (EPPO, 2016).

Currently, diseases and strains of Ca. Phytoplasma pruni, namely, X-disease phytoplasma causing cherry buckskin, cherry albino and peach western X diseases are already present in California and rated ‘C’, while peach red suture, peach rosette, little peach and X-disease (causing peach yellows disease) phytoplasmas are quarantine pathogens rated ‘A’.

California Distribution: Western X-disease phytoplasma (now, Ca. Phytoplasma pruni) is generally distributed throughout California and has been detected on plum, cherry, apricot, peach, nectarine, almond and celery (California Plant Disease Host Index by French, A. 1989, Updated 2014).

California Interceptions: The risk Ca. Phytoplasma pruni would pose to California is evaluated below.

Consequences of Introduction:

1) Climate/Host Interaction: Evaluate if the pest would have suitable hosts and climate to establish in California:

Score: 3

– Low (1) Not likely to establish in California; or likely to establish in very limited areas.

– Medium (2) may be able to establish in a larger but limited part of California.

– High (3) likely to establish a widespread distribution in California.

Risk is High (3) – Strains of Ca. Phytoplasma pruni are already established and widespread within California.

2) Known Pest Host Range: Evaluate the host range of the pest:

Score: 1

– Low (1) has a very limited host range.

– Medium (2) has a moderate host range.

– High (3) has a wide host range.

Risk is Low (1) – The host range is limited to Prunus spp. of which peach (P. persicae) is the principal host. Peach is a major stone fruit crop in California, cultivated in significant acreage throughout the State.

3) Pest Dispersal Potential: Evaluate the natural and artificial dispersal potential of the pest:

Score: 3

– Low (1) does not have high reproductive or dispersal potential.

– Medium (2) has either high reproductive or dispersal potential.

– High (3) has both high reproduction and dispersal potential.

Risk is High (3) – The pathogen is artificially transmitted mainly by a number of leafhopper species thereby marking it as having a high potential for increase and spread. It is also spread in infected plant materials through grafting and budding operations.

4) Economic Impact: Evaluate the economic impact of the pest to California using the criteria below:

A. The pest could lower crop yield.

B. The pest could lower crop value (includes increasing crop production costs).

C. The pest could trigger the loss of markets (includes quarantines).

D. The pest could negatively change normal cultural practices.

E. The pest can vector, or is vectored, by another pestiferous organism.

F. The organism is injurious or poisonous to agriculturally important animals.

G. The organism can interfere with the delivery or supply of water for agricultural uses.

Score: 3

– Low (1) causes 0 or 1 of these impacts.

– Medium (2) causes 2 of these impacts.

– High (3) causes 3 or more of these impacts.

Risk is High (3) – Ca. Phytoplasma pruni has the potential to seriously damage peach (and stone fruit) production by lowering crop yield and value, requiring changes in cultural management practices to maintain disease free plants, trigger loss of markets possibly through further impositions of quarantines by importing countries and increase costs in production of clean crops. The pathogen is vectored by many species of leafhopper.

5) Environmental Impact: Evaluate the environmental impact of the pest on California using the criteria below:

A. The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.

B. The pest could directly affect threatened or endangered species.

C. The pest could impact threatened or endangered species by disrupting critical habitats.

D. The pest could trigger additional official or private treatment programs.

E. The pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.

Score the pest for Environmental Impact. Score:

– Low (1) causes none of the above to occur.

– Medium (2) causes one of the above to occur.

– High (3) causes two or more of the above to occur.

Risk is Medium (2) – There is a medium impact to the environment expected. The pathogen is limited to Prunus spp. of which a few serve as wild hosts. These wild hosts may also serve as reservoirs from which the vectors can acquire and transmit the pathogen to non-infected main hosts. Home grown peach trees may be infected thereby requiring specific treatment measures.

Consequences of Introduction to California for X-disease phytoplasma:

Add up the total score and include it here. (Score)

-Low = 5-8 points

–Medium = 9-12 points

-High = 13-15 points

Total points obtained on evaluation of consequences of introduction of X-disease phytoplasma to California = (12).

6) Post Entry Distribution and Survey Information: Evaluate the known distribution in California. Only official records identified by a taxonomic expert and supported by voucher specimens deposited in natural history collections should be considered. Pest incursions that have been eradicated, are under eradication, or have been delimited with no further detections should not be included:

Score: 3

-Not established (0) Pest never detected in California, or known only from incursions.

-Low (-1) Pest has a localized distribution in California, or is established in one suitable climate/host area (region).

-Medium (-2) Pest is widespread in California but not fully established in the endangered area, or pest established in two contiguous suitable climate/host areas.

–High (-3) Pest has fully established in the endangered area, or pest is reported in more than two contiguous or non-contiguous suitable climate/host areas.

Evaluation is High (3).

Final Score:

7) The final score is the consequences of introduction score minus the post entry distribution and survey information score: (Score)

Final Score: Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 9.

Uncertainty:

Continued survey of stonefruit production for all strains of Ca. Phytoplasma pruni will lend more knowledge to the distribution of this pathogen in California. This information can result in further lowering the overall score but will not lower the proposed C rating.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Ca. Phytoplasma pruni (containing peach X-disease, peach rosette, peach red suture, and little peach strains) is C.

References:

Agrios, G. N. 2005. Plant Pathology fifth edition. Elsevier Academic Press, Massachusetts, USA. 922 p.

CABI. 2016. Phytoplasma pruni (peach X-disease) full datasheet report. Crop Protection Compendium. www.cabi.org/cpc/ .

Davis, R. E., Y. Zhao, E. L. Dally, Ing-Ming Lee, R. Jomantiene and S. M. Douglas. 2013. ‘Candidatus Phytoplasma pruni’, a novel taxon associated with X-disease of stone fruits, Prunus spp.: multilocus characterization based on 16S rRNA, secY, and ribosomal protein genes. International Journal of Systematic and Evolutionary Microbiology, 63:766-776.

EPPO. 2016. Phytoplasma pruni (PHYPPN). European and Mediterranean Plant Protection Organization PQR database. http://www.eppo.int/DATABASES/pqr/pqr.htm .

Douglas, S. M. 1986. Detection of mycoplasma-like organisms in peach and chokecherry with X-disease by fluorescence microscopy. Phytopathology 76:784-787.

Kirkpatrick, B. C. 1995. Diseases caused by mycoplasma-like organisms: Cherry Albino, Peach Rosette, Peach Yellows. In Compendium of Stone Fruit Diseases. Edited by J. M. Ogawa, E. I. Zehr, G. W. Bird, D. F. Ritchie, K. Uriu and J. K. Uyemoto. APS Press, The American Phytopathological Society, Minnesota, USA, pg. 55-59.

Kirkpatrick, B. C., J. K. Uyemoto and A. H. Purcell. 1995. Diseases caused by mycoplasmalike organisms: X-Disease. In Compendium of Stone Fruit Diseases. Edited by J. M. Ogawa, E. I. Zehr, G. W. Bird, D. F. Ritchie, K. Uriu and J. K. Uyemoto. APS Press, The American Phytopathological Society, Minnesota, USA, pg. 57-59.

Larsen, H. J., and H. E. Waterworth. 1995. Diseases caused by mycoplasmalike organisms: Peach Red Suture. In Compendium of Stone Fruit Diseases. Edited by J. M. Ogawa, E. I. Zehr, G. W. Bird, D. F. Ritchie, K. Uriu and J. K. Uyemoto. APS Press, The American Phytopathological Society, Minnesota, USA, pg. 55-56.

PCIT. 2016. USDA Phytosanitary Certificate Issuance & Tracking System. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp .

Stoddard, E. M., E. M. Hildebrand, D. H. Palmiter and K. G. Parker. 1951. X-disease. In Virus Diseases and Other Disorders with Viruslike Symptoms of Stone Fruits in North America, United States Department of Agriculture Handbook, Washington: US Government Printing Office. 10:37-42.

Thakur, P. D., A. Handa, S. C. Chowfla, and G. Krczal. 1998. Outbreak of a phytoplasma disease of peach in the northwestern Himalayas of India. Acta Horticulturae, No. 472: 737-739.

Responsible Party:

John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110, plant.health@cdfa.ca.gov.

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