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Spiroplasma citri: A Wide Host Range Phytopathogen



N. Nejat, G. Vadamalai and M. Dickinson
 
ABSTRACT

Spiroplasmas are helical motile filamentous, wall-less and culturable mollicutes. Thirty six spiroplasma species have been identified. Only S. citri, S. kunkelii and S. phoeniceum have been identified as plant pathogens. Spiroplasma citri, the causal agent of citrus stubborn disease, have a wide host range. S. citri infects most citrus species and cultivars and a wide range of non-rutaceous plant species. Citrus srubborn disease widely distributed in the southwestern united states of America, northern Africa and Mediterranean countries. It is naturally transmitted by phloem-feeding leafhopper vectors. S. citri can be detected by grafting to citrus indicators, culturing on artificial media, serological, DNA probes, dot-immunobinding assay, Immunocapture Polymerase Chain Reaction (I C- PCR), Polymerase Chain Reaction (PCR) and real-time PCR. There is genetic variability among isolates of S. citri.

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N. Nejat, G. Vadamalai and M. Dickinson, 2011. Spiroplasma citri: A Wide Host Range Phytopathogen. Plant Pathology Journal, 10: 46-56.

DOI: 10.3923/ppj.2011.46.56

URL: https://scialert.net/abstract/?doi=ppj.2011.46.56
 
Received: April 05, 2011; Accepted: April 21, 2011; Published: July 20, 2011

INTRODUCTION

Spiroplasmas (spira: a coil, spiral; plasma: something formed or molded) are motile, filamentous, wall-less and culturable mollicutes (Whitcomb and Tully, 1982; Bove, 1997). Spiroplasmas have helical, tubular and pleomorphic morphology. Extracellular spiroplasmas are more helical and tubular whilst round or flask forms are more dominant in intracellular spiroplasmas (Ammar et al., 2004). They were discovered from infected corn (Zea mays L.) plants with the corn stunt agent by dark-field microscopy (Davis et al., 1972). In 1971, Spiroplasma citri was cultured in artificial media (Saglio et al., 1971). The genus Spiroplasma was stablished in 1973 through studies on motile and helical microorganism associated with corn stunt disease (Davis and Worley, 1973). In 1973, the first spiroplasma species has been named as Spiroplasma citri as well (Saglio et al., 1973). S. citri is the type species of the type genus Spiroplasma of the family Spiroplasmataceae. Taxonomically, Spiroplasmas are in the kingdom Bacteria, Phylum Tenericutes, Class Mollicutes, Order Entomoplasmatales, Family Spiroplasmataceae and Genus Spiroplasma (Gasparich, 2002, 2010; Tully et al., 1987; Williamson et al., 1998). Based on the spiroplasma species concept as determined by the International Research Programme on Comparative Mycoplasmology and the International Subcommittee on the Taxonomy of Mollicutes, 36 spiroplasma species have been identified (Whitcomb et al., 1987; Whitcomb, 1977; Wang et al., 2010) (Table 1). Only S. citri, S. kunkelii and S. phoeniceum have been identified as plant pathogens.

The genome size of spiroplasmas ranges from 780 to 2220 kbp (Carle et al., 1992, 1995; Williamson et al., 2010) and the S. citri genome is one of the largest among Mollicutes with a high adenosine-thymidine content (up to 75%) (Melcher and Fletcher, 1999). G+C base composition of spiroplasmas ranges from 24-31% (Carle et al., 1983; Gasparich et al., 2004). They are helical filaments with 3-15 μm length range and 200-250 nm in width and an amplitude of 0.4 μm (Fletcher et al., 2006). Spiroplasmas require sterol for growth. They are resistance to penicillin. In spiroplasmas, UGA is not used as a stop codon. They use both UGA and UGG as tryptophan codons (Citti et al., 1992; Renaudin et al., 1986; Stamburski et al., 1992). In most mollicutes, comprising spiroplasmas, UAA and UAG are possible termination codons (Melcher and Fletcher, 1999).

Spiroplasma citri: Spiroplasma citri, the causal agent of citrus stubborn disease, is restricted to the phloem sieve tubes in plants. It is an obligate parasite, surviving in citrus or in a variety of other host plants, with no saprophytic phase. Citrus Stubborn Disease (CSD) was first observed in Washington navel orange trees in California about 1915 (Fawcett et al., 1944).

Spiroplasma citri infects most citrus species and cultivars and a wide range of non-rutaceous plant species (Gumpf and Calavan, 1981; Oldfield and Calavan, 1980; Whiteside et al., 1988).

Table 1: Spiroplasmas classification and characterization

Citrus is the main economic host of Spiroplasma citri. The name "stubborn" should be restricted to the disease in citrus.

Genome characteristics: G+C content of S. citri GII3-3X chromosome is 26.1%. It encodes one single 16S-23S-5S rRNA operon (Carle et al., 2010). Several pathways have been identified in S. citri, including phosphoenolpyruvate Phosphotransferase System (PTS) to import sugars to synthesize ATP using F0F1-ATP synthase, purine and pyrimidine metabolism pathways, pathway for the biosynthesis of a C55 terpenoid, 2-C-methyl-D-erythritol 4-phosphate/1-deoxy-D-xylulose 5-phosphate (MEP/DOXP) pathway to the synthesis of isopentenyl pyrophosphate, glycolytic and lactate dehydrogenase pathways to enhance fermentation. S. citri chromosome also encodes essential subunits for ATP synthase and ATP Binding Cassette (ABC) transporters. Whilst 21% of truncated CDS in S. citri GII-3X chromosome compared to their bacterial orthologs, reveals an important gene decay. It indicate that the reductive evolution of the spiroplasma genome to smaller genomes may be is still ongoing on the way (Carle et al., 2010).

There are many Coding Sequences (CDS) of plectovirus in the S. citri chromosome (Carle et al., 2010). Spiroplasma citri use fructose for pathogenicity and growth in plants (Andre et al., 2005; Gaurivaud et al., 2000). Spiralin, the most abundant and major membrane lipoprotein of 26 kDa, is essential for transmission of S. citri by the leafhopper vector Circulifer haematoceps (Duret et al., 2003).

Host range: Stubborn is an important disease of citrus. Sweet orange (C. sinensis (L.) Osbeck), sour orange (C. aurantium L.), mandarin (C. reticulata Blanco), grapefruit (C. paradisi Macfad.), lemon (C. limon (L.) Burm.f.), pomelo (C. maxima Merr.), sweet lime (C. limettioides Tan.), Rangpur (C. limonia Osbeck), Calamondin (C. madurensis Lour.), rough lemon (C. jambhiri Lush.), satsuma mandarin (C. unshiu Marcow), tangelo (C. paradisi x C. reticulata), kumquat (Fortunella spp.) and citrange (C. sinensis x Poncirus trifoliata) are susceptible to infection. Acid limes, trifoliate orange and trifoliate orange hybrids are tolerant (Calavan, 1980; Whiteside et al., 1988).

Many varieties of sweet orange comprising Washington navel, Valencia, Thomson navel, Frost Navel, Frost Valencia, Washington sanguine, Hamlin, Cadenera, Portugaise, Surprise navel, Beni Selman, Petit Jaffa, local cultivar of Fars and Ramsar Number 4 are infected to S. citri with different range of suscebtibility (Childs and Carpenter, 1960; Nejat et al., 2007).

Citrus is not the only host plant of S. citri. Many non-citrus plant species throughout the world have been also found to naturally and experimentally infected with S. citri (Table 2, 3).

Periwinkles (Catharanthus roseus (L.) G. Don) were the first non-rutaceous plants to have been found naturally infected by the Spiroplasma citri in California and Arizona (Allen, 1975; Granett et al., 1976) and then has been found in Mediterranean countries including Syria, United Arab Emirates, Oman, Cyprus and Turkey (Bove, 1986) and Malaysia (Nejat et al., 2011).

Symptoms: Stubborn disease can much reduces the quality and quantity of yields. Affected trees by stubborn disease usually are stunted and have a dense or bunchy type and upright position of growth with shortened stem internodes and multiple axillary buds. Typical leaves symptoms of stubborn are small, to call the disease little leaf, cupped shaped with rounded tip and leathery appearance. Infected leaves sometimes indicate a variety of chlorotic or mottled resembling zinc, iron and manganese deficiencies.

Fruits symptoms on stubborn-affected citrus trees is variable and include small, lopsided (curved columella), acorn-shaped with stem-end peel of normal thickness and thin rind at stylar end, stylar-end greening (retention of green color of the stylar end after ripening and become orange color of fruit) and small fruits drop. The taste of the diseased-fruits sometimes is insipid or bitter and show seed abortion (Fig. 1). (Bove, 1995; Calavan, 1968, 1979; Calavan and Carpenter, 1965; Calavan and Oldfield, 1979; Fawcett et al., 1944; Gumpf and Calavan, 1981).

Naturally infected periwinkle showing the following symptoms: Rapid decline in the number and size of the flowers were observed until flowering ceased. The buds and flowers were abscised prematurely with the reduction in leaf size and yellowing of the leaves that starts from the margin and tip, progressing to the center part. General chlorosis starts from down part, proliferation of auxillary buds, stunting and death.

Geographical distribution: Citrus srubborn disease widely distributed in the southwestern united states of America, northern Africa, Mediterranean countries and Southeast Asia including the Arizona, California, Illinois and Maryland in the United States of America, France, Greece, Italy, Spain, Libya, Algeria, Cyprus, Egypt, Iran, Iraq, Jordan, Lebanon, Palestine, Morocco, Oman, Saudi Arabia, , Syria, Tunisia, Turkey, Pakistan, Yemen and the United Arab Emirates in Mediterranean and Middle East areas, Mexico and Malaysia (Bove, 1995; Nejat et al., 2011).

Table 2: Natural non-rutaceous hosts of Spiroplasma citri

Table 3: Experimental non-rutaceous hosts of Spiroplasma citri

The disease does not appear to be a problem in cool areas or areas with warm, humid climates (Whiteside et al., 1988). While there is Spiroplasma citri in equatorial areas and can cause severe symptoms and lethal disease on periwinkle (Nejat et al., 2011).

Transmission: It is naturally transmitted by phloem-feeding leafhopper vectors in propagative manner: Circulifer tenellus Baker, Scaphytopius nitridus Delong and S. acutus delongi (Order Hemiptera, suborder Homoptera, family Cicadellidae) in California (USA) (Kaloostian et al., 1979; Mello et al., 2009; Oldfield, 1988; Oldfield et al., 1976, 1977), Neoaliturus haematoceps Mulsant and Rey (Bove et al., 1986) and C. tenellus (Klein et al., 1988) in the Mediterranean area. S. citri has been also transmitted experimentally by Euscelis plejebus Fallen (Markham and Towsend, 1974; Towsend et al., 1977) and Macrosteles fascifrons (O’Hayer et al., 1983). It is graft-transmissible through infected budwood but is neither seed nor mechanically transmissible (Whiteside et al., 1988; Rangel et al., 2005). It can be also transmitted via the parasitic plant, dodder (Cuscuta compestris or C. subinclusa) (Lee et al., 2001).

S. citri detection: S. citri can be detected by grafting to citrus indicators, culturing on artificial media, serological, DNA probes, dot-immunobinding assay, Immunocapture Polymerase Chain Reaction (I C- PCR), Polymerase Chain Reaction (PCR) and real-time PCR.

S. citri can be detected by graft inoculation of indicator plants of which the most suitables are sweet orange cv. Madame Vinous, grapefruit cv. Marsh and tangelo cv. Sexton, respectively (Bove, 1988). Side grafting is more successful than bud grafting to transmit S. citri (Rangel et al., 2005).

Phytopathogenic spiroplasmas is often detected by cultivation in artificial media. Several media have been used for the cultivation of S. citi such as: SMC (Saglio et al., 1971, 1973), C-3 (Chen and Liao, 1975), M-1 (Williamson and Whitcomb, 1975); LD8 (Lee and Davis, 1978, 1984); SP4 (Whitcomb, 1983).

Fig. 1: Citrus stubborn disease symptoms

S. citri culturing is time-consuming and 2-3 weeks need to growth S. citri in culture media and contamination can cause by non-target microorganisms (Rangel et al., 2005).

The Enzyme-linked Immunosorbent Assay (ELISA) with polyclonal and monoclonal antibodies as a sensitive serological method has been applied for identifying spiroplasmas directly in plant or insect material (Archer and Best, 1980; Archer et al., 1982; Clark et al., 1978; Lin and Chen, 1985; Saillard et al., 1980, 1993; Tully et al., 1973).

The DNA probes and dot-immunobinding assay (DIMA) were applied to detect the Spiroplasma citri in medium, infected plants and insects. DIMA is rapid assay but less sensitive than ELISA while DNA probe has a high level of sensitivity (Fletcher, 1987; Nur et al., 1986; Saillard et al., 1993).

Immuno-capture (IC)-PCR method has been applied for detection of stubborn (El-Banna et al., 2005; Saillard et al., 1993, 1996).

Polymerase Chain Reaction (PCR) is useful method for spiroplasma detection in infected plant phloem or insect vectors with 100 -1000 times of sensitivity greater than ELISA and it are also more rapid than serological techniques and culturing (Fletcher et al., 2006; Rangel et al., 2005). PCR detection of S. citri has been used with primers based on gene sequences for spiralin (Foissac et al., 1996), 16S rRNA gene in particular spiroplasma infection of carrot in the United States (Lee et al., 2006), Putative P89 adhesin and Putative P58 adhesin-like genes (Yokomi et al., 2008) (Table 4).

There is genetic diversity among isolates of S. citri based on the Crossed Immunoelectrophoresis (CIE) with intermediate gel and polyacrylamide gel electrophoresis, three repetitive extragenic palindromic elements (BOX, ERIC and REP), random amplified polymorphic DNA (RAPD) and spiroplasma bacteriophage insertions as discriminative techniques (Mello et al., 2006, 2008; Omar et al., 2006).

Control: Stablish S. citri –free mother trees and citrus nurseries in locations where very low or no spread of S. citri occur. Elimination of brassicaceous weed hosts within and around citrus groves.

Table 4: Several oligonucleotide primers used for spiroplasma detection by PCR and real-time PCR

Budwood should be taken from clean propagative materials and healthy trees. Trees that appear diseased and showing symptoms or abnormally stunted should be removed and replaced with healthy replants or more tolerant varieties. Use of trap plants such as sugarbeet which is leafhopper attractive but not host of S. citri can be reduced the incidence of stubborn disease in the citrus orchards. Although S. citri is highly sensitive to tetracylines in vitro but is not practical (Bowyer and Calavan, 1974; Fletcher et al., 2006; Gumpf and Calavan, 1981; Saglio et al., 1973; Whiteside et al., 1988).

REFERENCES
Abalain-Colloc, M.L., C. Chastel, J.G. Tully, J.M. Bove, R.F. Whitcomb, B. Gilot and D.L. Williamson, 1987. Spiroplasma sabaudiense sp. nov. from Culex tritaeniorhynchus mosquitoes collected in France. Int. J. Syst. Bacteriol., 37: 260-265.

Abalain-Colloc, M.L., L. Rosen, J.G. Tully, J. M. Bove, C. Chastel and D.L. Williamson, 1988. Spiroplasma taiwanense sp. nov. from Culex tritaeniorhynchus mosquitoes collected in Taiwan. Int. J. Syst. Bacteriol., 38: 103-107.
CrossRef  |  

Adams, J.R., R.F. Whitcomb, J.G. Tully, E.A. Clark and D.L. Rose et al., 1997. Spiroplasma alleghenense sp. nov., a new species from the scorpionfly Panorpa helena (Mecoptera, Panorpidae). Int. J. Syst. Bacteriol., 47: 759-762.
CrossRef  |  

Allen, R.M. and C.R. Donndelinger, 1981. Transmission of Spiroplasma citri by two leafhopper vectors in Arizona. Phytopathology, 71: 856-856.
Direct Link  |  

Allen, R.M., 1975. Spiroplasma organism found in naturally infected periwinkle. Citrograph, 60: 428-446.

Ammar, E.D., D. Fulton, X. Bai, T. Meulia and S.A. Hogenhout, 2004. An attachment tip and pili-like structures in insect- and plant-pathogenic spiroplasmas of the class Mollicutes. Arch. Microbiol., 181: 97-105.
CrossRef  |  

Andre, A., M. Maucourt, A. Moing, D. Rolin and J. Renaudin, 2005. Sugar import and phytopathogenicity of Spiroplasma citri: Glucose and fructose play distinct roles. Mol. Plant Microbe. Interact, 18: 32-42.
PubMed  |  Direct Link  |  

Archer, B.D. and J. Best, 1980. Serological relatedness of spiroplasmas estimated by enzyme-linked immunosorbent assay and crossed immunoelectrophoresis. J. Gen. Microbiol., 119: 413-422.
CrossRef  |  

Archer, D.B., R. Towsend and P.G. Markham, 1982. Detection of Spiroplasma citri in plants and insect hosts by ELISA. Plant Pathol., 31: 299-306.
CrossRef  |  

Bove, J.M., 1986. Stubborn and its natural transmission in the Mediterranean area and the Near East. FAO Plant Prot. Bull. 34: 15-23.
Direct Link  |  

Bove, J.M., 1988. Spiroplasma citri. In: European Handbook of Plant Diseases, Smith, I.M., J. Dunez, R.A. Lelliott, D.H. Phillips and S.A. Archer (Eds.). Blackwell Scientific Publications, Oxford, UK., ISBN-13: 9780632012220, pp: 129-131.

Bove, J.M., 1995. Virus and Virus-Like Diseases of Citrus in the Near East Region. FAO, Rome, Italy, ISBN-13: 9789251038277, Pages: 518.

Bove, J.M., 1997. Spiroplasmas: Infectious agents of plants, arthropods and vertebrates. Wien. Klin. Wochenschr., 109: 604-612.
PubMed  |  

Bove, J.M., A. Fos, J. Lallemand, A. Raie, Y. Ali and N. Ahmed, 1986. Epidemiology of Spiroplasma citri in the old world. Proceedings of the 10th International Organization of Citrus Virology Conference, (IOCV'86), Riverside, USA., pp: 295-299.

Bowyer, J.W. and E.C. Calavan, 1974. Antibiotic sensitivity in vitro of the mycoplasma-like organism associated with citrus stubborn disease. Phytopathology, 64: 346-349.

Calavan, E.C. and G.N. Oldfield, 1979. Symptomatology of Spiroplasmal Plant Diseases. In: The Mycoplasmas, Whitcomb, R.F. and J.G. Tully (Eds.). Vol. 3, Academic Press, New York, pp: 37-64.

Calavan, E.C. and J.B. Carpenter, 1965. Stubborn disease of citrus retards and growth, impairs quality and decrease yields. Calif. Citrogr., 50: 86-87.

Calavan, E.C., 1968. A review of stubborn and greening disease of citrus. Proceedings of the 4th International Organization of Citrus Virology Conference, (IOCV'68), Riverside, USA., pp: 105-117.

Calavan, E.C., 1979. Symptoms of stubborn disease and the culture of Spiroplasma citri. Procoeeding of the Republic of China-United States Cooperative Science Seminar on Mycoplasma Diseases of Plants, (CSSMDP'79), National Science Council, Republic of China, pp: 67-72.

Calavan, E.C., 1980. Stubborn. In: Description and Illustration of Virus and Virus-Like Diseases of Citrus: A Collection of Color Slides, Bove, J.M. and R. Vogel (Eds.). Vol. 3, IRFA, Paris,.

Carle, P., C. Saillard and J.M. Bove, 1983. Determination of guanine plus cytosine content of DNA. Meth. Mycoplasmol., 1: 301-308.

Carle, P., C. Saillard, N. Carrere, S. Carrere and S. Duret et al., 2010. Partial chromosome sequence of Spiroplasma citri reveals extensive viral invasion and important gene decay. Applied Environ. Microbiol., 76: 3420-3426.
CrossRef  |  

Carle, P., D.L. Rose, J.G. Tully and J.M. Bove, 1992. The genome size of spiroplasmas and other mollicutes. IOM Lett., 2: 263-263.

Carle, P., F. Laigret, J.G. Tully and J.M. Bove, 1995. Heterogeneity of genome sizes within the genus spiroplasma. Int. J. Syst. Bacteriol., 45: 178-181.
CrossRef  |  

Carle, P., R.F. Whitcomb, K.J. Hackett, J.G. Tully and D.L. Rose et al., 1997. Spiroplasma diabroticae sp. nov., from the southern corn rootworm beetle Diabrotica undecimpunctata (Coleoptera, Chrysomelidae). Int. J. Syst. Bacteriol., 47: 78-80.
CrossRef  |  

Chen, T.A. and C.H. Liao, 1975. Corn stunt spiroplasma: Isolation, cultivation and proof of pathogenicity. Science, 188: 1015-1017.
CrossRef  |  

Childs, J.F.L. and J.B. Carpenter, 1960. Observations on stubborn and other diseases of citrus in Morocco in 1959. Plant Dis. Rep., 44: 920-927.

Citti, C., L. Marechal-Drouard, C. Saillard, J.H. Weil and J.M. Bove, 1992. Spiroplasma citri UGG and UGA tryptophan codons: Sequence of the two tryptophanyl-tRNAs and organization of the corresponding genes. J. Bacteriol., 174: 6471-6478.
Direct Link  |  

Clark, M.F., C.L. Flegg, M. Bar-Joseph and S. Rottem, 1978. The detection of Spiroplasma citri by Enzyme-linked Immunosorbent Assay (ELISA). J. Phytopathol., 92: 332-337.
CrossRef  |  

Clark, T.B., R.F. Whitcomb, J.G. Tully, C. Mouches and C. Saillard et al., 1985. Spiroplasma melliferum, a new species from the honeybee (Apis mellifera). Int. J. Syst. Bacteriol., 35: 296-308.
CrossRef  |  

Davis, R.E. and J.F. Worley, 1973. Spiroplasma: Motile, helical microorganism associated with corn stunt disease. Phytopathology, 63: 403-408.
Direct Link  |  

Davis, R.E., I.M. Lee and J.F. Worley, 1981. Spiroplasma floricola, a new species isolated from surfaces of flowers of the tulip tree, Liriodendron tulipifera L. Int. J. Syst. Bacteriol., 31: 456-464.
CrossRef  |  

Davis, R.E., R.F. Whitcomb, T.A. Chen and R.R. Granados, 1972. Current Status of the Aetiology of Corn Stunt Disease. In: Pathogenic Mycoplasmas, Elliott, K. and J. Birch (Eds.). Elsevier-Excerpta, Amsterdam, Medica-North-Holland, pp: 205-225.

Duret, S., N. Berho, J.L. Danet, M. Garnier and J. Renaudin, 2003. Spiralin is not essential for helicity, motility, or pathogenicity but is required for efficient transmission of Spiroplasma citri by its leafhopper vector Circulifer haematoceps. Applied Environ. Microbiol., 69: 6225-6234.
CrossRef  |  

El-Banna, O.H.M., A. Zeid, A.A. Fawzya, I. Moursy and A.G. Farag, 2005. Immunocapture polymerase Chain reaction (I C- PCR) and nucleic acid hybridization techniques for detection of Spiroplasma citri. Int. J. Virol., 1: 13-13.
CrossRef  |  Direct Link  |  

Fawcett, H.S., J.C. Perry and J.C. Johnston, 1944. The stubborn disease of citrus. Calif. Citrog., 29: 146-147.

Fletcher, J., 1983. Brittle root of horseradish in Illinois and the distribution of Spiroplasma citri. Phytopathology, 73: 354-357.
Direct Link  |  

Fletcher, J., 1987. Filter paper dot-immunobinding assay for detection of of Spiroplasm acitri. Applied Environ. Microbiol., 53: 183-184.
PubMed  |  

Fletcher, J., U. Melcher and A. Wayadande, 2006. The phytopathogenic spiroplasmas. Prokaryotes, 4: 905-947.
CrossRef  |  

Foissac, X., C. Saillard, J. Gandar, L. Zreik and J.M. Bove, 1996. Spiralin polymorphism in strains of S. citri is not due to differences in posttranslational palmitoylation. J. Bacteriol., 178: 2934-2940.

French, F.E., R.F. Whitcomb, J.G. Tully, P. Carle and J.M. Bove et al., 1997. Spiroplasma lineolae, sp. nov. from the horse fly Tabanus lineola (Diptera, Tabanidae). Int. J. Syst. Bacteriol., 47: 1078-1081.
CrossRef  |  

Gasparich, G.E., 2002. Spiroplasmas: Evolution, adaptation and diversity. Front Biosci., 7: 619-640.
PubMed  |  

Gasparich, G.E., 2010. Spiroplasmas and phytoplasmas: Microbes associated with plant hosts. Biologicals, 38: 193-203.
CrossRef  |  

Gasparich, G.E., R.F. Whitcomb, D. Dodge, F.E. French, J. Glass and D.L. Williamson, 2004. The genus Spiroplasma and its nonhelical descendants: Phylogenetic classification, correlation with phenotype, and roots of the Mycoplasma mycoides clade. Int. J. Syst. Evol. Microbiol., 54: 893-918.
CrossRef  |  PubMed  |  

Gaurivaud, P., J.L. Danet, F. Laigret, M. Garnier and J.M. Bove, 2000. Fructose utilization and phytopathogenicity of Spiroplasma citri. Mol. Plant Microbe. Interact, 13: 1145-1155.
PubMed  |  Direct Link  |  

Granett, A.L., R.L. Blue, M.K. Harjung, E.C. Calavan and D.J. Gumpf, 1976. Occurrence of Spiroplasma citri in periwinkle in California. Calif. Agric., 30: 18-19.
Direct Link  |  

Gumpf, D.J. and E.C. Calavan, 1981. Stubborn Disease of Citrus. In: Mycoplasma Diseases of Trees and Shrubs, Maramorosch, K. and S.P. Raychaudhuri (Eds.). Academic Press, New York, pp: 97-134.

Guo, Y.H., T.A. Chen, R.F. Whitcomb, D.L. Rose and J.G. Tully et al., 1990. Spiroplasma chinense sp. nov. from flowers of Calystegia hederacea in China. Int. J. Syst. Bacteriol., 40: 421-425.
CrossRef  |  

Hackett, K.J., R.F. Whitcomb, F.E. French, J.G. Tully and G.E. Gasparich et al., 1996. Spiroplasma corruscae sp. nov., from a firefly beetle (Coleoptera, Lampyridae) and tabanid flies (Diptera, Tabanidae). Int. J. Syst. Bacteriol., 46: 947-950.
CrossRef  |  

Hackett, K.J., R.F. Whitcomb, J.G. Tully, D.L. Rose and P. Carle et al., 1993. Spiroplasma insolitum sp. nov., a new species of group I Spiroplasma with an unusual DNA base composition. Int. J. Syst. Bacteriol., 43: 272-277.
CrossRef  |  

Hackett, K.J., R.F. Whitcomb, T.B. Clark, R.B. Henegar and D.E. Lynn et al., 1996. Spiroplasma leptinotarsae sp. nov., a mollicute uniquely adapted to its host, the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera, Chrysomelidae). Int. J. Syst. Bacteriol., 46: 906-911.
CrossRef  |  

Helias, C., M. Vazeille-Falcoz, F. Le Goff, M.L. Abalain-Colloc and F. Rodhain et al., 1998. Spiroplasma turonicum sp. nov., from Haematopota horse flies (Diptera: Tabanidae) in France. Int. J. Syst. Bacteriol., 48: 457-461.
Direct Link  |  

Hung, S.H.Y., T.A. Chen, R.F. Whitcomb, J.G. Tully and Y.X. Chen, 1987. Spiroplasma culicicola, sp. nov., a new species from the salt marsh mosquito Aedes sollicitans. Int. J. Syst. Bacteriol., 37: 365-370.
CrossRef  |  

Kaloostian, G.H., G.N. Oldfield, H.D. Pierce and E.C. Calavan, 1979. Spiroplasma citri and Its Transmission to Citrus and Other Plants by Leafhoppers. In: Leafhopper Vectors and Plant Disease Agents, Maramorosch, K. and K.F. Harris (Eds.). Academic Pres, New York, pp: 447-450.

Kersting, U., C. Sengonca and A. Cinar, 1992. Detection of Spiroplasma citri in non-citrus host plants and their associated leafhopper vectors in Southern Turkey. FAO Plant Prot. Bull., 40: 89-94.

Kersting, U., H. Bagpinar, A. Cinar, C. Sengonca and N. Uygun, 1993. New findings on the epidemiology of Spiroplasma citri in the Eastern Mediterranean Region of Turkey. Proceedings of the 12th International Organization of Citrus Virology Conference, (IOCV'93), Riverside, USA., pp: 336-341.

Klein, M., P. Rasooly and B. Raccah, 1988. New findings on the transmission of Spiroplasma citri, the citrus stubborn disease agent in Israel, by a beet leafhopper from the Jordan valley. Hassadeh, 68: 1736-1737.

Konai, M., R.F. Whitcomb, F.E. French, J.G. Tully and D.L. Rose et al., 1997. Spiroplasma litorale sp. nov., from tabanid flies (Diptera, Tabanidae) in the Southeastern United States. Int. J. Syst. Bacteriol., 47: 359-362.
CrossRef  |  

Konai, M., R.F. Whitcomb, J.G. Tully, D.L. Rose and P. Carle et al., 1995. Spiroplasma velocicrescens sp. nov., from the vespid wasp monobia quadridens. Int. J. Syst. Bacteriol., 45: 203-206.
CrossRef  |  

Lee, I.M. and R.E. Davis, 1978. Identification of some growth-promoting components in an enriched cell-free medium for cultivation of Spiroplasma citri. Phytopathol. News, 12: 215-215.

Lee, I.M. and R.E. Davis, 1984. New media for rapid growth of Spiroplasma citri and corn stunt spiroplasma. Phytopathology, 74: 84-89.
CrossRef  |  

Lee, I.M., K.D. Bottner, J.E. Munyaneza, R.E. Davis, J.M. Crosslin, L.J. du Toit and T.T. Crosby, 2006. Carrot purple leaf: A new spiroplasmal disease associated with carrots in Washington State. Plant Dis., 90: 989-993.

Lee, I.M., R.E. Davis and J. Fletcher, 2001. Cell-Wall Free Bacteria. In: Laboratory Guide for Identification of Plant Pathogenic Bacteria, Schaad, N.W., J.B. Jones and W. Chun (Eds.). APS Press St. Paul, MN., USA., pp: 283-320.

Lin, C.P. and T.A. Chen, 1985. Production of monoclonal antibodies against Spiroplasma citri. Phytopathology, 75: 848-851.
CrossRef  |  

Markham, P.G. and D. Towsend, 1974. Transmission of Spiroplasma citri to Plant. In: Les Mycoplasmes/Mycoplasmas, Bove, J.M. and J.F. Duplan, (Eds.). INSEAM, Paris, pp: 201-206.

Melcher, U. and J. Fletcher, 1999. Genetic variation in Spiroplasma citri. Eur. J. Plant Pathol., 105: 519-533.
CrossRef  |  

Mello, A.F., R.K. Yokomi, U. Melcher, J. Chen and J. Fletcher, 2006. Assessment of genetic diversity in Spiroplasma citri by RAPD, rep-PCR and bacteriophage primers. Phytopathology, 96: S77-S77.
Direct Link  |  

Mello, A.F.S., A.C. Wayadande, R.K. Yokomi and J. Fletcher, 2009. Transmission of different isolates of Spiroplasma citri to carrot and citrus by Circulifer tenellus (Hemiptera: Cicadellidae). J. Econ. Entomol., 102: 1417-1422.
CrossRef  |  

Mello, A.F.S., R.K. Yokomi, U. Melcher, J.C. Chen, A.C. Wayadande and J. Fletcher, 2008. Genetic diversity of Spiroplasma citri strains from different regions, hosts and isolation dates. Phytopathology, 98: 960-968.
PubMed  |  Direct Link  |  

Mouches, C., J.M. Bove, J.G. Tully, D.L. Rose and R.E. McCoy et al., 1983. Spiroplasma apis, a new species from the honey-bee Apis mellifera. Ann. Inst. Microbiol., 134: 383-397.
CrossRef  |  

Nejat, N., G. Vadamalai, K. Sijam and M. Dickinson, 2011. First report of Spiroplasma citri associated with periwinkle lethal yellows in southeast Asia. Plant Dis.,

Nejat, N., H. Rahimian and M. Salehi, 2004. Herbaceous hosts of citrus stubborn disease agent in Fars province of Iran. Proceedings of the 16th Conference International Organization of Citrus Virology, (IOCV'04), Riverside, USA., pp: 89-89.

Nejat, N., H. Rahimian and M. Salehi, 2006. Herbaceous hosts of citrus stubborn disease agent in Fars province of Iran. Iran. J. Plant Pathol., 44: 121-124.

Nejat, N., M. Salehi, M. Fayyazi and K. Izadpanah, 2007. Survey of sweet orange cultivars for stubborn disease resistance in Iran. Bull. Insectol., 60: 305-306.
Direct Link  |  

Nunan, L.M., D.V. Lightner, M.A. Oduori and G.E. Gasparich, 2005. Spiroplasma penaei sp. nov., associated with mortalities in Penaeus vannamei, Pacific white shrimp. Int. J. Syst. Evol. Microbiol., 55: 2317-2322.
CrossRef  |  

Nur, I., J.M. Bove, C. Saillard, S. Rottem, R.M. Whitcomb and S. Razin, 1986. DNA probes in detection of spiroplasmas and mycoplasma-like organisms in plants and insects. FEMS Microbiol. Lett., 35: 157-162.
CrossRef  |  

O`Hayer, K.W., G.A. Schultz, C.E. Eastman, J. Fletcher and R.M. Goodman, 1983. Transmission of Spiroplasma citri by the aster leafhopper, Macrosteles fascifrons (Homoptera: Cicadellidae). Ann. Appl. Biol., 102: 311-318.
CrossRef  |  

Oldfield, G.N. and E.C. Calavan, 1980. Spiroplasma citri: Non-Rutaceous Hosts. In: Description and Illustration of Virus and Virus-Like Diseases of Citrus, Bove, J.M. and R. Vogel (Eds.). IRFA SETCO-FRUITS, Paris.

Oldfield, G.N., 1988. Ecological Associations of Spiroplasma citri with Insects, Plants and Other Plant Mycoplasmas in the Western United States. In: Mycoplasma Diseases of Crops: Basic and Applied Aspects, Maramorosch, K. and S.P. Raychaudhuri (Eds.). Springer-Verlag, New York, USA., pp: 175-191.

Oldfield, G.N., G.H. Kaloostian, H.D. Pierce, E.C. Calavan and A.L. Granett et al., 1977. Transmission of Spiroplasma citri from citrus to citrus by Scaphytopius nitrides. Phytopathology, 67: 763-765.
CrossRef  |  

Oldfield, G.N., G.H. Kaloostian, H.D. Pierce, E.C. Calavan, A.L. Granett and R.L. Blue, 1976. Beet leafhopper transmits citrus stubborn disease. Calif. Agric., 30: 15-15.
Direct Link  |  

Omar, A.F., K. Sijam, I. Sulaiman, H. Hashim and O.H.M. El-Banna, 2006. Comparison of two Egyptian isolates of Spiroplasma citri by crossed immunoelectrophoresis and polyacrylamide gel electrophoresis of cell proteins. Plant Pathol. J., 5: 88-91.
CrossRef  |  Direct Link  |  

Rangel, B., R.R. Krueger and R.F. Lee, 2005. Current research on Spiroplasma citri in California. Proceedings of the 16th International Organization of Citrus Virology Conference, (IOCV'05), Riverside, CA., pp: 439-441.

Renaudin, J., M.C. Pascarel, C. Saillard, C. Chevalier and J.M. Bove, 1986. Among the spiroplasmas codon UGA is not non-sense and appears coding for the tryptophan. C.R. Acad. Sci., 303: 539-540.

Saglio, P., D. Lafleche, D.C. Bonisol and J.M. Bove, 1971. Isolation and culture in vitro mycoplasma associated with the stubborn of citrus fruits and their observation in electronic microscope. C.R. Acad. Sci., 272: 1387-1390.

Saglio, P., M.L. Hospital, D. Lafleche, G. Dupont, J.M. Bove, J.G. Tully and E.A. Freundt, 1973. Spiroplasma citri gen. and sp. n.: A mycoplasma-like organism associated with stubborn disease of citrus. Int. J. Syst. Bact., 23: 191-204.
CrossRef  |  Direct Link  |  

Saillard, C., A. Nhami, P. Moreno, M. Garnier and J.M. Bove, 1996. Spiroplasma citri detection by immuno-capture PCR. Proceedings of the 13th International Organization of Citrus Virology Conference, (IOCV'96), Riverside, CA., pp: 413-413.

Saillard, C., C. Barthe, J. Renaudin, J.M. Bove and P. Moreno, 1993. Detection of Spiroplasma citri by culture, ELISA, dot-blot hybridization, PCR and immuno-capture PCR: An evaluation. Proceedings of the 12th International Organization of Citrus Virology Conference, (IOCV'93), Riverside, CA., pp: 467-467.

Saillard, C., J.C. Vignault, J.M. Bove, A. Raie and J.G. Tully et al., 1987. Spiroplasma phoeniceum sp. nov., a new plant-pathogenic species from Syria. Int. J. Syst. Bacteriol., 37: 106-115.
CrossRef  |  

Saillard, C., O. Garcia-Jurado, J.M. Bove, J.C. Vignault and G. Moutous et al., 1980. Application of ELISA to the detection of Spiroplasma citri in plants and insects. Proceedings of the 8th International Organization of Citrus Virology Conference, (IOCV'80), Riverside, CA., pp: 145-152.

Salehi, M. and K. Izadpanah, 2002. A disease of sesame in Iran caused by Spiroplasma citri. Proceedings of the 15th International Organization of Citrus Virology Conference, (IOCV'02), Riverside, CA., pp: 401-401.

Stamburski, C., J. Renaudin and J.M. Bove, 1992. Mutagenesis of a tryptophan codon from TGG to TGA in the CAT gene does not affect the expression of the CAT gene in Spiroplasma citi. Gene, 110: 133-134.

Stevens, C., A.Y. Tang, E. Jenkins, R.L. Goins and J.G. Tully et al., 1997. Spiroplasma lampyridicola sp. nov., from the firefly beetle Photuris pennsylvanicus. Int. J. Syst. Bacteriol., 47: 709-712.
CrossRef  |  

Towsend, R., P.G. Markham and K.A. Plaskitt, 1977. Multiplication and morphology of Spiroplasma citri in the leafhopper Euscelis plebejus. Ann. Applied Biol., 87: 307-313.
CrossRef  |  

Tully, J.G., D.L. Rose, C.E. Yunker, P. Carle, J.M. Bove, D.L. Williamson and R.F. Whitcomb, 1995. Spiroplasma ixodetis sp. nov., a new species from Ixodes pacificus ticks collected in Oregon. Int. J. Syst. Bacteriol., 45: 23-28.
CrossRef  |  

Tully, J.G., D.L. Rose, E. Clark, P. Carle and J.M. Bove et al., 1987. Revised group classification of the genus Spiroplasma (Class Mollicutes), with proposed new groups XII to XXIII. Int. J. Sys. Bacteriol., 37: 357-364.
CrossRef  |  

Tully, J.G., R.F. Whitcomb, D.L. Rose and J.M. Bove, 1982. Spiroplasma mirum, a new species from rabbit ticks (Haemaphysalis leporispalustris). Int. J. Syst. Bacteriol., 32: 92-100.
CrossRef  |  

Tully, J.G., R.F. Whitcomb, J.M. Bove and P. Saglio, 1973. Plant mycoplasmas: Seiological relationship between agents associated with citrus stubborn and corn stunt diseases. Science, 182: 827-829.

Wang, W., W. Gu, G.E. Gasparich, K. Bi and J. Ou et al., 2010. Spiroplasma eriocheiris sp. nov., a novel species associated with mortalities in Eriocheir sinensis, Chinese mitten crab. Int. J. Syst. Evol. Microbiol., 10.1099/ijs.0.020529-0

Whitcomb, R.F, J.M. Bove, T.A. Chen, J.G. Tully and D.L. Williamson, 1987. Proposed criteria for an interim serogroup classification for members of the genus Spiroplasma (class Mollicutes). Int. J. Syst. Bacteriol., 37: 82-84.
CrossRef  |  

Whitcomb, R.F. and J.G. Tully, 1982. Taxonomy and identification of spiroplasmas. Rev. Infec. Dis., 4: S148-S153.
CrossRef  |  

Whitcomb, R.F., 1977. International committee on systematic bacteriology. Subcommittee on the taxonomy of Mycoplasmatales. Minutes of the interim meeting, 22 September 1976, London, United Kingdom. Int. J. Syst. Bacteriol., 27: 392-394.

Whitcomb, R.F., 1983. Culture Media for Spiroplasmas. In: Methods in Mycoplasmology, Razin, S. and J.G. Tully (Eds.). Academic Press, New York, pp: 147-159.

Whitcomb, R.F., C. Chastel, M. Abalain-Colloc, C. Stevens and J.G. Tully et al., 1993. Spiroplasma cantharicola sp. nov., from cantharid beetles (Coleoptera: Cantharidae). Int. J. Syst. Bacteriol., 43: 421-424.
CrossRef  |  

Whitcomb, R.F., F.E. French, J.G. Tully, D.L. Rose and P.M. Carle et al., 1997. Spiroplasma montanense sp. nov., from Hybomitra horse flies at northern latitudes in North America. Int. J. Syst. Bacteriol., 47: 720-723.
CrossRef  |  

Whitcomb, R.F., F.E. French, J.G. Tully, G.E. Gasparich and D.L. Rose et al., 1997. Spiroplasma chrysopicola sp. nov., Spiroplasma gladiatoris sp. nov., Spiroplasma helicoides sp. nov. and Spiroplasma tabanidicola sp. nov., from tabanid (Diptera: Tananidae) flies. Int. J. Syst. Bacteriol., 47: 713-719.
CrossRef  |  

Whitcomb, R.F., G.E. Gasparich, F.E. French, J.G. Tully and D.L. Rose et al., 1996. Spiroplasma syrphidicola, sp. nov., from a syrphid (Diptera, Syrphidae) fly. Int. J. Syst. Bacteriol., 46: 797-801.
CrossRef  |  

Whitcomb, R.F., J.C. Vignault, J.G. Tully, D.L. Rose and P. Carle et al., 1993. Spiroplasma clarkii sp. nov., a new species from the green June beetle (Coleoptera: Scarabaeidae). Int. J. Syst. Bacteriol., 43: 261-265.
CrossRef  |  

Whitcomb, R.F., J.G. Tully, D.L. Rose, P. Carle and J.M. Bove et al., 1993. Spiroplasma monobiae sp. nov. from the vespid wasp Monobia quadridens (Hymenoptera: Vespidae). Int. J. Syst. Bacteriol., 43: 256-260.
CrossRef  |  

Whitcomb, R.F., T.A. Chen, D.L. Williamson, C. Liao and J.G. Tully et al., 1986. Spiroplasma kunkelii sp. nov., characterization of the etiological agent of corn stunt disease. Int. J. Syst. Bacteriol., 36: 170-178.
CrossRef  |  

Whiteside, J.O., S.M. Garnsey and L.W. Timmer, 1988. Compendium of Citrus Diseases. Association for Psychological Science, St. Paul, Minnesota. pp: 80.

Williamson, D.L, R.F. Whitcomb, J.G. Tully, G.E. Gasparich and D.L. Rose et al., 1998. Revised group classification of the genus Spiroplasma. Int. J. Syst. Bacteriol., 48: 1-12.
CrossRef  |  

Williamson, D.L. and R.F. Whitcomb, 1975. Plant mycoplasmas: A cultivable spiroplasma cause corn stunt disease. Science, 188: 1018-1020.
CrossRef  |  

Williamson, D.L., B. Sakaguchi, K.J. Hackett, R.F. Whitcomb and J.G. Tully et al., 1999. Spiroplasma poulsonii sp. nov., a new species associated with male-lethality in Drosophila willistoni, a neotropical species of fruit fly. Int. J. Syst. Bacteriol., 49: 611-618.

Williamson, D.L., G.E. Gasparich, L.B. Regassa, C. Saillard, J. Renaudin, J.M. Bove and R.F. Whitcomb, 2010. Family II. Spiroplasmataceae. In: Bergey's Manual of Systematic Bacteriology, Krieg, N.R., J.T. Staley, D.R. Brown, B. Hedlund and B.J. Paster (Eds.). 2nd Edn., Springer, New York, pp: 338-370.

Williamson, D.L., J.G. Tully, L. Rosen, D.L. Rose and R.F. Whitcomb et al., 1996. Spiroplasma diminutum, sp. nov., from Culex annulus mosquitoes collected in Taiwan. Int. J. Syst. Bacteriol., 46: 229-233.
CrossRef  |  

Williamson, D.L., J.R. Adams, R.F. Whitcomb, J.G. Tully and P. Carle et al., 1997. Spiroplasma platyhelix sp. nov., a new mollicute with unusual morphology and genome size from the dragonfly Pachydiplax longipennis. Int. J. Syst. Bacteriol., 47: 763-766.
CrossRef  |  

Yokomi, R.K., A.F.S. Mello, M. Saponari and J. Fletcher, 2008. Polymerase chain reaction-based detection of Spiroplasma citri associated with citrus stubborn disease. Plant Dis., 92: 253-260.

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