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Spiroplasma Citri: Fifteen Years of Research

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Spiroplasma Citri: Fifteen Years of Research Spiroplasma citri: Fifteen Years of Research J. M. Bove Dedicated to Richard Guillierme* I-HISTORICAL SIGNIFICANCE mas, molecular and cellular biology of OF SPIROPLASMA CITRI spiroplasmas, spiroplasma pathogen- icity, ecology of Spiroplasma citri, It is now well recognized that the biology and ecology of Spiroplasma agent of citrus stubborn disease was kunkelii. Volume IV of IOCV's Virus the first mollicute of plant origin to and Virus-like diseases of citrus (7) have been cultured (19, 33) and for also covers isolation, cultivation and which Koch's postulates were fulfilled characterization of S. citri. Stubborn (25). The serological, biological and disease has been reviewed (24). biochemical characterizations of the Methods in Mycoplasmology offers in citrus agent revealed it to be a new two volumes the techniques used in mollicute, one with helical morphol- the study of mollicutes including the ogy and motility (34), hence the name spiroplasmas (30, 37). These proceed- Spiroplasma citri, adopted from ings also cover epidemiology of S. Davis et al. (14, 15) who had given citri in the Old World (4) and spiro- the trivial name spiroplasma to helical plasma gene structure and expression filaments seen in corn stunt infected plants. These "helices" were cultured (5). and shown to be the agent of corn stunt disease in 1975 (9,44); the agent 11-MAJOR PROPERTIES is now called S~iro~lasmakunkelii OF SPIROPLASMA CITRl (40). The first bre;kthrough in the study of yellows diseases came in 1967 Spiroplasma citri is a mollicute with the discovery of mollicute-like (42). Mollicutes are prokaryotes that organisms (MLO) in plants (17). Cul- have evolved by degenerative evolu- ture of the stubborn agent was the tion from low guanine plus cytosine next important advance since it not (G + C) Gram positive bacteria. only offered a model for the study of While the bacterial cell has a pep- plant mollicutes, but also revealed the tidoglycane-containing cell wall, S. existence of a whole new world of citri, as a mollicute, has no cell wall microorganisms: the spiroplasmas, of and, hence, no peptidoglycane. which more than 30 different species Penicillin inhibits one of the last steps or serogroups are known today (42). in peptidoglycane biosynthesis. S. Many reviews on S. citri and other citri, with no peptidoglycane, is in- spiroplasmas have appeared (2, 12, sensitive to penicillin, but not to tet- 13, 39, 42). Be it enough to mention racycline and erythromycine, antibio- volume V of the Mycoplasmas (43), a tics that inhibit protein biosynthesis. revised edition of volume I11 (41), en- On solid medium, S. citri produces tirely devoted to plant and insect mol- fried egg-shaped (umbonate) colonies. licutes with chapters on the following Under certain environmental condi- topics: the genus Spiroplasma, tions, bacterial forms can be obtained spiroplasma-insect host relationships, which lack cell walls (bacterial L vari- nutrition and cultivation of spiroplas- ants). They also show umbonate col- onies. Thus. this articular colonv morphology is related to the absenie *Director General of Institut de Recherches of cell wall. sur les Fruits et Agrumes (IRFA) from 1942 to The various mollicutes that were 1973. known in animals before the discov- Diseases Induced by Procaryotic Pathogens ery of the spiroplasmas were acids from acetate. The type of fatty pleiomorphic and did not have a de- acids in the S. dtri membrane de- fined shape. Therefore, the helical pends on the fatty acid composition of morphology of S. citri was entirely the growth medium. S. citri derives unexpected. In addition, the helical its energy for growth from the fer- spiroplasma cells are motile, with mentation of glucose to organic acids, flexional and twitching movements, and the hydrolysis of arginine to yield and often show an apparent rotatory C02, NH, and ATP. The production motility. Flagella, periplasmic fibrils, of acid from glucose during S. citri or other organelles of locomotion are growth can be conveniently followed not present, but intracellular fibrils by the color-shift from red to yellow have been demonstrated. Motility of of the phenol red pH-indicator added S. citri is revealed in the colony mor- to the culture medium. Oxygen is not phology in that the umbonate colonies required for growth. S. citri is a facul- are diffuse, often with satellite col- tative anaerobe. The stubborn agent onies developing from foci adjacent to grows best in a narrow range of tem- the initial site of colony development. peratures centered around 32 C. This Poorly helical, nonmotile variants of explains why stubborn disease is well S. citri are known; their colonies expressed in hot climates, but not in exhibit a typical umbonate appear- those where temperatures above 30 ance with sharp margins and without C are rarely approached. satellite colonies. Growth and division of S. citri has In liquid medium of low viscosity, attracted much attention (21,22). The spiroplasmas do not achieve appreci- smallest helical spiroplasma cell, or able translational motility. Only when helix, was found to be a one- to two- the viscosity is increased by incorpo- turn helix (elementary helix). Such ration of agar or methylcellulose in cells increase in length into parental the medium can the spiroplasmas use helices which divide by constriction, their motility to move along (12b). liberating elementary helices. The Spiroplasmas display chemotaxis i. e., most frequently dividing parental they are attracted by certain sub- helix is one with approximately four stances and repelled by others (12b). turns, yielding two elementary Chemotaxis may be involved in the helices. At the unfavorable tempera- movement of S. citri in the phloem ture of 37 C, the number of short elements. Mutants have recently helices decreases drastically in favor been obtained that are devoid of of long helices with very few constric- motility but have retained their heli- tions, showing that the organism can cal morphology (Cohen & Williamson, still elongate, but not divide; division personal communication). This shows resumes at 32 C. During elongation that helical morphology and motility of an elementary helix, growth seems are genetically independent. to start at one end of the helix (polar Mollicutes of the genus Mycop- growth). lasma, Ureaplasm or Anaerop- In vitro, during log-phase growth, lasm require sterol for growth; all S. citri cells are found to be helical. those of the genus Acholeplasma or The situation is less simple when the Asteroleplasm do not. S. citri and spiroplasmas are studied in the tis- all other spiroplasmas need sterol in sues or cells of their hosts. In S. citri- their growth medium. The sterol infected plants, helical forms can al- (cholesterol) is generally supplied by ways be seen in the sieve tubes, but addition of horse or foetal calf serum nonhelical forms seem to exist too. In (10-20%) in the culture medium. The plants naturally infected with both a serum also supplies fatty acids. These MLO and S. citri (I), the symptoms are required for growth as the spiro- are generally those induced by the plasmas are unable to synthesize fatty MLO and in the sieve tubes the MLO Tenth ZOCV Conference cells outnumber the S. citri cells; the principal vector (4). For both vectors, latter might be difficult to see by elec- Salsola kali L (Russian thistle or tron microscopy. However, their tumbleweed), a Chenopodiaceae, is a presence can be detected by culturing major host plant. The discovery of the spiroplasma from such plants periwinkles naturally infected with S. (MLOs have not yet been obtained in citri in Arizona, California and culture). In contrast to the situation Morocco showed S. citri is not limited in culture media and in plants, the to citrus in nature. For instance, in morphology of S. citri is not helical in California, several species in the leafhoppers. No helical forms are seen Brassicaceae family are infected with either in the hemolymph or in any S. citri (27). In Illinois, brittle-root other tissues and all spiroplasma cells disease of horseradish is the second appear roughly spherical. S. citri can crop disease found to be caused by S. be shown to absorb to, and to be pres- citri (18). ent in cultured leafhopper cells. The S. citri is serologically related to identity of the non-helical forms in the S. melliferum a spiroplasma patho- insect cells as S. citri was de- genic to honeybees, S. kunkelii, the monstrated by immunofluorescence; corn stunt agent, and S. phoeniceum, and their viability demonstrated by a new plant pathogen recently discov- incorporation of 3H-thymidine into ered in periwinkles in Syria (35). The DNA (23). At this time, the factors DNAs of these four spiroplasmas that induce a helical spiroplasma cell show also appreciable degrees of to become nonhelical and vice versa homology (ca 50%). In spite of these are not known. They will probably be close relationships, the four spiroplas- better understood when the mecha- mas can easily be distinguished one nisms by which spiroplasmas achieve from the other by several techniques their helical morphology and motility and they produce specific diseases. have been elucidated. For these reasons, and in spite of In the early 1970s, fulfillment of their relationships with S. citri, the Koch's postulates required that S. corn stunt agent, the honeybee citri, after having been obtained in spiroplasma and the new periwinkle pure culture, be transmitted back to pathogen have eventually received citrus. Euscelis plebejus, a leafhop- species names: S. kunkelii (40), S. per vector of a number of European mell$erum (11) and S. phoeniceum yellows diseases assumed to be (35), respectively. In the spiroplasma caused by mycoplasmas, was origi- classification (38), based on serologi- nally chosen to transmit S. citri to cal and molecular genetic data, S.
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