Spiroplasma citri

Last updated

Spiroplasma citri is a bacterium species and the causative agent of Citrus stubborn disease. [1]

Contents

Its genome has been partially sequenced. [2]

The restriction enzyme SciNI, with the cutting site 5' GCGC / 3' CGCG, can be found in S. citri.

Euscelis incisa can be used as a vector of the bacterium to experimentally infect white clover ( Trifolium repens ). [3]

S. citri is a partially sequenced, Gram-positive plant pathogenic mollicute which has a wide host range. [4]

Spiroplasma citri
Scientific classification
Domain:
Bacteria
Phylum:
Mycoplasmatota
Class:
Mollicutes
Order:
Mycoplasmatales
Family:
Mycoplasmataceae
Genus:
Spiroplasma
Species:
S. citri
Binomial name
Spiroplasma citri

Taxonomy and Phylogeny

S. citri is a bacteria that belongs to the kingdom Bacteria, phylum Tenericutes, class Mollicutes, order Entomoplasmatales, family Spiroplasmataceae, and genus Spiroplasma [4] . Members of the Mollicutes class, such as Spiroplasma, are characterized by their reduced genomes and lack of a conventional cell wall, which is a result of their adaptation to parasitic or symbiotic lifestyles. [5] Although Spiroplasma, Mycoplasma , and Phytoplasma are all under the Mollicutes class, the Spiroplasma genus demonstrates a closer genetic relationship to Mycoplasma, an animal genus causing disease, than to Phytoplasma, a plant-associated genus [6] , as only Spiroplasma and Mycoplasma can import sugars through the phosphotransferase system and make ATP via ATP synthase, and Spiroplasma genomes are 1 Mbp larger than Phytoplasma genomes. [7] Most mollicutes are obligate pathogens or symbionts forming complex relationships with their hosts. [8] Notably, Spiroplasma and Phytoplasma exhibit complex life cycles associated with both insect and plant hosts. [6] Spiroplasma transfers between plants and insects through feeding, reflecting its dependency on both host types for survival and spread. [9] This taxonomic affiliation places S. citri within the Citri-Chrysopicola-Mirum clade; relevant neighboring species within this genus include S. kunkelii, S. phoeniceum, S. eriocheiris, S. melliferum, and S. penaei, which infect a variety of hosts including specific species of corn, periwinkles, shrimps, crabs, and honeybees. [6]

Discovery and Isolation

Around 1915, “Washington” navel trees near Redlands, California, were the first to show symptoms of what is now known as Citrus Stubborn Disease. [10] The disease was then reported outside of California for the first time in the Mediterranean in 1928 [11] , suggesting its wider geographical spread and impact on citrus production by that time. However, S. citri, the bacterium responsible for Citrus stubborn disease, was not cultured and identified until 1973, initially discovered in California. [9] This identification was made by J. M. Bové, P. Saglio, M. Lhospital, D. Lafléche, G. Dupont, J. G. Tully, and E. A. Freundt. This team of scientists aimed to find the root cause of citrus stubborn disease, responsible for stunting the growth of citrus plants. The research team focused on young citrus leaves from plants because they were more likely to transmit the disease. [12] To culture S. citri, the team used specialized nutrient-rich media that included horse serum or cholesterol, essential for growth, which mimicked the intracellular environment of the plant phloem, facilitating the growth of this bacterium. The cultures were maintained under anaerobic conditions to replicate the low-oxygen environment inside host issues. [12] To study S. citri, they grew this bacterium in culture and successfully isolated it as a pure culture. From there, the scientists learned the unique biochemical properties of S. citri and what characteristics distinguished it as its own species. [12]

Morphology

S. citri belongs to the Spiroplasma genus within the mollicutes class, which is composed of Gram-positive bacteria that lack a cell wall. [13] S. citri typically has a helical structure due to the arrangement of fibril and MreB filaments along its cytoskeleton. [14] In its helical form, S. citri moves in a corkscrew motion, which plays a significant role in cell division and elongation. [13] However, its alternate forms—spherical or ovoid shapes and branches, non-helical filaments—use intracellular fibril filaments for motility, compensating for the absence of flagella. These filaments create kinks in the cell body, allowing S. citri to move. [14] The sizes of these forms vary greatly: spherical shapes measure 100 to 240 nanometers wide, while helical and branched nonhelical filaments are about 120 nanometers wide, and 2-4 micrometers long, with the potential to reach 15 micrometers in later growth stages. [13] When cultured on agar, S. citricolonies are around 0.2 millimeters in width and display either a fried-egg-like or granular appearance. [13]

Metabolism and physiology

The metabolic pathways of S. citri allow it to survive and proliferate within citrus plants. The tricarboxylic acid cycle is missing from S. citri which means that this bacterium predominantly relies on glycolysis for ATP production. [15] S. citrihas a reduced genome and lacks various metabolic pathways which explains its heavy dependence on its hosts for nutrients, including amino acids, sugars, nucleotides, and vitamins. [16] It lacks a cell wall and is unable to make fatty acids. However, it can modify host-derived lipids for its membrane structure. [17] Like other Spiroplasma species, S. citri is an auxotroph for most of the necessary amino acids, meaning that it obtains them from the host. [18] Spiroplasmas in general are more metabolically flexible which allow them to easily adapt to different environments. [6] In the case of S. citri, this is typically inside an insect or plant phloem. S. citri has virulence factors involved in host tissue degradation and evasion of host immune responses. [19]

Genomics

S. citri's genomics, pieced together through shotgun and chromosome-specific libraries sequencing, reveal key features of its 1820 kbp chromosome. [7]

Sequencing

Although only 92% of the genome could be sequenced, scientists were able to uncover phage-related sequences, 69 transposase copies, and an almost complete terpenoid biosynthetic pathway. [7] Functional complementation and gene inactivation studies demonstrated that S. citri fructose consumption induces plant disease symptoms, and the ABC-type transporter solute binding protein is implicated in insect transmission. [7] The genome includes seven plasmids (10-14 copies/cell) containing proteins for DNA transfer. [7] However, gene decay, observed through shortened coding sequences and incomplete housekeeping genes, as well as repeated sequences, that prevent full chromosome sequencing, add some complexity. Despite these challenges, the S. citri's stable genome demonstrates its overall adaptability.

Ecology

The role of S. citri in its environment is related to how it interacts with host plants, insect vectors, and abiotic factors. This bacterium is mainly transmitted by leafhoppers, which spread it from infected to healthy citrus plants through feeding habits. [20] Young citrus plants are more susceptible to infection because they are more attractive to leafhoppers, whereas older plants become less appealing to these insects. [21] S. citri exploits the nutrients of host plants to survive and reproduce. It is primarily found in the plant phloem, a tissue that is particularly nutrient-rich because it is responsible for transportation of sugars. [20] S. citri thrives and spreads in hot, dry weather, making it commonly found in the United States, the Middle East, North Africa, Central America, New Zealand, and part of Western Europe, particularly France, Italy, and Spain. Notably, in California, major citrus plants like oranges, grapefruits, and tangelos suffer notable yield losses due to S. citri infection, impacting 5-10% of trees. [16]

Environmental Impact

S. citri causes citrus stubborn disease, a disease that reduces the yield and quality of our citrus fruits, which are excellent sources of vitamin C. [20] Though S. citri predominantly affects citrus plants, it also impacts other essential crops, including tomatoes, lettuce, and carrots [20] , which directly impacts the profitability of the agricultural industry and disrupts our food supply. It is important we further study this bacteria in order to learn how to effectively combat it, so that we can develop better management strategies to help minimize financial losses in the produce industry, and to reduce its impact on citrus production as well as on native plant species.

Related Research Articles

<i>Mycoplasma</i> Genus of bacteria

Mycoplasma is a genus of bacteria that, like the other members of the class Mollicutes, lack a cell wall around their cell membranes. Peptidoglycan (murein) is absent. This characteristic makes them naturally resistant to antibiotics that target cell wall synthesis. They can be parasitic or saprotrophic. Several species are pathogenic in humans, including M. pneumoniae, which is an important cause of "walking" pneumonia and other respiratory disorders, and M. genitalium, which is believed to be involved in pelvic inflammatory diseases. Mycoplasma species are among the smallest organisms yet discovered, can survive without oxygen, and come in various shapes. For example, M. genitalium is flask-shaped, while M. pneumoniae is more elongated, many Mycoplasma species are coccoid. Hundreds of Mycoplasma species infect animals.

<span class="mw-page-title-main">Psyllid</span> Family of true bugs

Psyllidae, the jumping plant lice or psyllids, are a family of small plant-feeding insects that tend to be very host-specific, i.e. each plant-louse species only feeds on one plant species (monophagous) or feeds on a few closely related plants (oligophagous). Together with aphids, phylloxerans, scale insects and whiteflies, they form the group called Sternorrhyncha, which is considered to be the most "primitive" group within the true bugs (Hemiptera). They have traditionally been considered a single family, Psyllidae, but recent classifications divide the group into a total of seven families; the present restricted definition still includes more than 70 genera in the Psyllidae. Psyllid fossils have been found from the Early Permian before the flowering plants evolved. The explosive diversification of the flowering plants in the Cretaceous was paralleled by a massive diversification of associated insects, and many of the morphological and metabolic characters that the flowering plants exhibit may have evolved as defenses against herbivorous insects.

<i>Phytoplasma</i> Genus of bacteria

Phytoplasmas are obligate intracellular parasites of plant phloem tissue and of the insect vectors that are involved in their plant-to-plant transmission. Phytoplasmas were discovered in 1967 by Japanese scientists who termed them mycoplasma-like organisms. Since their discovery, phytoplasmas have resisted all attempts at in vitro culture in any cell-free medium; routine cultivation in an artificial medium thus remains a major challenge. Phytoplasmas are characterized by the lack of a cell wall, a pleiomorphic or filamentous shape, a diameter normally less than 1 μm, and a very small genome.

Mollicutes is a class of bacteria distinguished by the absence of a cell wall. The word "Mollicutes" is derived from the Latin mollis, and cutis. Individuals are very small, typically only 0.2–0.3 μm in size and have a very small genome size. They vary in form, although most have sterols that make the cell membrane somewhat more rigid. Many are able to move about through gliding, but members of the genus Spiroplasma are helical and move by twisting. The best-known genus in the Mollicutes is Mycoplasma. Colonies show the typical "fried-egg" appearance.

<span class="mw-page-title-main">Citrus greening disease</span> Bacterial disease of citrus, bug-borne

Citrus greening disease or yellow dragon disease is a disease of citrus caused by a vector-transmitted pathogen. The causative agents are motile bacteria, Liberibacter spp. The disease is transmitted by the Asian citrus psyllid, Diaphorina citri, and the African citrus psyllid, Trioza erytreae, also known as the two-spotted citrus psyllid. It has no known cure. It has also been shown to be graft-transmissible.

<span class="mw-page-title-main">Acholeplasmataceae</span> Family of bacteria

Acholeplasmataceae is a family of bacteria. It is the only family in the order Acholeplasmatales, placed in the class Mollicutes. The family comprises the genera Acholeplasma and Phytoplasma. Phytoplasma has the candidatus status, because members still could not be cultured.

<i>Spiroplasma</i> Genus of bacteria

Spiroplasma is a genus of Mollicutes, a group of small bacteria without cell walls. Spiroplasma shares the simple metabolism, parasitic lifestyle, fried-egg colony morphology and small genome of other Mollicutes, but has a distinctive helical morphology, unlike Mycoplasma. It has a spiral shape and moves in a corkscrew motion. Many Spiroplasma are found either in the gut or haemolymph of insects where they can act to manipulate host reproduction, or defend the host as endosymbionts. Spiroplasma are also disease-causing agents in the phloem of plants. Spiroplasmas are fastidious organisms, which require a rich culture medium. Typically they grow well at 30 °C, but not at 37 °C. A few species, notably Spiroplasma mirum, grow well at 37 °C, and cause cataracts and neurological damage in suckling mice. The best studied species of spiroplasmas are Spiroplasma poulsonii, a reproductive manipulator and defensive insect symbiont, Spiroplasma citri, the causative agent of citrus stubborn disease, and Spiroplasma kunkelii, the causative agent of corn stunt disease.

<i>Xylella fastidiosa</i> Bacteria harming plants, including crops

Xylella fastidiosa is an aerobic, Gram-negative bacterium of the genus Xylella. It is a plant pathogen, that grows in the water transport tissues of plants and is transmitted exclusively by xylem sap-feeding insects such as sharpshooters and spittlebugs. Many plant diseases are due to infections of X. fastidiosa, including bacterial leaf scorch, oleander leaf scorch, coffee leaf scorch (CLS), alfalfa dwarf, phony peach disease, and the economically important Pierce's disease of grapes (PD), olive quick decline syndrome (OQDS), and citrus variegated chlorosis (CVC). While the largest outbreaks of X. fastidiosa–related diseases have occurred in the Americas and Europe, this pathogen has also been found in Taiwan, Israel, and a few other countries worldwide.

<span class="mw-page-title-main">Beet leafhopper</span> Species of insect

The beet leafhopper, also sometimes known as Neoaliturus tenellus, is a species of leafhopper which belongs to the family Cicadellidae in the order Hemiptera.

<span class="mw-page-title-main">Sugarcane grassy shoot disease</span> Phytoplasma (bacterial) disease

Sugarcane grassy shoot disease (SCGS), is associated with 'Candidatus Phytoplasma sacchari' which are small, pleomorphic, pathogenic mycoplasma that contribute to yield losses from 5% up to 20% in sugarcane. These losses are higher in the ratoon crop. A higher incidence of SCGS has been recorded in some parts of Southeast Asia and India, resulting in 100% loss in cane yield and sugar production.

<i>Diaphorina citri</i> Species of true bug

Diaphorina citri, the Asian citrus psyllid, is a sap-sucking, hemipteran bug in the family Psyllidae. It is one of two confirmed vectors of citrus greening disease. It has a wide distribution in southern Asia and has spread to other citrus growing regions.

<i>Liberibacter</i> Species of bacterium

Liberibacter is a genus of Gram-negative bacteria in the Rhizobiaceae family. Detection of the liberibacteria is based on PCR amplification of their 16S rRNA gene with specific primers. Members of the genus are plant pathogens mostly transmitted by psyllids. The genus was originally spelled Liberobacter.

<i>Planococcus citri</i> Species of true bug

Planococcus citri, commonly known as the citrus mealybug, is a species of mealybugs native to Asia. It has been introduced to the rest of the world, including Europe, the Americas, and Oceania, as an agricultural pest. It is associated with citrus, but it attacks a wide range of crop plants, ornamental plants, and wild flora.

The Citrus stubborn disease is a plant disease affecting species in the genus Citrus. Spiroplasma citri, a Mollicute bacterium species, is the causative agent of the disease. It is present in the phloem of the affected plant. Originally discovered transmitted by several leafhoppers including Circulifer tenellus and Scaphytopius nitridus in citrus-growing regions of California, it is now spread by the same hoppers in Arizona and Circulifer haematoceps in the Mediterranean region.

<i>Spiroplasma phage 1-R8A2B</i> Species of virus

Spiroplasma phage 1-R8A2B is a filamentous bacteriophage in the genus Vespertiliovirus of the family Plectroviridae, part of the group of single-stranded DNA viruses. The virus has many synonyms, such as SpV1-R8A2 B, Spiroplasma phage 1, and Spiroplasma virus 1, SpV1. SpV1-R8A2 B infects Spiroplasma citri. Its host itself is a prokaryotic pathogen for citrus plants, causing Citrus stubborn disease.

Mycoplasma orale is a small bacterium found in the class Mollicutes. It belongs to the genus Mycoplasma, a well-known group of bacterial parasites that inhabit humans. It also is known to be an opportunistic pathogen in immunocompromised humans. As with other Mycoplasma species, M. orale is not readily treated with many antibiotics due to its lack of a peptidoglycan cell wall. Therefore, this species is relevant to the medical field as physicians face the task of treating patients infected with this microbe. It is characterized by a small physical size, a small genome size, and a limited metabolism. It is also known to frequently contaminate laboratory experiments. This bacteria is very similar physiologically and morphologically to its sister species within the genus Mycoplasma; however, its recent discovery leaves many questions still unanswered about this microbe.

<span class="mw-page-title-main">Corn stunt disease</span> Bacterial plant disease

Corn stunt disease is a bacterial disease of corn and other grasses. Symptoms include stunted growth and leaves turning red. It is caused by the bacterium Spiroplasma kunkelii.

<i>Euscelis incisa</i> Species of true bug

Euscelis incisa is a leafhopper species in the family Cicadellidae. It is found in Europe, North Africa, and Asia. It is formerly known as Euscelis plebejus, among other names.

Candidatus Phytoplasma pruni is a species of phytoplasma in the class Mollicutes, a class of bacteria distinguished by the absence of a cell wall. The specific epithet pruni means "living on Prunus", emphasizing the fact that the phytoplasma is a parasite of various Prunus species, otherwise known as stone fruits. The phytoplasma is commonly called the X-disease phytoplasma.

<i>Spiroplasma kunkelii</i> Species of bacteria

Spiroplasma kunkelii is a species of Mollicutes, which are small bacteria that all share a common cell wall-less feature. They are characterized by helical and spherical morphology, they actually have the ability to be spherical or helical depending on the circumstances. The cells movement is bound by a membrane. The cell size ranges from 0.15 to 0.20 micrometers.

References

  1. ↑ Spiroplasma citri gen. and sp. n.: A Mycoplasma-Like Organism Associated with “Stubborn” Disease of Citrus. P. Saglio, M. Lhospital, D. Laflèche, G. Dupont, J. M. Bové, J. G. Tully and E. A. Freundt, IJSEM, July 1973, volume 23, number 3, pages 191-204, doi : 10.1099/00207713-23-3-191
  2. ↑ Partial Chromosome Sequence of Spiroplasma citri Reveals Extensive Viral Invasion and Important Gene Decay. Patricia Carle, Colette Saillard, Nathalie Carrère, Sébastien Carrère, Sybille Duret, Sandrine Eveillard, Patrice Gaurivaud, Géraldine Gourgues, Jérome Gouzy, Pascal Salar, Eric Verdin, Marc Breton, Alain Blanchard, Frédéric Laigret, Joseph-Marie Bové, Joel Renaudin and Xavier Foissac, Appl. Environ. Microbiol., June 2010, volume 76, number 11, pages 3420-3426, doi : 10.1128/AEM.02954-09
  3. ↑ Spiroplasmas are the causal agents of citrus little-leaf disease. P. G. Markham, R. Townsend, M. Bar-Joseph, M. J. Daniels, A. Plaskitt and B. M. Meddins, Annals of Applied Biology, September 1974, Volume 78, Issue 1, pages 49–57, doi : 10.1111/j.1744-7348.1974.tb01484.x
  4. 1 2 "Taxonomy browser (Spiroplasma citri)". www.ncbi.nlm.nih.gov. Retrieved 2024-05-06.
  5. ↑ "Mollicutes: Molecular Biology and Pathogenesis". www.caister.com. Retrieved 2024-05-07.
  6. 1 2 3 4 Lo, Wen-Sui; Chen, Ling-Ling; Chung, Wan-Chia; Gasparich, Gail E.; Kuo, Chih-Horng (2013-01-16). "Comparative genome analysis of Spiroplasma melliferumIPMB4A, a honeybee-associated bacterium". BMC Genomics. 14 (1): 22. doi: 10.1186/1471-2164-14-22 . ISSN   1471-2164. PMC   3563533 . PMID   23324436.
  7. 1 2 3 4 5 Carle, Patricia; Saillard, Colette; Carrère, Nathalie; Carrère, Sébastien; Duret, Sybille; Eveillard, Sandrine; Gaurivaud, Patrice; Gourgues, Géraldine; Gouzy, Jérome; Salar, Pascal; Verdin, Eric; Breton, Marc; Blanchard, Alain; Laigret, Frédéric; Bové, Joseph-Marie (June 2010). "Partial Chromosome Sequence of Spiroplasma citri Reveals Extensive Viral Invasion and Important Gene Decay". Applied and Environmental Microbiology. 76 (11): 3420–3426. doi:10.1128/AEM.02954-09. ISSN   0099-2240. PMC   2876439 . PMID   20363791.
  8. ↑ Taylor, Mark; Mediannikov, Oleg; Raoult, Didier; Greub, Gilbert (February 2012). "Endosymbiotic bacteria associated with nematodes, ticks and amoebae". FEMS Immunology & Medical Microbiology. 64 (1): 21–31. doi:10.1111/j.1574-695x.2011.00916.x. ISSN   0928-8244.
  9. 1 2 Cacciola, Santa Olga; Bertaccini, Assunta; Pane, Antonella; Furneri, Pio Maria (2017-04-12), "Spiroplasma spp.: A Plant, Arthropod, Animal and Human Pathogen", Citrus Pathology, IntechOpen, ISBN   978-953-51-3072-7 , retrieved 2024-05-07
  10. ↑ Gumpf, D. J. (1988), Maramorosch, Karl; Raychaudhuri, S. P. (eds.), "Stubborn Diseases of Citrus Caused by Spiroplasma Citri", Mycoplasma Diseases of Crops: Basic and Applied Aspects, New York, NY: Springer, pp. 327–342, doi:10.1007/978-1-4612-3808-9_17, ISBN   978-1-4612-3808-9 , retrieved 2024-05-07
  11. ↑ Bove, J. M.; Fos, A.; Lallemand, J. (June 1987). "Epidemiology of Spiroplasma citri in the Old World". Israel Journal of Medical Sciences. 23 (6): 663–666. ISSN   0021-2180. PMID   3312105.
  12. 1 2 3 SAGLIO, P.; LHOSPITAL, M.; LAFLÈCHE, D.; DUPONT, G.; BOVÈ, J. M.; TULLY, J. G.; FREUNDT, E. A. (1973). "Spiroplasma citri gen. and sp. n.: A Mycoplasma-Like Organism Associated with "Stubborn" Disease of Citrus". International Journal of Systematic and Evolutionary Microbiology. 23 (3): 191–204. doi:10.1099/00207713-23-3-191. ISSN   1466-5034.
  13. 1 2 3 4 Cisak, Ewa; Wójcik-Fatla, Angelina; Zając, Violetta; Sawczyn, Anna; Sroka, Jacek; Dutkiewicz, Jacek (2015-12-13). "Spiroplasma – an emerging arthropod-borne pathogen?". Annals of Agricultural and Environmental Medicine. 22 (4): 589–593. doi:10.5604/12321966.1185758. ISSN   1232-1966. PMID   26706960.
  14. 1 2 Harne, Shrikant; Gayathri, Pananghat; Béven, Laure (2020). "Exploring Spiroplasma Biology: Opportunities and Challenges". Frontiers in Microbiology. 11. doi: 10.3389/fmicb.2020.589279 . ISSN   1664-302X. PMC   7609405 . PMID   33193251.
  15. ↑ Pollack, J. D.; McElwain, M. C.; DeSantis, D.; Manolukas, J. T.; Tully, J. G.; Chang, C.-J.; Whitcomb, R. F.; Hackett, K. J.; Williams, M. V. (1989). "Metabolism of Members of the Spiroplasmataceae". International Journal of Systematic and Evolutionary Microbiology. 39 (4): 406–412. doi:10.1099/00207713-39-4-406. ISSN   1466-5034.
  16. 1 2 McNeil, Christopher J.; Araujo, Karla; Godfrey, Kristine; Slupsky, Carolyn M. (February 2023). "Metabolite Signature and Differential Expression of Genes in Washington Navel Oranges ( Citrus sinensis ) Infected by Spiroplasma citri". Phytopathology. 113 (2): 299–308. doi:10.1094/PHYTO-05-22-0177-R. ISSN   0031-949X. PMID   35984373.
  17. ↑ Freeman, B A; Sissenstein, R; McManus, T T; Woodward, J E; Lee, I M; Mudd, J B (March 1976). "Lipid composition and lipid metabolism of Spiroplasma citri". Journal of Bacteriology. 125 (3): 946–954. doi:10.1128/jb.125.3.946-954.1976. ISSN   0021-9193. PMC   236170 . PMID   1254560.
  18. ↑ Vera-Ponce León, Arturo; Dominguez-Mirazo, Marian; Bustamante-Brito, Rafael; Higareda-Alvear, Víctor; Rosenblueth, Mónica; Martínez-Romero, Esperanza (2021-04-06). "Functional genomics of a Spiroplasma associated with the carmine cochineals Dactylopius coccus and Dactylopius opuntiae". BMC Genomics. 22 (1): 240. doi: 10.1186/s12864-021-07540-2 . ISSN   1471-2164. PMC   8025503 . PMID   33823812.
  19. ↑ Bolaños, Luis M.; Servín-Garcidueñas, Luis E.; Martínez-Romero, Esperanza (2015-02-01). "Arthropod–Spiroplasma relationship in the genomic era". academic.oup.com. Retrieved 2024-05-07.
  20. 1 2 3 4 "Spiroplasma citri - an overview | ScienceDirect Topics". www.sciencedirect.com. Retrieved 2024-05-07.
  21. ↑ "Spiroplasma citri (stubborn disease of citrus)". PlantwisePlus Knowledge Bank. Species Pages. 2022-01-07. doi:10.1079/pwkb.species.50977. ISSN   2958-4329.


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