Skip to main content

Transovarial Transmission in Insect Vectors

  • Chapter
  • First Online:
Book cover Phytoplasmas: Plant Pathogenic Bacteria - II

Abstract

Phytoplasma ability to infect a new generation of insects by transovarial transmission was demonstrated in some insect vector/plant host combinations mainly by molecular evidence coupled with biological assays. Scaphoideus titanus was the first one in which phytoplasma detection in eggs, newly hatched nymphs and adults (reared on phytoplasma-free Vicia faba seedlings) was demonstrated. This kind of transmission was proved also for mulberry dwarf phytoplasmas and for the agent of white leaf disease of sugarcane, transmitted respectively by Hishimonoides sellatiformis and Matsumuratettix hiroglyphicus. Recently Cacopsylla pruni, vector of ‘Candidatus Phytoplasma prunorum’ and Cacopsylla picta one of the main insect vectors of ‘Candidatus Phytoplasma mali’ were also shown to have phytoplasma transovarial transmission, therefore this kind of transmission should be taken into consideration when epidemiological studies are performed on phytoplasma-associated diseases. The fact that the insect is not only the vector, but also a reservoir of the phytoplasma has implications for disease management, increasing the difficulty of disease control. Up to now only a few phytoplasma ribosomal groups such as 16SrI, 16SrX and 16SrXI have been demonstrated to be transferred transovarially in their insect vectors, very likely those capable of better adaptation to both plant and insect environments. Therefore, it can be speculated that only strains of phytoplasmas with specific genetic characteristics have become transovarially transmissible and probably only after a long host–parasite relationship.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alma A, Bosco D, Danielli A, Bertaccini A, Vibio M, Arzone A (1997) Identification of phytoplasmas in eggs, nymphs and adults of Scaphoideus titanus Ball reared on healthy plants. Insect Molecular Biology 6, 115–121.

    Google Scholar 

  • Alma A, Palermo S, Boccardo G, Conti M (2001) Transmission of chrysanthemum yellows, a subgroup 16SrI-B phytoplasma, to grapevine by four leafhopper species. Journal of Plant Pathology 83, 181–187.

    Google Scholar 

  • Alma A, Sacchi L, Favia G, Bandi C, Daffonchio D (2008) Symbiotic microorganisms in leafhopper and planthopper vectors of phytoplasmas in grapevine. Insect Symbiosis 3, 339–359.

    Google Scholar 

  • Arismendi NL, Fiore N, Carrillo R (2015) Absence of transovarial transmission of ‘Candidatus Phytoplasma ulmi’ in the vector Amplicephalus curtulus Linnavuori & DeLong (Hemiptera: Cicadellidae): is it a rule more than an exception? Neotropical Entomology 44, 1–9.

    Google Scholar 

  • Beanland L, Hoy CW, Miller SA, Nault LR (2000) Influence of aster yellows phytoplasma on the fitness of aster leafhopper (Homoptera: Cicadellidae). Annals of the Entomological Society of America 93, 271–276.

    Google Scholar 

  • Bertaccini A, Arzone A, Alma A, Bosco D, Vibio M (1993) Detection of mycoplasmalike organisms in Scaphoideus titanusBall reared on “flavescence dorée” infected grapevine by dot hybridizations using DNA probes. Phytopathologia Mediterranea 32, 20–24.

    Google Scholar 

  • Bertaccini A, Oshima K, Kakizawa S, Duduk B, Namba S (2016) Dissecting the multifaceted mechanisms that drive leafhopper host-phytoplasma specificity. In: Vector-Mediated Transmission of Plant Pathogens. Ed Brown JK. American Phytopathological Society Press, St Paul, United States of America, 21–28 pp.

    Google Scholar 

  • Bosco D, Tedeschi R (2013) Insect vector transmission assays. In: Phytoplasma: Methods and Protocols: Methods in Molecular Biology, vol 938. Eds Dickinson M, Hodgetts J. Humana Press, Springer, New York, United States of America, 73–85 pp.

    Google Scholar 

  • Bressan A, Clair D, Sémétey O, Boudon-Padieu E (2005) Effect of two strains of “flavescence dorée” phytoplasma on the survival and fecundity of the experimental leafhopper vector Euscelidius variegatus Kirschbaum. Journal of Invertebrate Pathology 89, 144–149.

    Google Scholar 

  • Capoccia R, Greub G, Baud D (2013) Ureaplasma urealyticum, Mycoplasma hominis and adverse pregnancy outcomes. Current Opinion in Infectious Diseases 26, 231–240.

    Google Scholar 

  • Cheung WWK (1994) Ultrastructural studies on the female reproductive system of the leafhopper Euscelidium variegatus Kirshbaum (Homoptera: Cicadellidae) I. The germarium. Cytologia 59, 93–101.

    Google Scholar 

  • Chiykowski LN (1967) Some host plants of a Canadian isolate of the clover phyllody virus. Canadian Journal of Plant Science 47, 141–148.

    Google Scholar 

  • Dan H, Ikeda N, Fujikami M, Nakabachi A (2017) Behavior of bacteriome symbionts during transovarial transmission and development of the Asian citrus psyllid. Plos One 12, e0189779.

    Google Scholar 

  • Danielli A, Bertaccini A, Alma A, Bosco D, Vibio M, Arzone A (1996) May evidence of 16SrI group-related phytoplasmas in eggs, nymphs and adults of Scaphoideus titanus Ball suggest their transovarial transmission? IOM Letters 4, 190–191.

    Google Scholar 

  • EFSA PLH Panel (EFSA Panel on Plant Health), Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehnen-Schmutz K, Gilioli G, Gregoire J-C, Jaques Miret JA, Navarro MN, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Winter S, Gardi C, Aukhojee M, Bergeretti F, MacLeod A (2017) Scientific opinion on the pest categorisation of Hishimonus phycitis. EFSA Journal 15, 5030–5056.

    Google Scholar 

  • Galetto L, Bosco D, Balestrini R, Genre A, Fletcher J, Marzachì C (2011) The major antigenic membrane protein of ‘Candidatus Phytoplasma asteris’ selectively interacts with ATP synthase and actin of leafhopper vectors. Plos One 6, 1–12.

    Google Scholar 

  • Gullan PJ, Cranston PS (2010) The insects: an outline of entomology, 5th edition. Wiley, Chichester, United Kingdom.

    Google Scholar 

  • Hanboonsong Y, Choosai C, Panyim S, Damak D (2002) Transovarial transmission of sugarcane white leaf phytoplasma in the insect vector Matsumuratettix hiroglyphicus (Matsumura). Insect Molecular Biology 11, 97–103.

    Google Scholar 

  • Hibino H (1996) Biology and epidemiology of rice viruses. Annual Review of Phytopathology 34, 249–274.

    Google Scholar 

  • Hodin J (2009) She shapes events as they come: plasticity in female reproduction. In: Phenotypic Plasticity of Insects: Mechanism and Consequences. Eds Whitman DW, Ananthakrishnan TN. Science Publishers, Enfield, United States of America, 423–521 pp.

    Google Scholar 

  • Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology 46, 327–359.

    Google Scholar 

  • Huo Y, Liu W, Zhang F, Chen X, Li L, Liu Q, Zhou Y, Wei T, Fang R, Wang X (2014) Transovarial transmission of a plant virus is mediated by vitellogenin of its insect vector. Plos Pathogens 10, e1003949.

    Google Scholar 

  • Ishii Y, Kakizawa S, Hoshi A, Maejima K, Kagiwada S, Yamaji Y, Oshima K, Namba S (2009a) In the non-insect-transmissible line of onion yellows phytoplasma (OY-NIM), the plasmid-encoded transmembrane protein ORF3 lacks the major promoter region. Microbiology 155, 2058–2067.

    Google Scholar 

  • Ishii Y, Oshima K, Kakizawa S, Hoshi A, Maejima K, Kagiwada S, Yamaji Y, Namba S (2009b) Process of reductive evolution during 10 years in plasmids of a non-insect-transmissible phytoplasma. Gene 446, 51–57.

    Google Scholar 

  • Jeger MJ, Madden LV, Van den Bosch F (2009) The effect of transmission route on plant virus epidemic development and disease control. Journal of Theoretical Biology 258, 198–207.

    Google Scholar 

  • Jia D, Mao Q, Chen Y, Liu Y, Chen Q, Wu W, Zhang X, Chen H, Li Y, Wei T (2017) Insect symbiotic bacteria harbour viral pathogens for transovarial transmission. Nature Microbiology 2, 17025.

    Google Scholar 

  • Kakizawa S, Oshima K, Namba S (2006) Diversity and functional importance of phytoplasma membrane proteins. Trends in Microbiology 14, 254–256.

    Google Scholar 

  • Kawakita H, Saiki T, Wei W, Mitsuhashi W, Watanabe K, Sato M (2000) Identification of mulberry dwarf phytoplasmas in the genital organs and eggs of leafhopper Hishimonoides sellatiformis. Phytopathology 90, 909–914.

    Google Scholar 

  • Konnerth A, Krczal G, Boonrod K (2016) Immunodominant membrane proteins of phytoplasmas. Microbiology 162, 1267–1273.

    Google Scholar 

  • Kot M, Büning J, Jankowska W, Drohojowska J, Szklarzewicz T (2016) Development of ovary structures in the last larval and adult stages of psyllids (Insecta, Hemiptera, Sternorrhyncha: Psylloidea). Arthropod Structure & Development 45, 389–398.

    Google Scholar 

  • Lefol C, Lherminier J, Boudon-Padieu E, Larrue J, Louis C, Caudwell A (1994) Propagation of “flavescence dorée” MLO in the leafhopper Euscelidius variegatus Kbm. Journal of Invertebrate Pathology 63, 85–93.

    Google Scholar 

  • Lequime S, Lambrechts L (2014) Vertical transmission of arboviruses in mosquitoes: a historical perspective. Infection, Genetics and Evolution 28, 681–690.

    Google Scholar 

  • Liao Z, Mao Q, Li J, Lu C, Wu W, Chen H, Chen Q, Jia D, Wei T (2017) Virus-induced tubules: a vehicle for spread of virions into ovary oocyte cells of an insect vector. Frontiers in Microbiology 8, 475.

    Google Scholar 

  • Mittelberger C, Obkircher L, Oettl S, Oppedisano T, Perdazzoli F, Panassiti B, Kerschbamer C, Anfora G, Janik K (2017) The insect vector Cacopsylla picta vertically transmits the bacterium ‘Candidatus Phytoplasma mali’ to its progeny. Plant Pathology 66, 1015–1021.

    Google Scholar 

  • Nation JL (2001) Insect physiology and biochemistry. CRC press, Boca Raton, United States of America, 496 pp.

    Google Scholar 

  • Posnette AF, Ellenberger CE (1963) Further studies of green petal and other leafhopper-transmitted viruses infecting strawberry and clover. Annals of Applied Biology 51, 69–83.

    Google Scholar 

  • Queiroz RB, Donkersley P, Silva FN, Al-Mahmmoli IH, Al-Sadi AM, Carvalho CM, Elliot SL (2016) Invasive mutualisms between a plant pathogen and insect vectors in the Middle East and Brazil. Royal Society Open Science 3, 160557.

    Google Scholar 

  • Rashidi M, Galetto L, Bosco D, Bulgarelli A, Vallino M, Veratti F, Marzachì C (2015) Role of the major antigenic membrane protein in phytoplasmas transmission by two insect vector species. BMC Microbiology 15, 193–193.

    Google Scholar 

  • Sacchi L, Genchi M, Clementi E, Bigliardi E, Avanzati AM, Pajoro M, Negri I, Marzorati M, Gonella E, Alma A, Daffonchio D, Bandi C (2008) Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): details of transovarial transmission of Cardinium sp. and yeast-like endosymbionts. Tissue and Cell 40, 231–242.

    Google Scholar 

  • Sinha RC, Chiykowski LN (1967) Initial and subsequent sites of aster yellows virus infection in a leafhopper vector. Virology 33, 702–708.

    Google Scholar 

  • Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA (2011) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proceedings of the National Academy of Sciences of the United States of America 108, E1254–E1263.

    Google Scholar 

  • Suzuki S, Oshima K, Kakizawa S, Arashida R, Jung HY, Yamaji Y, Nishigawa H, Ugaki M, Namba S (2006) Interaction between the membrane protein of a pathogen and insect microfilament complex determines insect-vector specificity. Proceedings of the National Academy of Sciences of the United States of America 103, 4252–4257.

    Google Scholar 

  • Szklarzewicz T, Michalik A (2017) Transovarial transmission of symbionts in insects. In: Results and Problems in Cell Differentiation 63: Oocytes. Maternal Information and Functions. Ed Kloc M. Springer International Publishing AG, Cham, Switzerland, 37–43 pp.

    Google Scholar 

  • Tedeschi R, Ferrato V, Rossi J, Alma A (2006) Possible phytoplasma transovarial transmission in the psyllids Cacopsylla melanoneuraand Cacopsylla pruni. Plant Pathology 55, 18–24.

    Google Scholar 

  • Tsai JH, Perrier JL (1996) Morphology of the digestive and reproductive systems of Dalbulus maidis and Graminella nigrifrons (Homoptera: Cicadellidae). Florida Entomology 79, 563–578.

    Google Scholar 

  • Wei W, Davis RE, Jomantiene R, Zhao Y (2008) Ancient, recurrent phage attacks and recombination shaped dynamic sequence-variable mosaics at the root of phytoplasma genome evolution. Proceedings of the National Academy of Sciences of the United States of America 105, 11827–11832.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rosemarie Tedeschi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Tedeschi, R., Bertaccini, A. (2019). Transovarial Transmission in Insect Vectors. In: Bertaccini, A., Weintraub, P., Rao, G., Mori, N. (eds) Phytoplasmas: Plant Pathogenic Bacteria - II. Springer, Singapore. https://doi.org/10.1007/978-981-13-2832-9_5

Download citation

Publish with us

Policies and ethics