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Genome size of Pachypsylla venusta (Hemiptera: Psyllidae) and the ploidy of its bacteriocyte, the symbiotic host cell that harbors intracellular mutualistic bacteria with the smallest cellular genome

Published online by Cambridge University Press:  23 March 2009

A. Nakabachi*
Affiliation:
Advanced Science Institute, RIKEN, 2-1 Hirosawa, Wako, Saitama351-0198, Japan
S. Koshikawa
Affiliation:
Graduate School of Environmental Science, Hokkaido University, Sapporo060-0810, Japan
T. Miura
Affiliation:
Graduate School of Environmental Science, Hokkaido University, Sapporo060-0810, Japan
S. Miyagishima
Affiliation:
Advanced Science Institute, RIKEN, 2-1 Hirosawa, Wako, Saitama351-0198, Japan
*
*Author for correspondence Fax: +81 48 462 9329 E-mail: bachi@riken.jp

Abstract

Psyllids harbor the primary symbiont, Carsonella ruddii (γ-Proteobacteria), within the cytoplasm of specialized cells called bacteriocytes. Carsonella has the smallest known cellular genome (160 kb), lacking numerous genes that appear to be essential for bacterial life. This raises the question regarding the genetic mechanisms of the host which supports the survival of Carsonella. Our preceding analyses have indicated that some of the genes that are encoded in the psyllid genome and which are highly expressed in the bacteriocyte are of bacterial origin. This implies that psyllids acquired genes from bacteria by lateral gene transfer (LGT) and are using these genes to maintain the primary symbiont, Carsonella. To reveal the complete picture of LGT from symbiotic bacteria to the genome of psyllids, whole genome analysis of psyllids is essential. In order to assess the feasibility of whole genome analysis of the host psyllid, the genome size of the hackberry petiole gall psyllid, Pachypsylla venusta, was estimated. Feulgen image analysis densitometry and flow cytometry demonstrated that the haploid genome size of P. venusta is 0.74 pg (724 Mb), verifying the feasibility of whole genome analysis. Feulgen image analysis densitometry further revealed that bacteriocytes of P. venusta are invariably 16-ploid. This higher ploidy may be essential to facilitate the symbiotic relationship with bacteria, as it appears to be a feature common to insect bacteriocytes. These results provide a foundation for genomics-based research into host-symbiont interactions.

Type
Research Paper
Copyright
Copyright © 2009 Cambridge University Press

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References

Baudisch, K. (1956) Zytologische Beobachtungen an den Mycetocyten von Periplaneta americana L. Naturwissenschaften 43, 358.CrossRefGoogle Scholar
Bennett, M.D., Leitch, I.J., Price, H.J. & Johnston, J.S. (2003) Comparisons with Caenorhabditis (approximately 100 Mb) and Drosophila (approximately 175 Mb) using flow cytometry show genome size in Arabidopsis to be approximately 157 Mb and thus approximately 25% larger than the Arabidopsis genome initiative estimate of approximately 125 Mb. Annals of Botany 91, 547557.CrossRefGoogle Scholar
Brown, J.K., Lambert, G.M., Ghanim, M., Czosnek, H. & Galbraith, D.W. (2005) Nuclear DNA content of the whitefly Bemisia tabaci (Aleyrodidae: Hemiptera) estimated by flow cytometry. Bulletin of Entomological Research 95, 309312.CrossRefGoogle ScholarPubMed
Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. 909 pp. New York, Interscience.Google Scholar
Clark, M.A., Baumann, L., Thao, M.L., Moran, N.A. & Baumann, P. (2001) Degenerative minimalism in the genome of a psyllid endosymbiont. Journal of Bacteriology 183, 18531861.CrossRefGoogle ScholarPubMed
Dolezel, J., Bartos, J., Voglmayr, H. & Greilhuber, J. (2003) Nuclear DNA content and genome size of trout and human. Cytometry A 51, 127128.Google ScholarPubMed
Douglas, A.E. (1989) Mycetocyte symbiosis in insects. Biological Reviews 64, 409434.CrossRefGoogle ScholarPubMed
Douglas, A.E. (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology 43, 1737.CrossRefGoogle ScholarPubMed
Dyall, S.D., Brown, M.T. & Johnson, P.J. (2004) Ancient invasions: from endosymbionts to organelles. Science 304, 253257.CrossRefGoogle ScholarPubMed
Edgar, B.A. & Orr-Weaver, T.L. (2001) Endoreplication cell cycles: more for less. Cell 105, 297306.CrossRefGoogle ScholarPubMed
Fukatsu, T. & Nikoh, N. (1998) Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Applied and Environmental Microbiology 64, 35993606.CrossRefGoogle ScholarPubMed
Galbraith, D.W., Harkins, K.R., Maddox, J.M., Ayres, N.M., Sharma, D.P. & Firoozabady, E. (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220, 10491051.CrossRefGoogle ScholarPubMed
Gomez-Palacio, A., Jaramillo-Ocampo, N., Triana-Chavez, O., Saldana, A., Calzada, J., Perez, R. & Panzera, F. (2008) Chromosome variability in the Chagas disease vector Rhodnius pallescens (Hemiptera, Reduviidae, Rhodniini). Memórias do Instituto Oswaldo Cruz 103, 160164.CrossRefGoogle ScholarPubMed
Gregory, T.R. (2005) The Evolution of the Genome. 768 pp. London, Elsevier/Academic Press.Google Scholar
Hardie, D.C., Gregory, T.R. & Hebert, P.D. (2002) From pixels to picograms: a beginners' guide to genome quantification by Feulgen image analysis densitometry. Journal of Histochemistry and Cytochemistry 50, 735749.CrossRefGoogle ScholarPubMed
Hillier, L.W., Marth, G.T., Quinlan, A.R., Dooling, D., Fewell, G., Barnett, D., Fox, P., Glasscock, J.I., Hickenbotham, M., Huang, W., Magrini, V.J., Richt, R.J., Sander, S.N., Stewart, D.A., Stromberg, M., Tsung, E.F., Wylie, T., Schedl, T., Wilson, R.K. & Mardis, E.R. (2008) Whole-genome sequencing and variant discovery in C. elegans. Nature Methods 5, 183188.CrossRefGoogle ScholarPubMed
Johnston, J.S., Bennett, M.D., Rayburn, A.L., Galbraith, D.W. & Price, H.J. (1999) Reference standards for determination of DNA content of plant nuclei. American Journal of Botany 86, 609.CrossRefGoogle ScholarPubMed
Koch, A. (1960) Intracellular symbiosis in insects. Annual Review of Entomology 14, 121140.Google ScholarPubMed
Koshikawa, S., Miyazaki, S., Cornette, R., Matsumoto, T. & Miura, T. (2008) Genome size of termites (Insecta, Dictyoptera, Isoptera) and wood roaches (Insecta, Dictyoptera, Cryptocercidae). Naturwissenschaften 95, 859867.CrossRefGoogle ScholarPubMed
Körner, H.K. (1969) Die embryonale Entwicklung der symbiontenführenden Organe von Euscelis plebejus Fall. (Homoptera-Cicadina). Oecologia 2, 319346.CrossRefGoogle ScholarPubMed
Mardis, E.R. (2008) Next-generation DNA sequencing methods. Annual Review of Genomics and Human Genetics 9, 387402.CrossRefGoogle ScholarPubMed
Maryanska-Nadachowska, A. (2002) A review of karyotype variation in jumping plant-lice (Psylloidea, Sternorrhyncha, Hemiptera) and checklist of chromosome numbers. Folia Biologica (Krakow) 50, 135152.Google ScholarPubMed
Megy, K., Hammond, M., Lawson, D., Bruggner, R.V., Birney, E. & Collins, F.H.Genomic resources for invertebrate vectors of human pathogens, and the role of VectorBase. Infection, Genetics and Evolution, in press (doi:10.1016/j.meegid.2007.12.007).Google Scholar
Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42, 165190.CrossRefGoogle ScholarPubMed
Munson, M.A., Baumann, P. & Kinsey, M.G. (1991) Buchnera gen. nov. and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. International Journal of Systematic and Evolutionary Microbiology 41, 566568.Google Scholar
Nakabachi, A. (2008) Mutualism revealed by symbiont genomics and bacteriocyte transcriptomics. pp. 163204in Bourtzis, K. & Miller, T.A. (Eds) Insect Symbiosis, vol 3. New York, CRC Press.CrossRefGoogle Scholar
Nakabachi, A., Shigenobu, S., Sakazume, N., Shiraki, T., Hayashizaki, Y., Carninci, P., Ishikawa, H., Kudo, T. & Fukatsu, T. (2005) Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. The Proceedings of the National Academy of Sciences of the United States of America 102, 54775482.Google ScholarPubMed
Nakabachi, A., Yamashita, A., Toh, H., Ishikawa, H., Dunbar, H.E., Moran, N.A. & Hattori, M. (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314, 267.CrossRefGoogle ScholarPubMed
Panzera, F., Ferrandis, I., Ramsey, J., Salazar-Schettino, P.M., Cabrera, M., Monroy, C., Bargues, M.D., Mas-Coma, S., O'Connor, J.E., Angulo, V.M., Jaramillo, N. & Perez, R. (2007) Genome size determination in chagas disease transmitting bugs (hemiptera-triatominae) by flow cytometry. American Journal of Tropical Medicine and Hygiene 76, 516521.CrossRefGoogle ScholarPubMed
Poole, A.M. & Penny, D. (2007) Evaluating hypotheses for the origin of eukaryotes. Bioessays 29, 7484.CrossRefGoogle ScholarPubMed
Rasch, E.M., Barr, H.J. & Rasch, R.W. (1971) The DNA content of sperm of Drosophila melanogaster. Chromosoma 33, 118.CrossRefGoogle ScholarPubMed
Ravid, K., Lu, J., Zimmet, J.M. & Jones, M.R. (2002) Roads to polyploidy: the megakaryocyte example. Journal of Cellular Physiology 190, 720.CrossRefGoogle ScholarPubMed
Riemann, J.G. (1966) Chromosome numbers in the hackberry psyllids Pachypsylla and Tetragonocephala (Homoptera: Psyllidae). Annals of the Entomological Society of America 59, 10881093.CrossRefGoogle Scholar
Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y. & Ishikawa, H. (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 8186.CrossRefGoogle ScholarPubMed
Spaulding, A.W. & von Dohlen, C.D. (1998) Phylogenetic characterization and molecular evolution of bacterial endosymbionts in psyllids (Hemiptera: Sternorrhyncha). Molecular Biology and Evolution 15, 15061513.CrossRefGoogle ScholarPubMed
Spaulding, A.W. & von Dohlen, C.D. (2001) Psyllid endosymbionts exhibit patterns of co-speciation with hosts and destabilizing substitutions in ribosomal RNA. Insect Molecular Biology 10, 5767.CrossRefGoogle ScholarPubMed
Stokstad, E. (2006) Agriculture. New disease endangers Florida's already-suffering citrus trees. Science 312, 523524.CrossRefGoogle ScholarPubMed
Subandiyah, S., Nikoh, N., Tsuyumu, S., Somowiyarjo, S. & Fukatsu, T. (2000) Complex endosymbiotic microbiota of the citrus psyllid Diaphorina citri (Homoptera: Psylloidea). Zoological Science 17, 983989.CrossRefGoogle Scholar
Tagu, D., Klingler, J.P., Moya, A. & Simon, J.C. (2008) Early progress in aphid genomics and consequences for plant-aphid interactions studies. Molecular Plant-Microbe Interactions 21, 701708.CrossRefGoogle ScholarPubMed
Thao, M.L., Moran, N.A., Abbot, P., Brennan, E.B., Burckhardt, D.H. & Baumann, P. (2000) Cospeciation of psyllids and their primary prokaryotic endosymbionts. Applied and Environmental Microbiology 66, 28982905.CrossRefGoogle ScholarPubMed
Wheeler, D.A., Srinivasan, M., Egholm, M., Shen, Y., Chen, L., McGuire, A., He, W., Chen, Y.J., Makhijani, V., Roth, G.T., Gomes, X., Tartaro, K., Niazi, F., Turcotte, C.L., Irzyk, G.P., Lupski, J.R., Chinault, C., Song, X.Z., Liu, Y., Yuan, Y., Nazareth, L., Qin, X., Muzny, D.M., Margulies, M., Weinstock, G.M., Gibbs, R.A. & Rothberg, J.M. (2008) The complete genome of an individual by massively parallel DNA sequencing. Nature 452, 872876.CrossRefGoogle ScholarPubMed