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Department of Biochemistry profile

Associate Professor Russell Poulter

PositionAssociate Professor
DepartmentDepartment of Biochemistry
QualificationsBSc(Lond) PhD(Leic)
Research summaryMolecular and classical genetics of yeasts and plants

Research

Eukaryote mobile genetic elements

A long-term interest of this laboratory has been in the genetics of imperfect fungi (i.e. fungi without a known sexual cycle). More recently, our focus shifted to the retrotransposons present in fungi and, by extension, to retroelements in general. The five major groups of LTR retrotransposons are known as the Ty3/gypsy, Ty1/copia, DIRS1, BEL, and vertebrate retrovirus groups. The elements within each group can generally be distinguished from elements of other groups by comparisons of the sequences of their shared enzymatic domains. We have isolated a Ty1/copia retrotransposon, TCa2, from the fungal pathogen Candida albicans. TCa2 has a number of interesting features including an in-phase suppressible stop codon between ORF1 and ORF2. We have also analysed a Ty3/Gypsy element from C. albicans, Tca3. Tca3 was first identified as a widespread form that lacks a large part of its coding region; however, comparative analyses between C. albicans and C. dubliniensis allowed us to identify the closely related full-length Tcd3 element. Subsequently, we uncovered the rare full-length Tca3 elements. The potential uses of retroelements in biotechnology and their application to the analysis of fungal pathogenicity are at present being investigated. We have also contributed to the analysis of mobile elements such as DNA transposons (including tyrosine recombinase-encoding elements and Helitrons) and retroelements in other fungi, especially the basidiomycete pathogen, Cryptococcus neoformans.

During an analysis of the mobile genetic elements of Cryptococcus we detected an intein in the Cryptococcus genome. Inteins are encoded transposable elements that occur naturally as in-frame, translated insertions in the coding sequences of organisms from all three biological kingdoms. The coding sequences (encoding the exteins) of certain host genes are interrupted by inserted sequences (encoding inteins). The inteins (internal protein) disrupt the functioning of the protein and must be removed after translation to allow the host protein to function. We are engaged in in vitro and in vivo studies of intein function in collaboration with Dr Sigurd Wilbanks of this department.

We have extended our interest to the retrotransposons of vertebrates and have characterised a full-length multi-copy (x1000) LTR retrotransposon from the Fugu fish, Takifugu rubripes. This work was in collaboration with the HGMP/MRC Cambridge. The retrotransposon, sushi, is the first full length LTR retrotransposon from any vertebrate. Sushi is a member of the ty3/Gypsy group. It has many features that suggest it could represent the ancestral group from which vertebrate retroviruses were derived. Sushi, however, has closest homology to a group of fungal retrotransposons. This presents the interesting possibility that retroviruses are derived from retrotransposons that were horizontally transmitted to vertebrates from fungi. Dr Poulter and Dr John Cutfield (also from the Dept. of Biochemistry) were awarded a Marsden grant, funded by the N.Z. Royal Society, to investigate this possibility.

During this project we discovered vertebrate representatives from other retrotransposon groups. We described an element (Gmr1) from the Atlantic cod (Gadus morhua) in which the pol domains appear in the same order as in Ty1/copia elements, PRO-INT-RT-RNH, yet sequence comparisons clearly show that the element is a member of the Ty3/gypsy group. Perhaps the most distinctive LTR retrotransposons are the members of the DIRS1 group. These elements have quite different structures from all other LTR retrotransposons, encode a different set of proteins, and probably have distinct replication mechanisms. They contain genes for a putative Gag protein, RT and RNH, and a tyrosine recombinase. We discovered DIRS1-like elements in the genome of Tetraodon (a freshwater pufferfish). Another family of retrotransposons, the Ngaro1-like elements, also contain genes encoding putative tyrosine recombinases. Ngaro1-like elements differ from members of the DIRS1 group in that they consistently form a separate clade on phylogenetic trees based on alignments of RT, RNH and recombinase sequences, and they have distinct structures. The new elements thus appear to represent a second lineage of tyrosine recombinase-encoding retrotransposons. Ngaro1-like retrotransposons are found in a wide variety of eukaryotes, including plants, fungi, and animals, suggesting that they are an ancient class of element.

Dr Poulter's laboratory has a wide range of other interests, ranging from transgenic yeast technology as applied to the wine industry to the application of genetic analyses to horticulture. Dr Poulter has recently described a gene conferring resistance to powdery mildew in Lathyrus, the Sweet pea.

Awards

  • Thomas Handley
    2013, QMB Enzyme Engineering and Evolution Poster Prize

Publications

Poulter, R. T. M., & Butler, M. I. (2015). Tyrosine recombinase retrotransposons and transposons. In N. L. Craig, M. Chandler, M. Gellert, A. M. Lambowitz, P. A. Rice & S. B. Sandmeyer (Eds.), Mobile DNA III. (pp. 1271-1291). Washington, DC: ASM Press.

Poulter, R. T. M., & Butler, M. I. (2015). Tyrosine recombinase retrotransposons and transposons. Microbiology Spectrum, 3(2), MDNA3-0036-2014. doi: 10.1128/microbiolspec.MDNA3-0036-2014

Ciarroni, S., Gallipoli, L., Taratufolo, M. C., Butler, M. I., Poulter, R. T., Pourcel, C., … Mazzaglia, A. (2015). Development of a Multiple Loci Variable number of tandem repeats Analysis (MLVA) to unravel the intra-pathovar structure of Pseudomonas syringae pv. actinidiae populations worldwide. PLoS ONE, 10(8), e0135310. doi: 10.1371/journal.pone.0135310

Butler, M. I., Stockwell, P. A., Black, M. A., Day, R. C., Lamont, I. L., & Poulter, R. T. M. (2013). Pseudomonas syringae pv. actinidiae from recent outbreaks of kiwifruit bacterial canker belong to different clones that originated in China. PLoS ONE, 8(2), e57464. doi: 10.1371/journal.pone.0057464

Bokor, A. A. M., Kohn, L. M., Poulter, R. T. M., & van Kan, J. A. L. (2012). PRP8 inteins in species of the genus Botrytis and other ascomycetes. Fungal Genetics & Biology, 49(3), 250-261. doi: 10.1016/j.fgb.2012.01.001

Chapter in Book - Research

Poulter, R. T. M., & Butler, M. I. (2015). Tyrosine recombinase retrotransposons and transposons. In N. L. Craig, M. Chandler, M. Gellert, A. M. Lambowitz, P. A. Rice & S. B. Sandmeyer (Eds.), Mobile DNA III. (pp. 1271-1291). Washington, DC: ASM Press.

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Journal - Research Article

Poulter, R. T. M., & Butler, M. I. (2015). Tyrosine recombinase retrotransposons and transposons. Microbiology Spectrum, 3(2), MDNA3-0036-2014. doi: 10.1128/microbiolspec.MDNA3-0036-2014

Ciarroni, S., Gallipoli, L., Taratufolo, M. C., Butler, M. I., Poulter, R. T., Pourcel, C., … Mazzaglia, A. (2015). Development of a Multiple Loci Variable number of tandem repeats Analysis (MLVA) to unravel the intra-pathovar structure of Pseudomonas syringae pv. actinidiae populations worldwide. PLoS ONE, 10(8), e0135310. doi: 10.1371/journal.pone.0135310

Butler, M. I., Stockwell, P. A., Black, M. A., Day, R. C., Lamont, I. L., & Poulter, R. T. M. (2013). Pseudomonas syringae pv. actinidiae from recent outbreaks of kiwifruit bacterial canker belong to different clones that originated in China. PLoS ONE, 8(2), e57464. doi: 10.1371/journal.pone.0057464

Bokor, A. A. M., Kohn, L. M., Poulter, R. T. M., & van Kan, J. A. L. (2012). PRP8 inteins in species of the genus Botrytis and other ascomycetes. Fungal Genetics & Biology, 49(3), 250-261. doi: 10.1016/j.fgb.2012.01.001

Bokor, A. A. M., van Kan, J. A. L., & Poulter, R. T. M. (2010). Sexual mating of Botrytis cinerea illustrates prp8 intein heg activity. Fungal Genetics & Biology, 47(4), 392-398. doi: 10.1016/j.fgb.2010.01.003

Dickson, G. C., Poulter, R. T. M., Maas, E. W., Probert, P. K., & Kieser, J. A. (2010). Marine bacterial succession as a potential indicator of postmortem submersion interval. Forensic Science International, 209(1-3), 1-10. doi: 10.1016/j.forsciint.2010.10.016

Dong, C., Poulter, R. T., & Han, J. S. (2009). Line-like retrotransposition in Saccharomyces cerevisiae. Genetics, 181(1), 301-311.

Bishop, P. J., Speare, R., Poulter, R., Butler, M., Speare, B. J., Hyatt, A., … Haigh, A. (2009). Elimination of the amphibian chytrid fungus Batrachochytrium dendrobatidis by Archey's frog Leiopelma archeyi. Diseases of Aquatic Organisms, 84(1), 9-15. doi: 10.3354/dao02028

Ma, L.-J., Ibrahim, A. S., Skory, C., Grabherr, M. G., Burger, G., Butler, M., … Poulter, R., … Wickes, B. L. (2009). Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genetics, 5(7), e1000549. doi: 10.1371/journal.pgen.1000549

Jackson, A. P., Gamble, J. A., Yeomans, T., Moran, G. P., Saunders, D., Harris, D., … Goodwin, T. J., … Poulter, R. T., … Berriman, M. (2009). Comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans. Genome Research, 19(12), 2231-2244. doi: 10.1101/gr.097501.109

Goodwin, T. J. D., Busby, J. N., & Poulter, R. T. M. (2007). A yeast model for target-primed (non-LTR) retrotransposition. BMC Genomics, 8, 263. doi: 10.1186/1471-2164-8-263

Pearl, E. J., Bokor, A. A. M., Butler, M. I., Poulter, R. T. M., & Wilbanks, S. M. (2007). Preceding hydrophobic and β-branched amino acids attenuate splicing by the CnePRP8 intein. Biochimica et Biophysica Acta: General Subjects, 1774, 995-1001. doi: 10.1016/j.bbapap.2007.05.015

Pearl, E. J., Tyndall, J. D. A., Poulter, R. T. M., & Wilbanks, S. M. (2007). Sequence requirements for splicing by the Cne PRP8 intein. FEBS Letters, 581, 3000-3004.

Poulter, R. T. M., Goodwin, T. J. D., & Butler, M. I. (2007). The nuclear-encoded inteins of fungi. Fungal Genetics & Biology, 44(3), 153-179.

Goodwin, T. J. D., Butler, M. I., & Poulter, R. T. M. (2006). Multiple, non-allelic, intein-coding sequences in eukaryotic RNA polymerase genes. BMC Biology, 4, 38. doi: 10.1186/1741-7007-4-38

Butler, M. I., Gray, J., Goodwin, T. J. D., & Poulter, R. T. M. (2006). The distribution and evolutionary history of the PRP8 intein. BMC Evolutionary Biology, 6, 42. doi: 10.1186/1471-2148-6-42

Butler, M. I., & Poulter, R. T. M. (2005). The PRP8 inteins in Cryptococcus are a source of phylogenetic and epidemiological information. Fungal Genetics & Biology, 42, 452-463.

Butler, M. I., Goodwin, T. J. D., & Poulter, R. T. M. (2005). Two new fungal inteins. Yeast, 22, 493-501.

Goodwin, T. J. D., & Poulter, R. T. M. (2004). A new group of tyrosine recombinase-encoding retrotransposons. Molecular Biology & Evolution, 21(4), 746-759.

Goodwin, T. J. D., Poulter, R. T. M., Lorenzen, M. D., & Beeman, R. W. (2004). DIRS retroelements in arthropods: Identification of the recently active TcDirs1 element in the red flour beetle Tribolium castaneum. Molecular Genetics & Genomics, 272, 47-56.

Goodwin, T., Butler, M. I., & Poulter, R. T. M. (2003). Cryptons: A group of tyrosine-recombinase-encoding DNA transposons from pathogenic fungi. Microbiology, 149, 3099-3109.

Poulter, R. T. M., Harvey, L., & Burritt, D. J. (2003). Qualitative resistance to powdery mildew in hybrid sweet peas. Euphytica, 133, 349-358.

Goodwin, T., Dalle Nogare, D. E., Butler, M. I., & Poulter, R. T. M. (2003). Ty3/gypsy-like retrotransposons in Candida albicans and Candida dubliniensis: Tca3 and Tcd3. Yeast, 20, 493-508.

Poulter, R. T. M., Goodwin, T., & Butler, M. I. (2003). Vertebrate helentrons and other novel Helitrons. Gene, 313, 201-212.

Dalle Nogare, D. E., Clark, M. S., Elgar, G., Frame, I. G., & Poulter, R. T. M. (2002). Xena, a full-length basal retroelement from Tetraondontid fish. Molecular Biology & Evolution, 19(3), 247-255.

Goodwin, T., & Poulter, R. T. M. (2002). A group of deuterostome Ty3/gypsy-like retrotransposons with Ty1/copia-like pol-domain orders. Molecular Genetics & Genomics, 264(4), 481-491.

Butler, M., Goodwin, T., & Poulter, R. (2001). An unusual vertebrate LTR retrotransposon from the cod Gadus morhua. Molecular Biology & Evolution, 18(3), 443-447.

Butler, M. I., Goodwin, T. J. D., Simpson, M., Singh, M., & Poulter, R. T. M. (2001). Vertebrate LTR retrotransposons of the Tf1/sushi group. Journal of Molecular Evolution, 52(3), 260-274.

Frame, I. G., Cutfield, J. F., & Poulter, R. T. M. (2001). New BEL-like LTR-retrotransposons in Fugu rubripes, Caenorhabditis elegans and Drosphilia melanogaster. Gene, 263, 219-230.

Goodwin, T. J. D., & Poulter, R. T. M. (2001). The DIRS1 group of retrotransposons. Molecular Biology & Evolution, 18(11), 2067-2082.

Holton, N. J., Goodwin, T. J. D., Butler, M. I., & Poulter, R. T. M. (2001). An active retrotransposon in Candida albicans. Nucleic Acids Research, 29(19), 4014-4024.

Goodwin, T. J. D., & Poulter, R. T. M. (2001). The diversity of retrotransposons in the yeast Cryptococcus neoformans. Yeast, 18(9), 865-880.

Butler, M. I., Goodwin, T. J. D., & Poulter, R. T. M. (2001). A nuclear-encoded intein in the fungal pathogen Cryptococcus neoformans. Yeast, 18(15), 1365-1370.

Goodwin, T. J. D., Ormandy, J. E., & Poulter, R. T. M. (2001). L1-like non-LTR retrotransposons in the yeast Candida albicans. Current Genetics, 39(2), 83-91.

Plant, E. P., Goodwin, T. J. D., & Poulter, R. T. M. (2000). Tca5, a Ty5-like retrotransposon from Candida albicans. Yeast, 16(16), 1509-1518.

Goodwin, T. J. D., & Poulter, R. T. M. (2000). Multiple LTR-retrotransposon families in the asexual yeast Candida albicans. Genome Research, 10(2), 174-191.

Poulter, R. T. M., Butler, M. I., & Ormandy, J. E. E. (1999). A LINE element from the pufferfish (fugu) Fugu rubripes which shows similarity to the CR1 family of non-LTR retrotransposons. Gene, 227(2), 169-179.

Plant, E. P., Becher, D., & Poulter, R. T. (1998). The SPL1 tRNA splicing gene of Candida maltosa and Candida albicans. Yeast, 14, 287-295.

Goodwin, T. J. D., & Poulter, R. T. (1998). The CARE-2 and Rel-2 repetitive elements of Candida albicans contain LTR fragments of a new retrotransposon. Gene, 218(1-2), 85-93.

Poulter, R. T., & Butler, M. I. (1998). A retrotransposon family from the pufferfish (fugu) Fugu rubripes. Gene, 215, 241-249.

Matthews, G. D., Goodwin, T. J. D., Butler, M. I., Berryman, T. A., & Poulter, R. T. (1997). pCal, a highly unusual Ty1/copia Retrotransposon from the pathogenic yeast Candida albicans. Journal of Bacteriology, 179(22), 7118-7128.

Longley, M., & Poulter, R. T. (1997). Characterization of pBP614, a putative rolling-circle plasmid from Bacillus popilliae. Plasmid, 37, 15-21.

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Journal - Research Other

Poulter, R. T. M., & Goodwin, T. J. D. (2005). DIRS-1 and the other tyrosine recombinase retrotransposons. Cytogenetic & Genome Research, 110(1-4), 575-588.

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