Faculty of Biological Sciences

Plant Nematology at Leeds: Publications

Refereed publications

Jain R., Lilley C.J and Urwin P.E. (2015) Reduction of phytate by down-regulation of Arabidopsis thaliana MIPS and IPK1 genes alters susceptibility to beet cyst nematodes. Nematology,

Tripathi L., Babirye A., Roderick H., Tripathi J., Changa C., Urwin P.E., Tushemereirwe W.K. and Atkinson H.J. (2015) Field resistance of transgenic plantain to nematodes has potential for future African food security. Scientific Reports, 5: 8127

Eves-van den Akker S., Lilley C.J., Jones J.T. and Urwin P.E. (2015) Plant-parasitic nematode feeding tubes and plugs: new perspectives on function. Nematology17: 1-9

Thorpe P., Mantelin S., Cock P.J.A, Blok V.C., Coke M.C., Eves-van den Akker S., Guzeeva E., Lilley C.J., Smant G., Reid A.J., Wright K.M., Urwin P.E and Jones J.T. (2014) Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida. BMC Genomics 15: 923

Eves-van den Akker S., Lilley C.J., Jones J.T. and Urwin P.E. (2014) Identification and characterisation of a hyper-variable apoplastic effector gene family of the potato cyst nematodes. PLoS Pathogens10(9): e1004391 DOI:10.1371/journal.ppat.100439

Eves-van den Akker S., Lilley C.J., Danchin E.G.J., Rancurel C., Cock P.J.A., Urwin P.E. and Jones J.T. (2014) The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes. Genome Biology and Evolution 6: 2181-2194

Cotton J.A., Lilley C.J., Jones L.M., Kikuchi T, Reid A.J., Thorpe P., Tsai I.J., Beasley H., Blok V., Cock P.J.A., Eves-van den Akker S., Holroyd N., Hunt M., Mantelin S., Naghra H., Pain A, Palomares-Rius J.E., Zarowiecki M., Berriman M., Jones J.T. and Urwin P.E. (2014) The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biology 15: R43

Hu C., Kearn J., Urwin P.E., Lilley C.J., O' Connor V., Holden-Dye L. and Morgan H. (2014) StyletChip: a microfluidic device for recording host invasion behaviour and feeding of plant parasitic nematodes. Lab Chip 14: 2447-2455

Eves-van den Akker S., Lilley C.J., Ault J.R., Ashcroft A.E., Jones J.T. and Urwin P.E. (2014) The Feeding Tube of Cyst Nematodes: Characterisation of Protein Exclusion. PLoS ONE 9(1): e87289

Atkinson N.J., Lilley C.J. and Urwin P.E. (2013) Identification of genes involved in the response of Arabidopsis to simultaneous siotic and abiotic stresses. Plant Physiology 162: 2028-2041

Jones L.M., Rayson S.J., Flemming A.J. and Urwin P.E. (2013) Adaptive and specialised transcriptional responses to xenobiotic stress in Caenorhabditis elegans are regulated by nuclear hormone receptors. PLoS ONE 8(7): e69956

Tripathi L., Tripathi J., Roderick H. and Atkinson H.J. (2013) Engineering nematode resistant plantains for sub-Saharan Africa. Acta Horticulturae 974: 99-107

Lilley C.J., Davies L.J. and Urwin P.E. (2012) RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology 139: 630-640

Roderick H., Mbiru E., Coyne D., Tripathi L. and Atkinson H.J. (2012) Quantitative digital imaging of banana growth suppression by plant parasitic nematodes PLoS ONE 7(12): e53355

Davies L.J. and Urwin P.E. (2012) The cell walls of syncytia formed by Heterodera schachtii in Arabidopsis thaliana are abundant in methyl-esterified pectin. Plant Signalling and Behaviour 7 (11): 1404-1406

Davies L.J., Lilley C.J., Knox P.J. and Urwin P.E. (2012) Syncytia formed by adult female Heterodera schachtii in Arabidopsis thaliana roots have a distinct cell wall molecular architecture. New Phytologist 196: 238–246

Atkinson N.J. and Urwin P.E. (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. Journal of Experimental Botany 63 (10): 3523-3543

Roderick H., Tripathi L., Babirye A., Wang D., Tripathi J., Urwin P.E. and Atkinson H.J. (2012) Generation of transgenic plantain (Musa spp.) with resistance to plant pathogenic nematodes. Molecular Plant Pathology, 13: 842–851

Atkinson H.J., Lilley C.J. and Urwin P.E. (2012) Strategies for transgenic nematode control in developed and developing world crops. Current Opinion in Biotechnology 23 (2): 251-256

Green J., Wang D., Lilley C.J., Urwin P.E. and Atkinson H.J. (2012) Transgenic Potatoes for Potato Cyst Nematode Control Can Replace Pesticide Use without Impact on Soil Quality. PLoS ONE 7 (2): e30973

Lilley C.J., Davies L.J. and Urwin P.E. (2012) RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology 139 (5): 630-640

Wang D., Jones L.M., Urwin P.E. and Atkinson H.J. (2011) A Synthetic Peptide Shows Retro- and Anterograde Neuronal Transport before Disrupting the Chemosensation of Plant-Pathogenic Nematodes. PLoS ONE 6 (3): e17475

Lilley C.J., Wang D., Atkinson H.J. and Urwin P.E. (2011) Effective delivery of a nematode-repellent peptide using a root-cap-specific promoter. Plant Biotechnology Journal 9 (2): 151–161

Atkinson N.J., Dew P.D., Orfila C. and Urwin P.E. (2011) Influence of combined biotic and abiotic stress on nutritional quality parameters in tomato (Solanum lycopersicum). Journal of Agricultural and Food Chemistry 59 (17): 9673-9682

Lord J.S., Lazzeri L., Atkinson H.J. and Urwin P.E. (2011) Biofumigation for Control of Pale Potato Cyst Nematodes: Activity of Brassica Leaf Extracts and Green Manures on Globodera pallida in Vitro and in Soil. Journal of Agricultural and Food Chemistry 59 (14): 7882–7890

Siddique S., Endres S., Atkins J.M., Szakasits D., Wieczorek K., Hofmann J., Blaukopf C., Urwin P.E., Tenhaken R., Grundler F.M.W., Kreil D.P. and Bohlmann H. (2009) Myo-inositol oxygenase genes are involved in the development of syncytia induced by Heterodera schachtii in Arabidopsis roots. New Phytologist 184 (2): 457–472

Costa J.C., Lilley C.J., Atkinson H.J. and Urwin P.E.. (2009) Functional characterisation of a cyst nematode acetylcholinesterase gene using Caenorhabditis elegans as a heterologous system. International Journal for Parasitology 39 (7): 849-858

Wang M.-L., Uruu G., Xiong L., He X., Nagai C., Cheah K.T., Hu J.S., Nan G.-L., Sipes B.S., Atkinson H.J., Moore P.H., Rohrbach K.G. and Paull R.E. (2009) Production of transgenic pineapple (Ananas cosmos (L.) Merr.) plants via adventitious bud regeneration. In Vitro Cellular & Developmental Biology - Plant 45 (2): 112-121  

Bakhetia M., Urwin P.E. and Atkinson H.J. (2008) Characterisation by RNAi of pioneer genes expressed in the dorsal pharyngeal gland cell of Heterodera glycines and the effects of combinatorial RNAi. International Journal for Parasitology 38 (13): 1589-1597

Fuller V.L., Lilley C.J. and Urwin P.E. (2008), Nematode resistance. New Phytologist 180: 27–44

Cabos R.Y., Sipes B.S., Schmitt D.P. and Atkinson H.J. (2007) Plant proteinase inhibitors as a natural and introduced defense mechanism for root-knot nematode in Coffea arabica. Journal of Nematology 39 (1): 100-100

Bakhetia M., Urwin P.E. and Atkinson H.J. (2007) QPCR analaysis and RNAi define pharyngeal gland cell- expressed genes for Heterodera glycines required for inital interactions with the host. Molecular Plant-Microbe Interactions 20 (3): 306-312

Shingles J., Lilley C.J., Atkinson H.J. and Urwin P.E., (2007) Meloidogyne incognita: Molecular and biochemical characterisation of cathepsin L cysteine proteinase and the effect of parasitism following RNAi. Experimental parasitology 115 (2): 114-120

Cabos R., Sipes B.S., Schmitt D.P. and Atkinson H.J. (2006) Engineering Coffea arabica for resistance to Meloidogyne konaensis using cysteine and serine proteinase inhibitors. Journal of Nematology 38 (2): 265-265

Lilley C.J., Goodchild S.A. and Atkinson H.J. (2005) Cloning and characterisation of Heterodera glycines aminopeptidase cDNA. International Journal for Parisitology 35(14): 1577-1585

Green J., Fearnehough M.T. and Atkinson H.J. (2005) Development of biosafe genetically modified Solanum tuberosum (potato) cultivars for growth within a centre of origin of the crop. Molecular Breeding 16: 285–293

Lilley C. J., Atkinson H.J. and Urwin P.E. (2005) Molecular aspects of cyst nematodes. Molecular Plant Pathology 6(6): 577-588

Bakhetia M., Charlton W., Atkinson H.J. and Mcpherson M.J. (2005) RNA interference of dual oxidase in the plant nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 18 (10): 1099-1106

Liu B., Hibbard J.K., Urwin P.E. and Atkinson H.J. (2005) The production of synthetic chemodisruptive peptides in planta disrupts the establishment of cyst nematodes. Plant Biotechnology Journal 3: 487-496

Bakhetia M.,Charlton W.L., Urwin P.E., McPherson M.J. and Atkinson H.J. (2005) RNA interference and plant parasitic nematodes. TRENDS in Plant Sciences 10(9): 362-367

Celis C., Scurrah S., Cowgill S., Chumbiauca S., Green J., Franco J., Main G., Kiezebrink D., Visser R.G.F. and Atkinson H.J.(2004) Environmental biosafety and transgenic potato in a centre of diversity for this crop. Nature 432: 222-225

Bee

Atkinson H.J., Grimwood S., Johnston K. and Green J. (2004) Prototype demonstration of transgenic resistance to the nematode Radopholus similis conferred on banana by a cystatin. Transgenic Research 13 (2): 135-142

Lilley C.J., Urwin P.E., Johnston K.A. and Atkinson H.J. (2004) Preferential expression of a plant cystatin at nematode feeding sites confers resistance to Meloidogyne incognita and Globodera pallida. Plant Biotechnology Journal 2(1): 3-12

Cowgill S.E., Danks C. and Atkinson H.J. (2004) Mutitrophic interactions involving genetically modified potatoes, nontarget aphids, natural enemies and hyperoarasitoids. Molecular Ecology 13 (3): 639-647

Atkinson H.J., Johnston K.A. and Robbins M. (2004) Prima facie evidence that a phytocystatin for transgenic plant resistance to nematodes is not a toxic risk in the human diet. Journal of Nutrition 134 (2):431-434

Urwin P.E., Green J. and Atkinson H.J. (2003) Expression of a plant cystatin confers partial resistance to Globodera, full resistance is achieved by pyramiding a cystatin with natural resistance. Molecular Breeding 12 (3):263-269

Atkinson H.J., Urwin P.E. and McPherson M.J. (2003) Engineering plants for nematode resistance. Annual Review of Phytopathology 41: 615-639

Cowgill S.E. and Atkinson H.J. (2003) A sequential approach to risk assessment of transgenic plants expressing proteases inhibitors: effects on non target herbivorous insects. Transgenic Research 12 (4): 439-449

Winter M.D., McPherson M.J. and Atkinson H.J. (2002) Neuronal uptake of pesticides disrupts chemosensory cells of nematodes. Parasitology 125: 561-565

Cowgill S.E., Bardgett R.D., Kiezebrink D.T. and Atkinson H.J. (2002) The effect of transgenic nematode resistance on non-target organisms in the potato rhizosphere. Journal of Applied Ecology 39 (6): 915-923

Urwin P.E., Zubko E.I. and Atkinson H.J. (2002) The biotechnological application and limitation of IRES to deliver multiple defense genes to plant pathogens. Physiological and Molecular Plant Pathology 61 (2): 103-108

Urwin P.E., Lilley C.J. and Atkinson H.J. (2002) Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant Microbe In. 15 (8): 747-752

Green J., Vain P., Fearnehough M.T., Worland B., Snape J.W. and Atkinson H.J. (2002) Analysis of the expression patterns of the Arabidopsis thaliana tubulin-1 and Zea mays ubiquitin-1 promoters in rice plants in association with nematode infection. Physiological and Molecular Plant Pathology 60: 197-205

Cowgill S.E., Wright C., and Atkinson H.J. (2002) Transgenic potatoes with enhanced levels of nematode resistance do not have altered susceptibility to non-target aphids. Molecular Ecology. 11: 821-827

Atkinson H.J., Holz R.A., Riga E., Main G., Oros R. and Franco J. (2001) An algorithm for optimizing rotational control of Globodera rostochiensis on potato crops in Bolivia. Journal of Nematology 33 (2-3): 121-125

Urwin P.E., Troth K.M., Zubko E.I. and Atkinson H.J. (2001). Effective transgenic resistance to Globodera pallida in potato field trials. Molecular Breeding 8 (1): 95-101

Atkinson H.J., Green J., Cowgill S. and Levesley A. (2001) The case for genetically modified crops with a poverty focus. Trends in Biotechnology 19 (3): 91-96

Urwin P.E., Yi l., Martin H., Atkinson H.J., and Gilmartin P.M. (2000) Functional characterization of the EMCV IRES in plants. The Plant Journal 24 (5): 583–589

Urwin P.E., Levesley A., McPherson M.J. and Atkinson H.J. (2000) Transgenic resistance to the nematode Rotylenchulus reniformis conferred by A. thaliana plants expressing proteinase inhibitors. Molecular Breeding 6 (3): 257-264

Walker A.J., Urwin P.E., Atkinson H.J., Brain P., Glen D.M. and Shewry P.R. (1999) Transgenic Arabidopsis leaf tissue expressing a modified oryzacystatin shows resistance to the field slug Deroceras reticulatum (Muller). Transgenic Research 8 (2): 95-103

Lilley C.J., Devlin P., Urwin P.E. and Atkinson H.J. (1999) Parasitic nematodes, proteinases and transgenic plants. Parasitology Today 15 (10): 414-417

Lilley C.J., Urwin P.E. and Atkinson H.J. (1999) Characterization of plant nematode genes: identifying targets for a transgenic defence. Parasitology 118 Suppl:S63-72. Rev

Urwin P.E. and Lilley C.J. (1999) Resistance to plant parasitic nematodes conferred by GM-crops. Pesticide Outlook 10:145-149

Urwin P.E., McPherson M.J. and Atkinson H.J. (1998) Enhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructs. Planta 204 (4): 472-479

Roman R., Urwin P.E., Atkinson H.J. and Gilmartin P.M. (1998) Hgm1 a novel male-specific gene from Heterodera glycines identified by differential mRNA display. Molecular and Biochemical Parasitology 95: 45-52

Møller S.G., Urwin P.E., Atkinson H.J. and McPherson M.J. (1998) Nematode-induced expression of atao1 a gene encoding an extracellular diamine oxidase associated with developing vascular tissue. Physiological and Molecular Plant Pathology 53: 73-79

Lilley C.J., Urwin P.E., Atkinson H.J. and McPherson M.J. (1997) Characterization of cDNAs encoding serine proteinases from the soybean cyst nematode Heterodera glycines. Molecular and Biochemical Parasitology 89 (2): 195-207

Urwin P.E., Lilley C.J., McPherson M.J. and Atkinson H.J. (1997) Resistance to both cyst and root-knot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant Journal 12 (2): 455-461

Urwin P.E., Lilley C.J., McPherson M.J. and Atkinson H.J. (1997) Characterization of two cDNAs encoding cysteine proteinases from the soybean cyst nematode Heterodera glycines. Parasitology 114 (Pt 6): 605-613

Urwin P.E., Moller S.G., Lilley C.J., McPherson M.J. and Atkinson H.J. (1997) Continual green-fluorescent protein monitoring of cauliflower mosaic virus 35S promoter activity in nematode-induced feeding cells in Arabidopsis thaliana. Mol Plant Microbe Interact. 10 (3): 394-400

Lilley CJ, Urwin PE, McPherson MJ, Atkinson HJ. (1996) Characterization of intestinally active proteinases of cyst-nematodes. Parasitology. 113 (Pt 4): 415-24

Urwin PE, Atkinson HJ, McPherson MJ. (1995) Involvement of the NH2-terminal region of oryzacystatin-I in cysteine proteinase inhibition. Protein Eng. 8 (12): 1303-1307

Urwin PE, Atkinson HJ, Waller DA, McPherson MJ (1995) Engineered oryzacystatin-I expressed in transgenic hairy roots confers resistance to Globodera pallida. Plant J. 1995 Jul;8(1):121-31

Koritsas VM, Atkinson HJ (1995) An assay for detecting nanogram levels of proteolytic enzymes. Anal Biochem. 227 (1): 22-26.

Reviews and book chapters

Cowgill S.E. Coates DA Atkinson HJ. (1999) In Gene Fow: Relevance to Agriculture. Keele YK: British Crop Protection Council. vol 72 p203-208.

Urwin, P.E., Green, J. Atkinson, H.J. (2000) Resistance to Globodera spp. in transgenic Solanum tuberosum cv. Désirée that express proteinase inhibitors (Ed. Haydock, P.P.J.) In, Aspects of Applied Biology No. 59: Potato cyst nematode management. pp. 27-32.

Lilley, C.J., Urwin, P.E. and Atkinson, H.J. (1999) Characterisation of plant nematode genes: identifying targets for a transgenic defence. Parasitology. 118: S63-S72.

Urwin, P.E., Møller, S.G., Blumsom, J. K., and Atkinson, H.J. (1999) Continual monitoring of promoter activity in plants. Methods in Enzymology. 302: 316-328.

Atkinson, H.J., Lilley, C.J., McPherson, M.J. and Urwin, P.E. (1998) Transgenic crops for protection from nematodes. In, Pests and Diseases, British Crop Protection Council. pp.747-754.*

Urwin, P.E., Lilley, C.J., Atkinson, H.J. (1998) Nematode control by genetically modified crops (Ed. Dale, M.F.B. et al) In, Aspects of Applied Biology No. 52: Production and Protection of sugar beet and potatoes. pp. 255-262.*

Atkinson, H.J., Lilley, C.J., Urwin, P.E. and McPherson, M.J. (1998) Engineering resistance to plant nematodes (Ed. Perry, R.) In, The Physiology and Biochemistry of Free-living and Plant-parasitic Nematodes. CABI St Albans, U.K. pp. 381-413.*

McPherson, M.J., Urwin, P.E., Lilley, C.J. and Atkinson, H.J. (1997) Engineering plant nematode resistance by an anti-feedant approach. (Eds. Fenoll, C., Ohl, S. and Grundler, F.) In, Molecular Basis for Plant-Nematode Interactions. Kluwer Academic Publishers, Netherlands. pp237-249.

Atkinson, H.J., Lilley, C.J., Urwin, P.E. and McPherson, M.J. (1997) Engineered resistance to potato cyst-nematode. In, Potato cyst nematodes: Biology, distribution and control. (Eds. Marks, J. and Brodie, W.) CABI St Albans, U.K. pp. 209-236.*

Patents

Atkinson, H.J., Urwin, P.E. and McPherson, M.J.
Translationally linked proteins (International patent application number PCT/EP98/07792)*

Atkinson, H.JMcPherson MJ Urwin PE Novartis
Proteinase inhibitor fusion proteins (published 10-Jun-99, Pub no:.WO9928484)

Atkinson, H.J, Winter MD McPherson MJ
Control of crop pests and animal parasites through direct neuronal uptake (published 1-Sep-00, pub. no: 46070GB

Atkinson, H.J, Koritsas VM Lee DL MacGregor AN
Control of parasites. (date granted: 26-Jan-99). Patent no:US 5,863,775

Atkinson, H.J, Lilley CJ
Root specific promoters.(date granted: 21-Oct-98). Patent no: EP1996000940016

Atkinson, H.J, McPherson MJ Urwin PE
Modified proteinase inhibitors. 10-Sep-97. Patent no: EP1995000937951

Atkinson, H.J, Hepher A
Nematode control with proteinase inhibitors. 27-Feb-96. Patent no: US 5,494,813

Atkinson, H.J, Gurr SJ McPherson MJ Bowles DJ
Plant parasitic nematode control. 31-Dec-96. Patent no: US 5,589,622

Atkinson, H.J, Gurr SJ McPherson MJ Bowles DJ
Plant parasitic nematode control. 20-Oct-98. Patent no: US 5,824,876