Abstract
Plant-parasitic nematodes are important and cosmopolitan pathogens of crops. Here, we describe the generation and analysis of 1928 expressed sequence tags (ESTs) of a splice-leader 1 (SL1) library from mixed life stages of the root-lesion nematode Pratylenchus penetrans. The ESTs were grouped into 420 clusters and classified by function using the Gene Ontology (GO) hierarchy and the Kyoto KEGG database. Approximately 80% of all translated clusters show homology to Caenorhabditis elegans proteins, and 37% of the C. elegans gene homologs had confirmed phenotypes as assessed by RNA interference tests. Use of an SL1-PCR approach, while ensuring the cloning of the 5′ ends of mRNAs, has demonstrated bias toward short transcripts. Putative nematode-specific and Pratylenchus -specific genes were identified, and their implications for nematode control strategies are discussed.
Similar content being viewed by others
References
Acedo JR, Rohde RA (1971) Histochemical root pathology of Brassica oleracea capitata L. infected by Pratylenchus penetrans (Cobb) Filipjev and Schuurmans Stekhoven (Nematoda: Tylenchidae). J Nematol 3:62–68
Al-Banna L, Williamson V, Gardner SL (1997) Phylogenetic analysis of nematodes of the genus Pratylenchus using 26S rDNA. Mol Phylogenet Evol 7:94–102
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Apweiler R, et al (2001) The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 29:37–40
Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995
Bargmann CI (1998) Neurobiology of the Caenorhabditis elegans genome. Science 282:2028–2033
Bird AF, Bird J (1991) The structure of nematodes (2nd edn) Academic Press, San Diego
Blaxter ML (2003) Nematoda: genes, genomes and the evolution of parasitism. Adv Parasitol 54:101–195
Blaxter M, Bird DM (1997) Parasitic nematodes. In: Riddle DL, Blumenthal T, Meyer B, Priess J (eds) C. elegans II. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
Blaxter M, Liu L (1996) Nematode spliced leaders -- ubiquity, evolution and utility. Int J Parasitol 26:1025–1033
Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75
Blumenthal T, Steward K (1997) RNA processing and gene structure. In: Riddle DL, Blumenstiel B, Meyer BJ, Priess JR (eds) C. elegans. Vol. II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 117–145
Bono H, Ogata H, Goto S, Kanehisa M (1998) Reconstruction of amino acid biosynthesis pathways from the complete genome sequence. Genome Res 8:203–210
Boucher G, Lambshead PJD (1994) Ecological biodiversity of marine nematodes in samples from temperate, tropical, and deep-sea regions. Conserv Biol 9:1594–1604
Conrad R, Thomas J, Spieth J, Blumenthal T (1991) Insertion of part of an intron into the 5′ untranslated region of a Caenorhabditis elegans gene converts it into a trans-spliced gene. Mol Cell Biol 11:1921–1926
Cunningham ML, Titus RG, Turco SJ, Beverley SM (2001) Regulation of differentiation to the infective stage of the protozoan parasite Leishmania major by tetrahydrobiopterin. Science 292:285–287
Dautova M, Overmars HA, Schots A, Gommers FJ, Bakker J, Smant G (2001a) A novel cell wall degrading enzyme in the plant parasitic nematode Meloidogyne incognita. Phytopathology 91:S21
Dautova M, Rosso MN, Abad P, Gommers FJ, Bakker J, Smant G (2001b) Single pass cDNA sequencing—a powerful tool to analyse gene expression in preparasitic juveniles of the Southern root-knot nematode Meloidogyne incognita. Nematology 3:129–139
De Meutter J, Tytgat T, van der Schueren E, Smant G, Schots A, Coomans A, van Montagu M, Gheysen G (1998) Cloning of two endoglucanase genes from Heterodera schachtii. Med Fac Landbouww Univ Gent 63/3a:619–623
Dickerson OJ, Darling HM, Griffin GD (1964) Pathogenicity and population trends of Pratylenchus penetrans on potato and corn. Phytopathology 54:317–322
Doyle EA, Lambert KN (2002) Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica. Mol Plant-Microbe Interacts 15:549–556
Elliott AP, Bird GW (1985) Pathogenicity of Pratylenchus penetrans to navy bean ( Phaseolus vulgaris L.). J Nematol 17:81–85
Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408:325–330
Goellner M, Smant G, de Boer JM, Baum TJ, Davis EL (2000) Isolation of beta-1,4-endoglucanase genes from Globodera tabacum and their expression during parasitism. J Nematol 32:154–165
Gonczy P, et al (2000) Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408:331–336
Gross SS, Jones CL, Hattori Y, Raman CS (2000) Tetrahydrobiopterin: an essential cofactor of nitric oxide synthase with an elusive role. In: Ignarro LJ (ed) Nitric oxide: biology and pathobiology. Academic Press, San Diego, pp 167–185
Hoekstra R, Visser A, Otsen M, Tibben J, Lenstra JA, Roos MH (2000) EST sequencing of the parasitic nematode Haemonchus contortus suggests a shift in gene expression during transition to the parasitic stages. Mol Biochem Parasitol 110:53–68
Hung CL, Rohde RA (1973) Phenol accumulation related to resistance in tomato to infection by root-knot and lesion nematodes. J Nematol 5:253–258
IUBMB (1992) Enzyme Nomenclature: Recommendations of the Nomenclature Committee of the International Union of Biochemistry and Molecular Biology. Academic Press, San Diego
Jaubert S, Laffaire JB, Abad P, Rosso MN (2002) A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett 522:109–112
Javed AA, Ogata K, Sanadi DR (1991) Human mitochondrial ATP synthase: cloning cDNA for the nuclear-encoded precursor of coupling factor 6. Gene 97:307–310
Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231–237
Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30
Katzenmeier G, Schmid C, Kellermann J, Lottspeich F, Bacher A (1991) Biosynthesis of tetrahydrofolate. Sequence of GTP cyclohydrolase I from Escherichia coli. Biol Chem Hoppe Seyler 372:991–997
Kaufman S (1993) New tetrahydrobiopterin-dependent systems. Annu Rev Nutr 13:261–286
Koenning SR, Overstreet C, Noling JW, Donald PA, Becker JO, Fortnum BA (1999) Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994. J Nematol 31:587–618
Krause M, Hirsh D (1987) A trans -spliced leader sequence on actin mRNA in C. elegans. Cell 49:753–761
Krusberg LR (1960) Hydrolytic and respiratory enzymes of species of Ditylenchus and Pratylenchus. Phytopathology 50:9–22
Kurppa S, Vrain TC (1985) Penetration and feeding behavior of Pratylenchus penetrans in strawberry roots. Revue de Nematologie 8:273–276
Maeda I, Kohara Y, Yamamoto M, Sugimoto A (2001) Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 11:171–176
McCarter J, Abad P, Jones JT, Bird D (2000) Rapid gene discovery in plant parasitic nematodes via Expressed Sequence Tags. Nematology 2:719–731
McCarter J, Dautova Mitreva M, Martin J, Dante M, Wylie T, Rao U, Pape D, Bowers Y, Theising B, Murphy CV, Kloek AP, Chiapelli BJ, Clifton SW, Bird MD, Waterston R (2003a) Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. Genome Biol 4:R26
McCarter JP, Mitreva M, Clifton SW, Bird DM, Waterston R (2003b) Nematode gene sequences: update for December 2003. J Nematol 35:465–469
Mitreva M, McCarter JP, Martin J, Dante M, Wylie T, Chiapelli B, Pape D, Clifton SW, Nutman TB, Waterston RH (2004) Comparative genomics of gene expression in the parasitic and free-living nematodes Strongyloides stercoralis and Caenorhabditis elegans. Genome Res 14:209–220
Mountain WB, Patrick ZA (1959) The peach replant problem in Ontario. Can J Bot 37:459–470
Nathoo AN, Moeller RA, Westlund BA, Hart AC (2001) Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. Proc Natl Acad Sci USA 98:14000–14005
Nickle WR (1991) Manual of agricultural nematology. Marcel Dekker, New York
Nilsen TW (1993) Trans -splicing of nematode premessenger RNA. Annu Rev Microbiol 47:413–440
Parkinson J, Mitreva M, Hall N, Blaxter M, McCarter JP (2003) 400000 nematode ESTs on the Net. Trends Parasitol 4922:132–136
Pitcher RS, Patrick ZA, Mountain WB (1960) Studies on the host-parasite relations of Pratylenchus penetrans (Cobb) to apple seedlings. Nematologica 5:309–314
Popeijus H, Blok VC, Cardle L, Bakker E, Phillips MS, Helder J, Smant G, Jones JT (2000a) Analysis of genes expressed in second stage juveniles of the potato cyst nematodes Globodera rostochiensis and G. pallida using the expressed sequence tag approach. Nematology 2:567–574
Popeijus H, Overmars HA, Jones JT, Blok VC, Goverse A, Helder J, Schots A, Bakker J, Smant G (2000b) Degradation of plant cell walls by a nematode. Nature 406:36–37
Rosso MN, Favery B, Piotte C, Arthaud L, De Boer JM, Hussey RS, Bakker J, Baum TJ, Abad P (1999) Isolation of a cDNA encoding a beta-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Mol Plant Microbe Interact 12:585–591
Scholl EH, Thorne JL, McCarter JP, Bird DM (2003) Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol 4:R39
Schramek N, Bracher A, Fischer M, Auerbach G, Nar H, Huber R, Bacher A (2002) Reaction mechanism of GTP cyclohydrolase I: single turnover experiments using a kinetically competent reaction intermediate. J Mol Biol 316:829–837
Skalka AM, Goff SP (1993) Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Smant G, Stokkermans JP, Yan Y, de Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci USA 95:4906–4911.
Snedecor WG, Cochran GW (1967) Statistical methods. The Iowa State University Press, Ames, Iowa
Taguchi H, Armarego WL (1998) Glyceryl-ether monooxygenase [EC 1.14.16.5]. A microsomal enzyme of ether lipid metabolism. Med Res Rev 18:43–89
The Gene Ontology Consortium (2000) Gene ontology: a tool for the unification of biology. Nat Genet 25:25–29
Townshend JL (1963a) The pathogenicity of Pratylenchus penetrans to celery. Can J Plant Sci 43:70–74
Townshend JL (1963b) The pathogenicity of Pratylenchus penetrans to strawberry. Can J Plant Sci 43:75–78
Townshend JL (1978) Infectivity of Pratylenchus penetrans on alfalfa. J Nematol 10:318–323
Townshend JL, Stobbs L (1981) Histopathology and histochemistry of lesions caused by Pratylenchus penetrans in roots of forage legumes. Can J Plant Pathol 3:123–128
Townshend JL, Stobbs L, Carter R (1989) Ultrastructural pathology of cells affected by Pratylenchus penetrans in alfalfa roots. J Nematol 21:530–539
Troll J, Rohde RA (1966) Pathogenicity of Pratylenchus penetrans and Tylenchorhynchus claytoni on turfgrasses. Phytopathology 56:995–998
Uehara T, Kushida A, Momota Y (2001) PCR-based cloning of two beta-1,4-endoglucanases from the root-lesion nematode Pratylenchus penetrans. Nematology 3:335–341
Wheeler DL, Church DM, Lash AE, Leipe DD, Madden TL, Pontius JU, Schuler GD, Schriml LM, Tatusova TA, Wagner L, Rapp BA (2001) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 29:11–16
Wylie T, Martin J, Dante M, Mitreva M, Clifton SW, Chinwalla A, Waterston RH, Wilson RK, McCarter JP (2003) Nematode.net: a tool for navigating sequences from parasitic and free-living nematodes. Nucleic Acids Res 32:D423-D426
Wyss U (1970) Parasitierungsvorgang und Pathogenität wandernder Wurzelnematoden an Fragaria vesca var. semperflorens. Nematologica 16:55–62
Yim JJ, Brown GM (1976) Characteristics of guanosine triphosphate cyclohydrolase I purified from Escherichia coli. J Biol Chem 251:5087–5094
Zdobnov EM, Apweiler R (2001) InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848
Zunke U (1990a) Ectoparasitic feeding behaviour of the root lesion nematode, Pratylenchus penetrans , on root hairs of different host plants. Revue Nématol 13:331–337
Zunke U (1990b) Observations on the invasion and endoparasitic behavior of the root lesion nematode Pratylenchus penetrans. J Nematol 22:309–320
Acknowledgements
Plant parasitic nematode genome research at Washington University was supported by NSF Plant Genome award 0077503 to D.M.B. and S.W.C. J.P.M. was supported by a Helen Hay Whitney/Merck postdoctoral fellowship. A.A.E. was supported by the Iowa Agriculture and Home Economics Experiment Station, Ames, IA and by Hatch Act and State of Iowa funds as well as by a Storkan-Hanes-McCaslin Foundation fellowship. We thank Merry McLaird, Brandi Chiapelli, Claire Murphy, and the GSC EST Group for their role in library generation and sequencing, Todd Wylie and John Martin for bioinformatics analysis, and Robert H. Waterston for project guidance. J.P.M. and A.P.K. are employees and equity holders of Divergence Inc.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by W. R. McCombie
Electronic Supplementary Material
Rights and permissions
About this article
Cite this article
Mitreva, M., Elling, A.A., Dante, M. et al. A survey of SL1-spliced transcripts from the root-lesion nematode Pratylenchus penetrans. Mol Genet Genomics 272, 138–148 (2004). https://doi.org/10.1007/s00438-004-1054-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-004-1054-0