Abstract
Sedentary plant-parasitic nematodes are able to induce the redifferentiation of root cells into multinucleate nematode feeding sites (NFSs). We have isolated by promoter trapping an Arabidopsis thaliana gene that is essential for the early steps of NFS formation induced by the root-knot nematode Meloidogyne incognita. Its pattern of expression is similar to that of key regulators of the cell cycle, but it is not observed with the cyst nematode. Later in NFS development, this gene is induced by both root-knot and cyst nematodes. It encodes a protein similar to the D-ribulose-5-phosphate 3-epimerase (RPE) (EC 5.1.3.1), a key enzyme in the reductive Calvin cycle and the oxidative pentose phosphate pathway (OPPP). Quantitative RT-PCR showed the accumulation of RPE transcripts in potato, as in Arabidopsis NFS. Homozygous rpe plants have a germination mutant phenotype that can be rescued in dwarf plants on sucrose-supplemented medium. During root development, this gene is expressed in the meristems and initiation sites of lateral roots. These results suggest that the genetic control of NFSs and the first stages of meristem formation share common steps and confirms the previous cytological observations which indicate that root cells undergo metabolic reprogramming when they turn into NFSs.
Full Text
The Full Text of this article is available as a PDF (875.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Atamna H., Pascarmona G., Ginsburg H. Hexose-monophosphate shunt activity in intact Plasmodium falciparum-infected erythrocytes and in free parasites. Mol Biochem Parasitol. 1994 Sep;67(1):79–89. doi: 10.1016/0166-6851(94)90098-1. [DOI] [PubMed] [Google Scholar]
- Barrett M. P. The pentose phosphate pathway and parasitic protozoa. Parasitol Today. 1997 Jan;13(1):11–16. doi: 10.1016/s0169-4758(96)10075-2. [DOI] [PubMed] [Google Scholar]
- Barthels N., van der Lee F. M., Klap J., Goddijn O. J., Karimi M., Puzio P., Grundler F. M., Ohl S. A., Lindsey K., Robertson L. Regulatory sequences of Arabidopsis drive reporter gene expression in nematode feeding structures. Plant Cell. 1997 Dec;9(12):2119–2134. doi: 10.1105/tpc.9.12.2119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bird D. M., Wilson M. A. DNA sequence and expression analysis of root-knot nematode-elicited giant cell transcripts. Mol Plant Microbe Interact. 1994 May-Jun;7(3):419–424. doi: 10.1094/mpmi-7-0419. [DOI] [PubMed] [Google Scholar]
- Blattner F. R., Burland V., Plunkett G., 3rd, Sofia H. J., Daniels D. L. Analysis of the Escherichia coli genome. IV. DNA sequence of the region from 89.2 to 92.8 minutes. Nucleic Acids Res. 1993 Nov 25;21(23):5408–5417. doi: 10.1093/nar/21.23.5408. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brinkmann H., Martin W. Higher-plant chloroplast and cytosolic 3-phosphoglycerate kinases: a case of endosymbiotic gene replacement. Plant Mol Biol. 1996 Jan;30(1):65–75. doi: 10.1007/BF00017803. [DOI] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Conkling M. A., Cheng C. L., Yamamoto Y. T., Goodman H. M. Isolation of transcriptionally regulated root-specific genes from tobacco. Plant Physiol. 1990 Jul;93(3):1203–1211. doi: 10.1104/pp.93.3.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Creusot F., Fouilloux E., Dron M., Lafleuriel J., Picard G., Billault A., Le Paslier D., Cohen D., Chabouté M. E., Durr A. The CIC library: a large insert YAC library for genome mapping in Arabidopsis thaliana. Plant J. 1995 Nov;8(5):763–770. doi: 10.1046/j.1365-313x.1995.08050763.x. [DOI] [PubMed] [Google Scholar]
- Dean C., Tamaki S., Dunsmuir P., Favreau M., Katayama C., Dooner H., Bedbrook J. mRNA transcripts of several plant genes are polyadenylated at multiple sites in vivo. Nucleic Acids Res. 1986 Mar 11;14(5):2229–2240. doi: 10.1093/nar/14.5.2229. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Earp D. J., Lowe B., Baker B. Amplification of genomic sequences flanking transposable elements in host and heterologous plants: a tool for transposon tagging and genome characterization. Nucleic Acids Res. 1990 Jun 11;18(11):3271–3279. doi: 10.1093/nar/18.11.3271. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Falcone D. L., Tabita F. R. Complementation analysis and regulation of CO2 fixation gene expression in a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion strain of Rhodospirillum rubrum. J Bacteriol. 1993 Aug;175(16):5066–5077. doi: 10.1128/jb.175.16.5066-5077.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferreira P. C., Hemerly A. S., Engler J. D., van Montagu M., Engler G., Inzé D. Developmental expression of the arabidopsis cyclin gene cyc1At. Plant Cell. 1994 Dec;6(12):1763–1774. doi: 10.1105/tpc.6.12.1763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fleischmann R. D., Adams M. D., White O., Clayton R. A., Kirkness E. F., Kerlavage A. R., Bult C. J., Tomb J. F., Dougherty B. A., Merrick J. M. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. doi: 10.1126/science.7542800. [DOI] [PubMed] [Google Scholar]
- Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gavel Y., von Heijne G. A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett. 1990 Feb 26;261(2):455–458. doi: 10.1016/0014-5793(90)80614-o. [DOI] [PubMed] [Google Scholar]
- Gheysen G., Montagu M. V., Zambryski P. Integration of Agrobacterium tumefaciens transfer DNA (T-DNA) involves rearrangements of target plant DNA sequences. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6169–6173. doi: 10.1073/pnas.84.17.6169. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilliland G., Perrin S., Blanchard K., Bunn H. F. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2725–2729. doi: 10.1073/pnas.87.7.2725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goddijn O. J., Lindsey K., van der Lee F. M., Klap J. C., Sijmons P. C. Differential gene expression in nematode-induced feeding structures of transgenic plants harbouring promoter-gusA fusion constructs. Plant J. 1993 Nov;4(5):863–873. doi: 10.1046/j.1365-313x.1993.04050863.x. [DOI] [PubMed] [Google Scholar]
- Hemerly A. S., Ferreira P., de Almeida Engler J., Van Montagu M., Engler G., Inzé D. cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell. 1993 Dec;5(12):1711–1723. doi: 10.1105/tpc.5.12.1711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jefferson R. A., Kavanagh T. A., Bevan M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Joshi C. P. Putative polyadenylation signals in nuclear genes of higher plants: a compilation and analysis. Nucleic Acids Res. 1987 Dec 10;15(23):9627–9640. doi: 10.1093/nar/15.23.9627. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaneko S., Murakami S., Unoura M., Kobayashi K. Quantitation of hepatitis C virus RNA by competitive polymerase chain reaction. J Med Virol. 1992 Aug;37(4):278–282. doi: 10.1002/jmv.1890370408. [DOI] [PubMed] [Google Scholar]
- Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M., Sasamoto S. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 1996 Jun 30;3(3):109–136. doi: 10.1093/dnares/3.3.109. [DOI] [PubMed] [Google Scholar]
- Kertbundit S., De Greve H., Deboeck F., Van Montagu M., Hernalsteens J. P. In vivo random beta-glucuronidase gene fusions in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5212–5216. doi: 10.1073/pnas.88.12.5212. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
- Koncz C., Martini N., Mayerhofer R., Koncz-Kalman Z., Körber H., Redei G. P., Schell J. High-frequency T-DNA-mediated gene tagging in plants. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8467–8471. doi: 10.1073/pnas.86.21.8467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koncz C., Mayerhofer R., Koncz-Kalman Z., Nawrath C., Reiss B., Redei G. P., Schell J. Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana. EMBO J. 1990 May;9(5):1337–1346. doi: 10.1002/j.1460-2075.1990.tb08248.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986 Jan 31;44(2):283–292. doi: 10.1016/0092-8674(86)90762-2. [DOI] [PubMed] [Google Scholar]
- Kusian B., Yoo J. G., Bednarski R., Bowien B. The Calvin cycle enzyme pentose-5-phosphate 3-epimerase is encoded within the cfx operons of the chemoautotroph Alcaligenes eutrophus. J Bacteriol. 1992 Nov;174(22):7337–7344. doi: 10.1128/jb.174.22.7337-7344.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lyngstadaas A., Løbner-Olesen A., Boye E. Characterization of three genes in the dam-containing operon of Escherichia coli. Mol Gen Genet. 1995 Jun 10;247(5):546–554. doi: 10.1007/BF00290345. [DOI] [PubMed] [Google Scholar]
- Martin W., Brinkmann H., Savonna C., Cerff R. Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8692–8696. doi: 10.1073/pnas.90.18.8692. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayerhofer R., Koncz-Kalman Z., Nawrath C., Bakkeren G., Crameri A., Angelis K., Redei G. P., Schell J., Hohn B., Koncz C. T-DNA integration: a mode of illegitimate recombination in plants. EMBO J. 1991 Mar;10(3):697–704. doi: 10.1002/j.1460-2075.1991.tb07999.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meyerowitz E. M. Arabidopsis, a useful weed. Cell. 1989 Jan 27;56(2):263–269. doi: 10.1016/0092-8674(89)90900-8. [DOI] [PubMed] [Google Scholar]
- Miosga T., Zimmermann F. K. Cloning and characterization of the first two genes of the non-oxidative part of the Saccharomyces cerevisiae pentose-phosphate pathway. Curr Genet. 1996 Nov;30(5):404–409. doi: 10.1007/s002940050149. [DOI] [PubMed] [Google Scholar]
- Niebel A., De Almeida Engler J., Tire C., Engler G., Van Montagu M., Gheysen G. Induction Patterns of an Extensin Gene in Tobacco upon Nematode Infection. Plant Cell. 1993 Dec;5(12):1697–1710. doi: 10.1105/tpc.5.12.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Niebel A., Heungens K., Barthels N., Inzé D., Van Montagu M., Gheysen G. Characterization of a pathogen-induced potato catalase and its systemic expression upon nematode and bacterial infection. Mol Plant Microbe Interact. 1995 May-Jun;8(3):371–378. doi: 10.1094/mpmi-8-0371. [DOI] [PubMed] [Google Scholar]
- Niebel A., de Almeida Engler J., Hemerly A., Ferreira P., Inzé D., Van Montagu M., Gheysen G. Induction of cdc2a and cyc1At expression in Arabidopsis thaliana during early phases of nematode-induced feeding cell formation. Plant J. 1996 Dec;10(6):1037–1043. doi: 10.1046/j.1365-313x.1996.10061037.x. [DOI] [PubMed] [Google Scholar]
- Nowitzki U., Wyrich R., Westhoff P., Henze K., Schnarrenberger C., Martin W. Cloning of the amphibolic Calvin cycle/OPPP enzyme D-ribulose-5-phosphate 3-epimerase (EC 5.1.3.1) from spinach chloroplasts: functional and evolutionary aspects. Plant Mol Biol. 1995 Dec;29(6):1279–1291. doi: 10.1007/BF00020468. [DOI] [PubMed] [Google Scholar]
- Opperman C. H., Taylor C. G., Conkling M. A. Root-knot nematode--directed expression of a plant root--specific gene. Science. 1994 Jan 14;263(5144):221–223. doi: 10.1126/science.263.5144.221. [DOI] [PubMed] [Google Scholar]
- Ruwende C., Khoo S. C., Snow R. W., Yates S. N., Kwiatkowski D., Gupta S., Warn P., Allsopp C. E., Gilbert S. C., Peschu N. Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature. 1995 Jul 20;376(6537):246–249. doi: 10.1038/376246a0. [DOI] [PubMed] [Google Scholar]
- Schiefelbein J. W., Benfey P. N. The development of plant roots: new approaches to underground problems. Plant Cell. 1991 Nov;3(11):1147–1154. doi: 10.1105/tpc.3.11.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmidt R., Love K., West J., Lenehan Z., Dean C. Description of 31 YAC contigs spanning the majority of Arabidopsis thaliana chromosome 5. Plant J. 1997 Mar;11(3):563–572. doi: 10.1046/j.1365-313x.1997.11030563.x. [DOI] [PubMed] [Google Scholar]
- Schnarrenberger C., Flechner A., Martin W. Enzymatic Evidence for a Complete Oxidative Pentose Phosphate Pathway in Chloroplasts and an Incomplete Pathway in the Cytosol of Spinach Leaves. Plant Physiol. 1995 Jun;108(2):609–614. doi: 10.1104/pp.108.2.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sijmons P. C. Plant-nematode interactions. Plant Mol Biol. 1993 Dec;23(5):917–931. doi: 10.1007/BF00021809. [DOI] [PubMed] [Google Scholar]
- Teige M., Kopriva S., Bauwe H., Süss K. H. Chloroplast pentose-5-phosphate 3-epimerase from potato: cloning, cDNA sequence, and tissue-specific enzyme accumulation. FEBS Lett. 1995 Dec 27;377(3):349–352. doi: 10.1016/0014-5793(95)01373-3. [DOI] [PubMed] [Google Scholar]
- Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Topping J. F., Wei W., Lindsey K. Functional tagging of regulatory elements in the plant genome. Development. 1991 Aug;112(4):1009–1019. doi: 10.1242/dev.112.4.1009. [DOI] [PubMed] [Google Scholar]
- Van der Eycken W., de Almeida Engler J., Inzé D., Van Montagu M., Gheysen G. A molecular study of root-knot nematode-induced feeding sites. Plant J. 1996 Jan;9(1):45–54. doi: 10.1046/j.1365-313x.1996.09010045.x. [DOI] [PubMed] [Google Scholar]
- White O., Soderlund C., Shanmugan P., Fields C. Information contents and dinucleotide compositions of plant intron sequences vary with evolutionary origin. Plant Mol Biol. 1992 Sep;19(6):1057–1064. doi: 10.1007/BF00040537. [DOI] [PubMed] [Google Scholar]
- Williamson V. M., Hussey R. S. Nematode pathogenesis and resistance in plants. Plant Cell. 1996 Oct;8(10):1735–1745. doi: 10.1105/tpc.8.10.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wood T. Physiological functions of the pentose phosphate pathway. Cell Biochem Funct. 1986 Oct;4(4):241–247. doi: 10.1002/cbf.290040403. [DOI] [PubMed] [Google Scholar]
- Yamamoto Y. T., Taylor C. G., Acedo G. N., Cheng C. L., Conkling M. A. Characterization of cis-acting sequences regulating root-specific gene expression in tobacco. Plant Cell. 1991 Apr;3(4):371–382. doi: 10.1105/tpc.3.4.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
- von Heijne G., Steppuhn J., Herrmann R. G. Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem. 1989 Apr 1;180(3):535–545. doi: 10.1111/j.1432-1033.1989.tb14679.x. [DOI] [PubMed] [Google Scholar]
