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. 1999 Jun;11(6):1129–1140. doi: 10.1105/tpc.11.6.1129

Effect of pectin methylesterase gene expression on pea root development.

F Wen 1, Y Zhu 1, M C Hawes 1
PMCID: PMC144245  PMID: 10368183

Abstract

Expression of an inducible gene with sequences common to genes encoding pectin methylesterase (PME) was found to be tightly correlated, both spatially and temporally, with border cell separation in pea root caps. Partial inhibition of the gene's expression by antisense mRNA in transgenic pea hairy roots prevented the normal separation of root border cells from the root tip into the external environment. This phenotype was correlated with an increase in extracellular pH, reduced root elongation, and altered cellular morphology. The translation product of the gene exhibited PME activity in vitro. These results are consistent with the long-standing hypothesis that the demethylation of pectin by PME plays a key role in cell wall metabolism.

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Selected References

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  1. Albani D., Altosaar I., Arnison P. G., Fabijanski S. F. A gene showing sequence similarity to pectin esterase is specifically expressed in developing pollen of Brassica napus. Sequences in its 5' flanking region are conserved in other pollen-specific promoters. Plant Mol Biol. 1991 Apr;16(4):501–513. doi: 10.1007/BF00023417. [DOI] [PubMed] [Google Scholar]
  2. Albersheim P., An J., Freshour G., Fuller M. S., Guillen R., Ham K. S., Hahn M. G., Huang J., O'Neill M., Whitcombe A. Structure and function studies of plant cell wall polysaccharides. Biochem Soc Trans. 1994 May;22(2):374–378. doi: 10.1042/bst0220374. [DOI] [PubMed] [Google Scholar]
  3. Bordenave M., Breton C., Goldberg R., Huet J. C., Perez S., Pernollet J. C. Pectinmethylesterase isoforms from Vigna radiata hypocotyl cell walls: kinetic properties and molecular cloning of a cDNA encoding the most alkaline isoform. Plant Mol Biol. 1996 Aug;31(5):1039–1049. doi: 10.1007/BF00040722. [DOI] [PubMed] [Google Scholar]
  4. Brigham L. A., Woo H. H., Hawes M. C. Root border cells as tools in plant cell studies. Methods Cell Biol. 1995;49:377–387. doi: 10.1016/s0091-679x(08)61467-3. [DOI] [PubMed] [Google Scholar]
  5. Brigham LA, Woo HH, Wen F, Hawes MC. Meristem-specific suppression of mitosis and a global switch in gene expression in the root cap of pea by endogenous signals . Plant Physiol. 1998 Dec;118(4):1223–1231. doi: 10.1104/pp.118.4.1223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carpita N., McCann M., Griffing L. R. The plant extracellular matrix: news from the cell's frontier. Plant Cell. 1996 Sep;8(9):1451–1463. doi: 10.1105/tpc.8.9.1451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cassab G. I., Varner J. E. Immunocytolocalization of extensin in developing soybean seed coats by immunogold-silver staining and by tissue printing on nitrocellulose paper. J Cell Biol. 1987 Dec;105(6 Pt 1):2581–2588. doi: 10.1083/jcb.105.6.2581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Charnay D., Nari J., Noat G. Regulation of plant cell-wall pectin methyl esterase by polyamines--interactions with the effects of metal ions. Eur J Biochem. 1992 Apr 15;205(2):711–714. doi: 10.1111/j.1432-1033.1992.tb16833.x. [DOI] [PubMed] [Google Scholar]
  9. De Lorenzo G., Cervone F., Bellincampi D., Caprari C., Clark A. J., Desiderio A., Devoto A., Forrest R., Leckie F., Nuss L. Polygalacturonase, PGIP and oligogalacturonides in cell-cell communication. Biochem Soc Trans. 1994 May;22(2):394–397. doi: 10.1042/bst0220394. [DOI] [PubMed] [Google Scholar]
  10. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ditta G., Stanfield S., Corbin D., Helinski D. R. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347–7351. doi: 10.1073/pnas.77.12.7347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gaffe J., Tiznado M. E., Handa A. K. Characterization and functional expression of a ubiquitously expressed tomato pectin methylesterase. Plant Physiol. 1997 Aug;114(4):1547–1556. doi: 10.1104/pp.114.4.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gorshkova T. A., Chemikosova S. B., Lozovaya V. V., Carpita N. C. Turnover of Galactans and Other Cell Wall Polysaccharides during Development of Flax Plants. Plant Physiol. 1997 Jun;114(2):723–729. doi: 10.1104/pp.114.2.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hall L. N., Bird C. R., Picton S., Tucker G. A., Seymour G. B., Grierson D. Molecular characterisation of cDNA clones representing pectin esterase isozymes from tomato. Plant Mol Biol. 1994 May;25(2):313–318. doi: 10.1007/BF00023246. [DOI] [PubMed] [Google Scholar]
  15. Hawes M. C., Brigham L. A., Wen F., Woo H. H., Zhu Y. Function of root border cells in plant health: pioneers in the rhizosphere. Annu Rev Phytopathol. 1998;36:311–327. doi: 10.1146/annurev.phyto.36.1.311. [DOI] [PubMed] [Google Scholar]
  16. Hawes M. C., Lin H. J. Correlation of Pectolytic Enzyme Activity with the Programmed Release of Cells from Root Caps of Pea (Pisum sativum). Plant Physiol. 1990 Dec;94(4):1855–1859. doi: 10.1104/pp.94.4.1855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hawes M. C., Robbs S. L., Pueppke S. G. Use of a Root Tumorigenesis Assay to Detect Genotypic Variation in Susceptibility of Thirty-four Cultivars of Pisum sativum to Crown Gall. Plant Physiol. 1989 May;90(1):180–184. doi: 10.1104/pp.90.1.180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jorgensen R. A. Cosuppression, flower color patterns, and metastable gene expression States. Science. 1995 May 5;268(5211):686–691. doi: 10.1126/science.268.5211.686. [DOI] [PubMed] [Google Scholar]
  19. Joshi C. P. An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucleic Acids Res. 1987 Aug 25;15(16):6643–6653. doi: 10.1093/nar/15.16.6643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Liang X. W., Dron M., Schmid J., Dixon R. A., Lamb C. J. Developmental and environmental regulation of a phenylalanine ammonia-lyase-beta-glucuronidase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9284–9288. doi: 10.1073/pnas.86.23.9284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Markovic O., Jörnvall H. Disulfide bridges in tomato pectinesterase: variations from pectinesterases of other species; conservation of possible active site segments. Protein Sci. 1992 Oct;1(10):1288–1292. doi: 10.1002/pro.5560011007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Moustacas A. M., Nari J., Diamantidis G., Noat G., Crasnier M., Borel M., Ricard J. Electrostatic effects and the dynamics of enzyme reactions at the surface of plant cells. 2. The role of pectin methyl esterase in the modulation of electrostatic effects in soybean cell walls. Eur J Biochem. 1986 Feb 17;155(1):191–197. doi: 10.1111/j.1432-1033.1986.tb09476.x. [DOI] [PubMed] [Google Scholar]
  23. Mu J. H., Stains J. P., Kao T. Characterization of a pollen-expressed gene encoding a putative pectin esterase of Petunia inflata. Plant Mol Biol. 1994 Jun;25(3):539–544. doi: 10.1007/BF00043881. [DOI] [PubMed] [Google Scholar]
  24. Murray M. G., Thompson W. F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980 Oct 10;8(19):4321–4325. doi: 10.1093/nar/8.19.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nari J., Noat G., Diamantidis G., Woudstra M., Ricard J. Electrostatic effects and the dynamics of enzyme reactions at the surface of plant cells. 3. Interplay between limited cell-wall autolysis, pectin methyl esterase activity and electrostatic effects in soybean cell walls. Eur J Biochem. 1986 Feb 17;155(1):199–202. doi: 10.1111/j.1432-1033.1986.tb09477.x. [DOI] [PubMed] [Google Scholar]
  26. Richard L., Qin L. X., Goldberg R. Clustered genes within the genome of Arabidopsis thaliana encoding pectin methylesterase-like enzymes. Gene. 1996 May 8;170(2):207–211. doi: 10.1016/0378-1119(95)00766-0. [DOI] [PubMed] [Google Scholar]
  27. Robbs S. L., Hawes M. C., Lin H. J., Pueppke S. G., Smith L. Y. Inheritance of Resistance to Crown Gall in Pisum sativum. Plant Physiol. 1991 Jan;95(1):52–57. doi: 10.1104/pp.95.1.52. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Saghai-Maroof M. A., Soliman K. M., Jorgensen R. A., Allard R. W. Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci U S A. 1984 Dec;81(24):8014–8018. doi: 10.1073/pnas.81.24.8014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schmid J., Doerner P. W., Clouse S. D., Dixon R. A., Lamb C. J. Developmental and environmental regulation of a bean chalcone synthase promoter in transgenic tobacco. Plant Cell. 1990 Jul;2(7):619–631. doi: 10.1105/tpc.2.7.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stephenson M. B., Hawes M. C. Correlation of Pectin Methylesterase Activity in Root Caps of Pea with Root Border Cell Separation. Plant Physiol. 1994 Oct;106(2):739–745. doi: 10.1104/pp.106.2.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Thomas N. S., Matts R. L., Petryshyn R., London I. M. Distribution of reversing factor in reticulocyte lysates during active protein synthesis and on inhibition by heme deprivation or double-stranded RNA. Proc Natl Acad Sci U S A. 1984 Nov;81(22):6998–7002. doi: 10.1073/pnas.81.22.6998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tieman D. M., Handa A. K. Reduction in Pectin Methylesterase Activity Modifies Tissue Integrity and Cation Levels in Ripening Tomato (Lycopersicon esculentum Mill.) Fruits. Plant Physiol. 1994 Oct;106(2):429–436. doi: 10.1104/pp.106.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tieman D. M., Harriman R. W., Ramamohan G., Handa A. K. An Antisense Pectin Methylesterase Gene Alters Pectin Chemistry and Soluble Solids in Tomato Fruit. Plant Cell. 1992 Jun;4(6):667–679. doi: 10.1105/tpc.4.6.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Town C. D., Dominov J. A., Karpinski B. A., Jentoft J. E. Relationships between extracellular pH, intracellular pH, and gene expression in Dictyostelium discoideum. Dev Biol. 1987 Aug;122(2):354–362. doi: 10.1016/0012-1606(87)90300-9. [DOI] [PubMed] [Google Scholar]
  35. Twell D., Yamaguchi J., Wing R. A., Ushiba J., McCormick S. Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev. 1991 Mar;5(3):496–507. doi: 10.1101/gad.5.3.496. [DOI] [PubMed] [Google Scholar]
  36. Woo H. H., Brigham L. A., Hawes M. C. Primary structure of the mRNA encoding a 16.5-kDa ubiquitin-conjugating enzyme of Pisum sativum. Gene. 1994 Oct 21;148(2):369–370. doi: 10.1016/0378-1119(94)90715-3. [DOI] [PubMed] [Google Scholar]

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