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. 1995 Jun;108(2):503–516. doi: 10.1104/pp.108.2.503

Hrp Mutant of Pseudomonas syringae pv phaseolicola Induces Cell Wall Alterations but Not Membrane Damage Leading to the Hypersensitive Reaction in Lettuce.

C S Bestwick 1, M H Bennett 1, J W Mansfield 1
PMCID: PMC157369  PMID: 12228488

Abstract

Both wild-type (S21-WT) and hrpD- (S21-533) strains of Pseudomonas syringae pv phaseolicola induced the formation of large paramural papillae in lettuce (Lactuca sativa) mesophyll cells adjacent to bacterial colonies. Localized alterations to the plant cell wall included deposition of hydroxyproline-rich glycoproteins, phe-nolics, and callose, and were associated with proliferation of the endoplasmic reticulum and multivesicular bodies. Tissue collapse during the hypersensitive reaction caused by S21-WT was associated with electrolyte leakage and rapid accumulation of the phy-toalexin lettucenin A, both of which followed membrane damage indicated by the failure of mesophyll cells to plasmolyze. A few cells lost the ability to plasmolyze after inoculation with S21-533, and low levels of lettucenin A were recorded, but neither leakage of electrolytes nor tissue collapse were detected. Dysfunction of the plasma membrane in cells adjacent to colonies of S21-WT led to extensive vacuolation of the cytoplasm, organelle disruption, and cytoplasmic collapse[mdash]changes unlike those occurring in cells undergoing apoptosis. Strain S21-533 remained viable within symptomless tissue, whereas cells of S21-WT were killed as a consequence of the hypersensitive reaction. Our observations emphasize the subtle coordination of the plant's response occurring at the subcellular level.

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Selected References

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  1. Baker C. J., Orlandi E. W., Mock N. M. Harpin, An Elicitor of the Hypersensitive Response in Tobacco Caused by Erwinia amylovora, Elicits Active Oxygen Production in Suspension Cells. Plant Physiol. 1993 Aug;102(4):1341–1344. doi: 10.1104/pp.102.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bowles D. J. Defense-related proteins in higher plants. Annu Rev Biochem. 1990;59:873–907. doi: 10.1146/annurev.bi.59.070190.004301. [DOI] [PubMed] [Google Scholar]
  3. Bradley D. J., Kjellbom P., Lamb C. J. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell. 1992 Jul 10;70(1):21–30. doi: 10.1016/0092-8674(92)90530-p. [DOI] [PubMed] [Google Scholar]
  4. Brady S. T. Motor neurons and neurofilaments in sickness and in health. Cell. 1993 Apr 9;73(1):1–3. doi: 10.1016/0092-8674(93)90151-f. [DOI] [PubMed] [Google Scholar]
  5. Buja L. M., Eigenbrodt M. L., Eigenbrodt E. H. Apoptosis and necrosis. Basic types and mechanisms of cell death. Arch Pathol Lab Med. 1993 Dec;117(12):1208–1214. [PubMed] [Google Scholar]
  6. Cooper J. B., Varner J. E. Insolubilization of hydroxyproline-rich cell wall glycoprotein in aerated carrot root slices. Biochem Biophys Res Commun. 1983 Apr 15;112(1):161–167. doi: 10.1016/0006-291x(83)91811-9. [DOI] [PubMed] [Google Scholar]
  7. Dietrich R. A., Delaney T. P., Uknes S. J., Ward E. R., Ryals J. A., Dangl J. L. Arabidopsis mutants simulating disease resistance response. Cell. 1994 May 20;77(4):565–577. doi: 10.1016/0092-8674(94)90218-6. [DOI] [PubMed] [Google Scholar]
  8. Driouich A., Faye L., Staehelin L. A. The plant Golgi apparatus: a factory for complex polysaccharides and glycoproteins. Trends Biochem Sci. 1993 Jun;18(6):210–214. doi: 10.1016/0968-0004(93)90191-o. [DOI] [PubMed] [Google Scholar]
  9. Everdeen D. S., Kiefer S., Willard J. J., Muldoon E. P., Dey P. M., Li X. B., Lamport D. T. Enzymic cross-linkage of monomeric extensin precursors in vitro. Plant Physiol. 1988 Jul;87(3):616–621. doi: 10.1104/pp.87.3.616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fenselau S., Balbo I., Bonas U. Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):390–396. doi: 10.1094/mpmi-5-390. [DOI] [PubMed] [Google Scholar]
  11. Graham M. Y., Graham T. L. Rapid Accumulation of Anionic Peroxidases and Phenolic Polymers in Soybean Cotyledon Tissues following Treatment with Phytophthora megasperma f. sp. Glycinea Wall Glucan. Plant Physiol. 1991 Dec;97(4):1445–1455. doi: 10.1104/pp.97.4.1445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Herman E. M., Lamb C. J. Arabinogalactan-rich glycoproteins are localized on the cell surface and in intravacuolar multivesicular bodies. Plant Physiol. 1992 Jan;98(1):264–272. doi: 10.1104/pp.98.1.264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Horn M. A., Heinstein P. F., Low P. S. Characterization of parameters influencing receptor-mediated endocytosis in cultured soybean cells. Plant Physiol. 1992 Feb;98(2):673–679. doi: 10.1104/pp.98.2.673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jakobek J. L., Lindgren P. B. Generalized Induction of Defense Responses in Bean Is Not Correlated with the Induction of the Hypersensitive Reaction. Plant Cell. 1993 Jan;5(1):49–56. doi: 10.1105/tpc.5.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lamb C. J., Lawton M. A., Dron M., Dixon R. A. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell. 1989 Jan 27;56(2):215–224. doi: 10.1016/0092-8674(89)90894-5. [DOI] [PubMed] [Google Scholar]
  16. Leach J. E., Cantrell M. A., Sequeira L. Hydroxyproline-rich bacterial agglutinin from potato : extraction, purification, and characterization. Plant Physiol. 1982 Nov;70(5):1353–1358. doi: 10.1104/pp.70.5.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Marco Y. J., Ragueh F., Godiard L., Froissard D. Transcriptional activation of 2 classes of genes during the hypersensitive reaction of tobacco leaves infiltrated with an incompatible isolate of the phytopathogenic bacterium Pseudomonas solanacearum. Plant Mol Biol. 1990 Jul;15(1):145–154. doi: 10.1007/BF00017732. [DOI] [PubMed] [Google Scholar]
  18. Martin S. J., Green D. R., Cotter T. G. Dicing with death: dissecting the components of the apoptosis machinery. Trends Biochem Sci. 1994 Jan;19(1):26–30. doi: 10.1016/0968-0004(94)90170-8. [DOI] [PubMed] [Google Scholar]
  19. Mazau D., Rumeau D., Esquerre-Tugaye M. T. Two different families of hydroxyproline-rich glycoproteins in melon callus: biochemical and immunochemical studies. Plant Physiol. 1988 Feb;86(2):540–546. doi: 10.1104/pp.86.2.540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Meier B. M., Shaw N., Slusarenko A. J. Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell death. Mol Plant Microbe Interact. 1993 Jul-Aug;6(4):453–466. doi: 10.1094/mpmi-6-453. [DOI] [PubMed] [Google Scholar]
  21. Mäder M., Amberg-Fisher V. Role of peroxidase in lignification of tobacco cells : I. Oxidation of nicotinamide adenine dinucleotide and formation of hydrogen peroxide by cell wall peroxidases. Plant Physiol. 1982 Oct;70(4):1128–1131. doi: 10.1104/pp.70.4.1128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rahme L. G., Mindrinos M. N., Panopoulos N. J. Genetic and transcriptional organization of the hrp cluster of Pseudomonas syringae pv. phaseolicola. J Bacteriol. 1991 Jan;173(2):575–586. doi: 10.1128/jb.173.2.575-586.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sen S. Programmed cell death: concept, mechanism and control. Biol Rev Camb Philos Soc. 1992 Aug;67(3):287–319. doi: 10.1111/j.1469-185x.1992.tb00727.x. [DOI] [PubMed] [Google Scholar]
  24. Swords K. M., Staehelin L. A. Complementary immunolocalization patterns of cell wall hydroxyproline-rich glycoproteins studied with the use of antibodies directed against different carbohydrate epitopes. Plant Physiol. 1993 Jul;102(3):891–901. doi: 10.1104/pp.102.3.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Vera-Estrella R., Blumwald E., Higgins V. J. Effect of Specific Elicitors of Cladosporium fulvum on Tomato Suspension Cells : Evidence for the Involvement of Active Oxygen Species. Plant Physiol. 1992 Jul;99(3):1208–1215. doi: 10.1104/pp.99.3.1208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Vianello A., Macrì F. Generation of superoxide anion and hydrogen peroxide at the surface of plant cells. J Bioenerg Biomembr. 1991 Jun;23(3):409–423. doi: 10.1007/BF00771012. [DOI] [PubMed] [Google Scholar]

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