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. 1996 Jun;8(6):1001–1011. doi: 10.1105/tpc.8.6.1001

Decreased Susceptibility to Viral Disease of [beta]-1,3-Glucanase-Deficient Plants Generated by Antisense Transformation.

R S Beffa 1, R M Hofer 1, M Thomas 1, F Meins Jr 1
PMCID: PMC161154  PMID: 12239410

Abstract

Antifungal class I [beta]-1,3-glucanases are believed to be part of the constitutive and induced defenses of plants against fungal infection. Unexpectedly, mutants deficient in these enzymes generated by antisense transformation showed markedly reduced lesion size, lesion number, and virus yield in the local-lesion response of Havana 425 tobacco to tobacco mosaic virus (TMV) and of Nicotiana sylvestris to tobacco necrosis virus. These mutants also showed decreased severity of mosaic disease symptoms, delayed spread of symptoms, and reduced yield of virus in the susceptible response of N. sylvestris to TMV. The symptoms of disease in the responses of both plant species were positively correlated with [beta]-1,3-glucanase content in a series of independent transformants. Taken together, these results provide direct evidence that [beta]-1,3-glucanases function in viral pathogenesis. Callose, a substrate for [beta]-1,3-glucanase, acts as a physical barrier to the spread of virus. Callose deposition in and surrounding TMV-induced lesions was increased in the [beta]-1,3-glucanase-deficient, local-lesion Havana 425 host, suggesting as a working hypothesis that decreased susceptibility to virus resulted from increased deposition of callose in response to infection. Our results suggest novel means, based on antisense transformation with host genes, for protecting plants against viral infection. These observations also raise the intriguing possibility that viruses can use a defense response of the host against fungal infection[mdash]production of [beta]-1,3-glucanases[mdash]to promote their own replication and spread.

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Selected References

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  1. Beffa R. S., Neuhaus J. M., Meins F., Jr Physiological compensation in antisense transformants: specific induction of an "ersatz" glucan endo-1,3-beta-glucosidase in plants infected with necrotizing viruses. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8792–8796. doi: 10.1073/pnas.90.19.8792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ding B., Haudenshield J. S., Hull R. J., Wolf S., Beachy R. N., Lucas W. J. Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell. 1992 Aug;4(8):915–928. doi: 10.1105/tpc.4.8.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Edelbaum O., Sher N., Rubinstein M., Novick D., Tal N., Moyer M., Ward E., Ryals J., Sela I. Two antiviral proteins, gp35 and gp22, correspond to beta-1,3-glucanase and an isoform of PR-5. Plant Mol Biol. 1991 Jul;17(1):171–173. doi: 10.1007/BF00036825. [DOI] [PubMed] [Google Scholar]
  4. Kasamo K., Shimomura T. The role of the epidermis in local lesion formation and the multiplication of tobacco mosaic virus and its relation to kinetin. Virology. 1977 Jan;76(1):12–18. doi: 10.1016/0042-6822(77)90276-8. [DOI] [PubMed] [Google Scholar]
  5. Kauffmann S., Legrand M., Geoffroy P., Fritig B. Biological function of ;pathogenesis-related' proteins: four PR proteins of tobacco have 1,3-beta-glucanase activity. EMBO J. 1987 Nov;6(11):3209–3212. doi: 10.1002/j.1460-2075.1987.tb02637.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kauss H. Callose biosynthesis as a Ca2+-regulated process and possible relations to the induction of other metabolic changes. J Cell Sci Suppl. 1985;2:89–103. doi: 10.1242/jcs.1985.supplement_2.5. [DOI] [PubMed] [Google Scholar]
  7. Kjemtrup S., Borkhsenious O., Raikhel N. V., Chrispeels M. J. Targeting and release of phytohemagglutinin from the roots of bean seedlings. Plant Physiol. 1995 Oct;109(2):603–610. doi: 10.1104/pp.109.2.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Mauch F., Mauch-Mani B., Boller T. Antifungal Hydrolases in Pea Tissue : II. Inhibition of Fungal Growth by Combinations of Chitinase and beta-1,3-Glucanase. Plant Physiol. 1988 Nov;88(3):936–942. doi: 10.1104/pp.88.3.936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Mauch F., Staehelin L. A. Functional Implications of the Subcellular Localization of Ethylene-Induced Chitinase and [beta]-1,3-Glucanase in Bean Leaves. Plant Cell. 1989 Apr;1(4):447–457. doi: 10.1105/tpc.1.4.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Moore A. E., Stone B. A. Effect of infection with TMV and other viruses on the level of a -1,3-glucan hydrolase in leaves of Nicotiana glutinosa. Virology. 1972 Dec;50(3):791–798. doi: 10.1016/0042-6822(72)90433-3. [DOI] [PubMed] [Google Scholar]
  11. Ori N., Sessa G., Lotan T., Himmelhoch S., Fluhr R. A major stylar matrix polypeptide (sp41) is a member of the pathogenesis-related proteins superclass. EMBO J. 1990 Nov;9(11):3429–3436. doi: 10.1002/j.1460-2075.1990.tb07550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Payne G., Ward E., Gaffney T., Goy P. A., Moyer M., Harper A., Meins F., Jr, Ryals J. Evidence for a third structural class of beta-1,3-glucanase in tobacco. Plant Mol Biol. 1990 Dec;15(6):797–808. doi: 10.1007/BF00039420. [DOI] [PubMed] [Google Scholar]
  13. Pritchard D. W., Ross A. F. The relationship of ethylene to formation of tobacco mosaic virus lesions in hypersensitive responding tobacco leaves with and without induced resistance. Virology. 1975 Apr;64(2):295–307. doi: 10.1016/0042-6822(75)90106-3. [DOI] [PubMed] [Google Scholar]
  14. Shinshi H., Wenzler H., Neuhaus J. M., Felix G., Hofsteenge J., Meins F. Evidence for N- and C-terminal processing of a plant defense-related enzyme: Primary structure of tobacco prepro-beta-1,3-glucanase. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5541–5545. doi: 10.1073/pnas.85.15.5541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Vögeli-Lange R., Fründt C., Hart C. M., Nagy F., Meins F., Jr Developmental, hormonal, and pathogenesis-related regulation of the tobacco class I beta-1,3-glucanase B promoter. Plant Mol Biol. 1994 May;25(2):299–311. doi: 10.1007/BF00023245. [DOI] [PubMed] [Google Scholar]
  16. Ward E. R., Uknes S. J., Williams S. C., Dincher S. S., Wiederhold D. L., Alexander D. C., Ahl-Goy P., Metraux J. P., Ryals J. A. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. doi: 10.1105/tpc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Worrall D., Hird D. L., Hodge R., Paul W., Draper J., Scott R. Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell. 1992 Jul;4(7):759–771. doi: 10.1105/tpc.4.7.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Wu J. H., Dimitman J. E. Leaf structure and callose formation as determinants of TMV movement in bean leaves as revealed by UV irradiation studies. Virology. 1970 Apr;40(4):820–827. doi: 10.1016/0042-6822(70)90127-3. [DOI] [PubMed] [Google Scholar]

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