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Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins

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Abstract

Genes that are expressed during leaf senescence in Brassica napus were identified by the isolation of representative cDNA clones. DNA sequence and deduced protein sequence from two senescence-related cDNAs, LSC94 and LSC222, representing genes that are expressed early in leaf senescence before any yellowing of the leaves is visible, showed similarities to genes for pathogenesis-related (PR) proteins: a PR-1a-like protein and a class IV chitinase, respectively. The LSC94 and LSC222 genes showed differential regulation with respect to each other; an increase in expression was detected at different times during development of healthy leaves. Expression of both genes was induced by salicylic acid treatment. These findings suggest that some PR genes, as well as being induced by pathogen infection, may have alternative functions during plant development, for example in the process of leaf senescence.

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References

  1. Ainsworth CC, Clark J, Balsdon J: Expression, organisation and structure of the genes encoding the waxy protein (granule bound starch synthase) in wheat. Plant Mol Biol 22: 67–82 (1993).

    Google Scholar 

  2. Beintema JJ: Structural features of plant chitinases and chitin-binding proteins. FEBS Letters 350: 159–163 (1994).

    Google Scholar 

  3. Benhamou N, Asselin A: Attempted localisation of a substrate for chitinases in plant cells reveals abundant N-acetyl-D-glucosamine residues in secondary walls. Biol Cell 67: 341–350 (1989).

    Google Scholar 

  4. Bernhard W, Matile P: Differential expression of glutamine synthetase genes during the senescence of Arabidopsis thaliana rosette leaves. Plant Sci: 98: 7–14 (1994).

    Google Scholar 

  5. Bryngelsson T, Sommer-Knudsen J, Gregersen P, Collinge D, Ek B, Thordal-Christensen H: Purification, characterisation and molecular cloning of basic PR-1-type pathogenesis-related proteins from barley. Mol Plant-Microbe Interact 7: 267–275 (1994).

    Google Scholar 

  6. Buchanan-Wollaston V: Isolation of cDNA clones for genes that are expressed during leaf senescence in Brassica napus. Plant Physiol 104: 839–846 (1994).

    Google Scholar 

  7. Coghlan SE, Walters SR: Photosynthesis in green islands on powdery midew-infected barley leaves. Physiol Mol Plant Path 40: 31–38 (1992).

    Google Scholar 

  8. Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K: Plant chitinases. Plant J 3: 31–40 (1993).

    Google Scholar 

  9. Cote F, Hahn MG: Oligosaccharins: structures and signal transduction. Plant Mol Biol 26: 1379–1411 (1994).

    Google Scholar 

  10. Davies KM, Grierson D: Identification of cDNA clones for tomato (Lycopersicon esculentum Mill.) mRNAs that accumulate during fruit ripening and leaf senescence in response to ethylene. Planta 179: 73–80 (1989).

    Google Scholar 

  11. de Jong A, Cordewener J, Loshiavo F, Terzi M, Vanderkerckhove J, van Kammen A, de Vries SC: A carrot somatic embryo mutant is rescued by chitinase. Plant Cell 4: 425–433 (1992).

    Google Scholar 

  12. Dellaporta SL, Wood J, Hicks JB: A plant DNA minipreparation: Version II. Plant Mol Biol Rep 1(4): 19–21 (1983).

    Google Scholar 

  13. Fraser RSS: Evidence for the occurrence of the ‘pathogenesis-related’ proteins in leaves of healthy tobacco plants during flowering. Physiol Plant Path 19: 69–76 (1981).

    Google Scholar 

  14. Graham IA, Leaver CJ, Smith SM: Induction of malate synthase gene expression in senescent and detached organs of cucumber. Plant Cell 4: 349–357 (1992).

    Google Scholar 

  15. Gillikin J, Burkhardt W, Graham J: Complete amino acid sequence of a polypeptide from Zea mays similar to pathogenesis-related 1 family. Plant Physiol 96: 1372–1375 (1991).

    Google Scholar 

  16. Grüner R, Pfitzner UM: The upstream region of the gene for the pathogenesis-related protein 1a from tobacco responds to environmental as well as to developmental signals in transgenic plants. Eur J Biochem 220: 247–255 (1994).

    Google Scholar 

  17. Gut H, Matile P: Apparent induction of key enzymes of the glyoxylic acid cycle in senescent barley leaves. Planta 176: 548–550 (1988).

    Google Scholar 

  18. Hamel F, Bellemare G: Nucleotide sequence of a Brassica napus endochitinase gene. Plant Physiol 101: 1403 (1993).

    Google Scholar 

  19. Hamilton AJ, Lycett GW, Grierson D: Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 346: 284–287 (1990).

    Google Scholar 

  20. Hennig J, Dewey RE, Cutt JR, Klessig DF: Pathogen, salicylic acid and developmental dependent expression of a β-1,3-glucanase/GUS gene fusion in transgenic tobacco plants. Plant J 4: 481–493 (1993).

    Google Scholar 

  21. Hensel LL, Grbic V, Baumgarten DA, Bleecker AB: Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5: 553–564 (1993).

    Google Scholar 

  22. Hill CM, Pearson SA, Smith AJ, Rogers LJ: Inhibition of chlorophyll synthesis in Hordeum vulgare by 3-amino 2,3-dihydrobenzoic acid (gabaculin). Biosci Rep 5: 775–781 (1985).

    Google Scholar 

  23. Huffaker RC: Proteolytic activity during senescence of plants. New Phytol 116: 199–231 (1990).

    Google Scholar 

  24. Kamachi K, Yamaya T, Mae T, Ojima K: A role for glutamine synthetase in the remobilisation of leaf nitrogen during natural senescence in rice leaves. Plant Physiol 96: 411–417 (1991).

    Google Scholar 

  25. Leah R, Skriver K, Knudsen S, Ruud-Hansen J, Raikhel NV, Mundy J: Identification of an enhancer/silencer sequence directing the aleurone-specific expression of a barley chitinase gene. Plant J 6: 579–589 (1994).

    Google Scholar 

  26. Linthorst HJM: Pathogenesis-related proteins of plants. Crit Rev Plant Sci 10: 123–150 (1991).

    Google Scholar 

  27. Lohman KN, Gan S, John MC, Amasino RM: Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92: 322–328 (1994).

    Google Scholar 

  28. Lotan T, Ori N, Fluhr R: Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1: 881–887 (1989).

    Google Scholar 

  29. Margis-Pinheiro M, Metz-Boutigue MH, Awade A, Tapiade M, Retle M, Burkhard G: Isolation of complimentary DNA encoding the bean PR4 chitinase: an acidic enzyme with an amino terminus cysteine-rich domain. Plant Mol Biol 17: 243–253 (1991).

    Google Scholar 

  30. Meins F, Fritig B, Linthorst HJM, Mikkelsen JD, Neuhaus J-M, Ryals J: Plant chitinase genes. Plant Mol Biol Rep 12: 522–528 (1994).

    Google Scholar 

  31. Metzler MC, Cutt JR, Klessig DF: Isolation and characterization of a gene encoding a PR-1-like protein from Arabidopsis thaliana. Plant Physiol 96: 346–348 (1991).

    Google Scholar 

  32. Nooden LD: The phenomena of senescence and aging. In: Nooden LD, Leopold AC (eds) Senescence and Aging in Plants Academic Press, San Diego (1988).

    Google Scholar 

  33. Picton S, Barton SL, Bouzayen M, Hamilton AJ, Grierson D: Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. Plant J 3: 469–481 (1993).

    Google Scholar 

  34. Rasmussen U, Bojsen K, Collinge DB: Cloning and characterisation of a pathogen-induced chitinase in Brassica napus. Plant Mol Biol 20: 277–287 (1992).

    Google Scholar 

  35. Scholes JD, Farrar JF: Development of symptoms of brown rust of barley in relation to the distribution of fungal mycelium, starch accumulation and localised changes in the concentration of chlorophyll. New Phytol 107: 103–117 (1987).

    Google Scholar 

  36. Shinshi H, Neuhaus J-M, Ryals J, Meins F: Structure of a tobacco endochitinase gene: evidence that different chitinase genes can arise by transposition of sequences encoding a cysteine-rich domain. Plant Mol Biol 14: 357–368 (1990).

    Google Scholar 

  37. Smart CM: Gene expression during leaf senescence. New Phytol 126: 419–448 (1994).

    Google Scholar 

  38. Smart CM, Hoskin SE, Thomas H, Greaves JA, Blair BG, Schuch W: The timing of maize leaf senescence and characterisation of senescence-related cDNAs. Physiol Plant 93: 673–682 (1995).

    Google Scholar 

  39. Thomas H, Stoddart JL: Leaf senescence. Annu Rev Plant Physiol 31: 83–111 (1982).

    Google Scholar 

  40. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals R: Acquired resistance in Arabidopsis. Plant Cell 4: 645–656 (1992).

    Google Scholar 

  41. van Kan JAL, Joosten M, Wagemakers CAM, van den Berg-Velthuis GCM, de Wit P: Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum. Plant Mol Biol 20: 513–527 (1992).

    Google Scholar 

  42. van Staden J, Cook EL, Nooden LD: Cytokinins and senescence. In: Nooden LD, Leopold AC (eds) Senescence and Aging in Plants, pp. 281–328. Academic Press, San Diego (1988).

    Google Scholar 

  43. Verburg JG, Smith CE, Lisek CA, Khaihuynh Q: Identification of an essential tyrosine residue in the catalytic site of a chitinase isolated from Zea mays that is selectively modified during inactivation with 1-ethyl-3-(3-dimethylaminopropyl)-carbodiimide. J Biol Chem 267: 3886–3893 (1992).

    Google Scholar 

  44. Ward ER, Uknes SJ, Willias SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux JP, Ryals JA: Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085–1094 (1991).

    Google Scholar 

  45. Wemmer T, Kaufmann H, Kirch H-H, Schneider K, Lottspeich F, Thompson RD: The most abundant soluble basic protein of the stylar transmitting tract in potato (Solanum tuberosum L.) is an endochitinase. Planta 194: 264–273 (1994).

    Google Scholar 

  46. Yalpani N, Silverman P, Wilson TMA, Kleier DA, Raskin I: Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3: 809–818 (1991).

    Google Scholar 

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Authors and Affiliations

  1. Plant Molecular Biology Laboratory, Department of Biological Sciences, Wye College, University of London, Wye, TN25 5AH, Ashford, Kent, UK

    Colin Hanfrey, Mark Fife & Vicky Buchanan-Wollaston

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  1. Colin Hanfrey
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  2. Mark Fife
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  3. Vicky Buchanan-Wollaston
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Hanfrey, C., Fife, M. & Buchanan-Wollaston, V. Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins. Plant Mol Biol 30, 597–609 (1996). https://doi.org/10.1007/BF00049334

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  • DOI: https://doi.org/10.1007/BF00049334

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