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Symbiotic and non-symbiotic expression of cgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca

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Abstract

A clone for a type 1 metallothionein (cgMT1) was isolated from a Casuarina glauca nodule cDNA library. The corresponding gene belongs to a small family and is highly expressed in roots and nitrogen-fixing nodules, whereas low expression was observed in aerial parts of the plant. The promoter region of cgMT1 was isolated and fused to the β-glucuronidase (gus) gene. Transgenic Casuarinaceae plants showed that the cgMT1 promoter was most active in roots and in the oldest region of the shoot. In situ hybridization indicated that in nodules cgMT1 transcript is present in mature Frankia-infected cells and in the pericycle. Possible roles for cgMT1 in symbiotic and non-symbiotic tissues are discussed.

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References

  • Andersson, C.R., Llewellyn, D.J., Peacock, W.J. and Dennis, E.S. 1997. Cell-specific expression of the promoters of two non-legume hemoglobin genes in transgenic legume, Lotus corniculatus. Plant Physiol. 113: 45-57.

    Google Scholar 

  • Andrews, G.K. 2000. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem. Pharmacol. 59: 95-104.

    Google Scholar 

  • Angulo Carmona, A.F. 1974. La formation des nodules fixateurs d'azote chez Alnus glutinosa (L.). Acta Bot. Neerl. 23: 257-303.

    Google Scholar 

  • Becana, M., Dalton, D.A., Moran, J.F., Iturbe-Ormaetxe, I., Matamoros, M.A. and Rubio, M.C. 2000. Reactive oxygen species and antioxidants in legume nodules. Physiol. Plant. 109: 372-381.

    Google Scholar 

  • Benson, D.R. and Silvester, W.B. 1993. Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57: 297-319.

    Google Scholar 

  • Berry, A.M. and Sunell, L.A. 1990. The infection process and nodule development. In: C.R. Schwintzer and J.D. Tjepkema (Eds.) The Biology of Frankia and Actinorhizal Plants, Academic Press, New York, pp. 61-81.

    Google Scholar 

  • Birch, P.R.J., Avrova, A.O., Duncan, J.M., Lyon, G.D. and Toth, R.L. 1999. Isolation of potato genes that are induced during an early stage of the hypersensitive response to Phytophtora infestans. Mol. Plant-Microbe Interact. 12: 356-361.

    Google Scholar 

  • Buchanan-Wollaston, V. 1994. Isolation of cDNA clones for genes that are expressed during leaf senescence in Brassica napus. Plant Physiol. 105: 839-846.

    Google Scholar 

  • Bugos, R.C., Chiang, V.L., Zhang, X.H., Campbell, E.R., Podila, G.K. and Campbell, W.H. 1995. RNA isolation from plant tissues recalcitrant to extraction in guanidine. Biotechniques 19: 734-737.

    Google Scholar 

  • Butt, A., Mousley, C., Morris, K., Beynon, J., Can, C., Holub, E., Greenberg, J. T. and Buchanan-Wollaston, V. 1998. Differential expression of a senescence-enhanced metallothionein gene in Arabidopsis in response to isolates of Peronospora parasitica and Pseudomonas syringae. Plant J. 16: 209-221.

    Google Scholar 

  • Callaham, D. and Torrey, J.G. 1977. Prenodule formation and primary nodule development in roots of Comptonia (Myricaceae). Can. J. Bot. 51: 2306-2318.

    Google Scholar 

  • Carnero-Diaz, E., Tagu, D. and Martin, F. 1997. Ribosomal DNA internal transcribed spacers to estimate the proportion of Pisolithus tinctorius and Eucalyptus globulus RNAs in ectomycorhiza. Appl. Environ. Microbiol. 63: 840-843.

    Google Scholar 

  • Carsolio, C., Campos, F., Sanchez, F. and Rocha-Sosa, M. 1994. The expression of a chimeric Phaseolus vulgaris nodulin 30-GUS gene is restricted to the rhizobially infected cells in transgenic Lotus corniculatus nodules. Plant Mol. Biol. 26: 1995-2001.

    Google Scholar 

  • Chen, R., Silver, D. L. and de Bruijn, F. J. 1998. Nodule parenchyma-specific expression of the Sesbania rostrata early nodulin gene SrEnod2 is mediated by its 3' untranslated region. Plant Cell 10: 1585-1602.

    Google Scholar 

  • Choi, D., Kim, H.M., Yun, H.K., Park, J.-A., Kim, W.T. and Bok, S.H. 1996. Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L. and its induction by wounding and tobacco mosaic virus induction. Plant Physiol. 112: 353-359.

    Google Scholar 

  • Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucl. Acids Res. 16: 10881-10890.

    Google Scholar 

  • de Framond, A.J. 1991. A metallothionein-like gene from maize (Zea mays): cloning and characterization. FEBS Lett. 290: 103-106.

    Google Scholar 

  • De Miranda, J.R., Thomas, M.A., Thurman, D.A. and Tomsett, A.B. 1990. Metallothionein genes from the flowering plant Mimulus guttatus. FEBS Lett. 260: 277-280.

    Google Scholar 

  • Evans, I.M., Gatehouse, L.N., Gatehouse, J.A., Robinson, N.J. and Croy, R.D.D. 1990. A gene from pea (Pisum sativum L.) with homology to metallothionein genes. FEBS Lett. 262: 29-32.

    Google Scholar 

  • Foley, R.C., Liang, Z.M. and Singh, K.B. 1997. Analysis of type 1 metallothionein cDNAs in Vicia faba. Plant Mol. Biol. 33: 583-591.

    Google Scholar 

  • Fordham-Skelton, A.P., Lilley, C., Urwin, P.E. and Robinson, N.J. 1997. GUS expression in Arabidopsis directed by 5' regions of the pea metallothionein-like gene PsMTA. Plant Mol. Biol. 34: 659-668.

    Google Scholar 

  • Franche, C., Diouf, D., Le, Q.V., N'Diaye, A., Gherbi, H., Bogusz, D., Gobé, C. and Duhoux, E. 1997. Genetic transformation of the actinorhizal tree Allocasuarina verticillata by Agrobacterium tumefaciens. Plant J. 11: 897-904.

    Google Scholar 

  • Franche, C., Diouf, D., Laplaze, L., Auguy, F., Frutz, T., Rio, M., Duhoux E. and Bogusz, D. 1998a. Soybean (lbc3), Parasponia, and Trema hemoglobin gene promoters retain symbiotic and nonsymbiotic specificity in transgenic Casuarinaceae: implications for hemoglobin gene evolution and root nodule symbioses. Mol. Plant-Microbe Interact. 11: 887-894.

    Google Scholar 

  • Franche, C., Laplaze, L., Duhoux, E. and Bogusz, D. 1998b. Actinorhizal symbioses: recent advances in plant molecular and genetic transformation studies. Crit. Rev. Plant Sci. 17: 1-28.

    Google Scholar 

  • Gherbi, H., Duhoux, E., Franche, C., Pawlowski, K., Berry, A. and Bogusz, D. 1997. Cloning of a full-length symbiotic hemoglobin cDNA and in situ localization of the corresponding mRNA in Casuarina glauca root nodule. Physiol. Plant. 99: 608-616.

    Google Scholar 

  • Girgis, Z.G.M., Ishac, Z.Y., El-Haddad, M., Saleh, A.E., Diem, H.G. and Dommergues, R.Y. 1990. First report on isolation and culture of effective Casuarina-compatible strains of Frankia from Egypt. In: M.H. El-Lakany, J.W. Turnbull and J.L. Bewbaker (Eds.) Advances in Casuarina Research and Utilisation, Desert Development Center, AUC, Cairo, pp. 156-164.

    Google Scholar 

  • Hsieh, H.M., Liu, W.K. and Huang, P.C. 1995. A novel stress-inducible metallothionein-like gene from rice. Plant Mol. Biol. 28: 381-389.

    Google Scholar 

  • Hudspeth, R.L., Hobbs, S.L., Anderson, D.M., Rajasekaran, K. and Grula, J.W. 1996. Characterization and expression of metallothionein-like genes in cotton. Plant Mol. Biol. 31: 701-705.

    Google Scholar 

  • Jorgensen, J.E., Stougaard, J. and Marcker, K.A. 1991. A two-component nodule-specific enhancer in the soybean N23 gene promoter. Plant Cell 3: 819-827.

    Google Scholar 

  • Kägi, J.H.R. 1991. Methods Enzymol. 205: 613-626.

    Google Scholar 

  • Laplaze, L., Duhoux, E., Franche, C., Frutz, T., Svistoonoff, S., Bisseling, T., Bogusz, D. and Pawlowski, K. 2000a. Casuarina glauca prenodule cells display the same diferentiation as the corresponding nodule cells. Mol. Plant-Microbe Interact. 13: 107-112.

    Google Scholar 

  • Laplaze, L., Ribeiro, A., Franche, C., Duhoux, E., Auguy, F., Bogusz, D. and Pawlowski, K. 2000b. Characterization of a Casuarina glauca nodule-specific subtilisin-like protease gene, a homolog of Alnus glutinosa ag12. Mol. Plant-Microbe Interact. 13: 113-117.

    Google Scholar 

  • Le, Q.V., Bogusz, D., Gherbi, H., Lappartient, A., Duhoux, E. and Franche, C. 1996. Agrobacterium tumefaciens gene transfer to Casuarina glauca, a tropical nitrogen-fixing tree. Plant Sci. 118: 57-69.

    Google Scholar 

  • Ledger, S.E. and Gardner, R.C. 1994. Cloning and characterization of five cDNAs for genes differentially expressed during fruit development of kiwifruit (Actinidia deliciosa var. deliciosa). Plant Mol. Biol. 25: 877-886.

    Google Scholar 

  • Loake, G.J., Faktor, O., Lamb, C.J. and Dixon, R.A. 1992. Combination of H-box [CCTACC(N)7CT] and G-box (CACGTG) cis elements is necessary for feed-forward stimulation of a chalcone synthase promoter by phenylpropanoid-patway intermediate pcoumaric acid. Proc. Natl. Acad. Sci. USA 89: 9230-9234.

    Google Scholar 

  • Macknight, R.C., Reynolds, P.H.S. and Farnden, K.J.F. 1995. Analysis of the lupin Nodulin-45 promoter: conserved regulatory sequences are important for promoter activity. Plant Mol. Biol. 27: 457-465.

    Google Scholar 

  • Pawlowski, K. and Bisseling, T. 1996. Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 6: 1899-1913.

    Google Scholar 

  • Rauser, W.E. 1999. Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin and metallothioneins. Cell Biochem. Biophys. 31: 19-48.

    Google Scholar 

  • Ribeiro, A., Akkermans, A.D.L. van Kammen, A., Bisseling, T. and Pawlowski, K. 1995. A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7: 785-794.

    Google Scholar 

  • Robinson, N.J., Tommey, A.M., Kuske, C. and Jackson, P.J. 1993. Plant metallothioneins. Biochem. J. 295: 1-10.

    Google Scholar 

  • Rushmore, T.H., Morton, M.R. and Pickett, C.B. 1991. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266: 11632-11639.

    Google Scholar 

  • Sandal, N.N., Bojsen, K. and Marker, K.A. 1987. A small family of nodule specific genes from soybean. Nucl. Acid Res. 15: 1507-1519.

    Google Scholar 

  • Sato, M. and Bremner, I. 1993. Oxygen free radicals and metallothionein. Free Rad. Biol. Med. 14: 325-337.

    Google Scholar 

  • Smouni, A., Laplaze, L., SY, M., Bogusz, D., Franche, C. and Duhoux, E. 2000. Gene transfer in actinorhizal plants of the family Casuarinaceae. In: N.S. Subba Rao and Y.R. Dommergues (Eds.) Microbial Interactions in Agriculture and Forestry, vol. 2, Science Publishers, Enfield, NH, pp. 111-129.

    Google Scholar 

  • Snowden, K.C. and Gardner, R.C. 1993. Five genes induced by aluminium in wheat (Triticum aestivum L.) roots. Plant Physiol. 103: 855-861.

    Google Scholar 

  • Stougaard, J., Sandal, N.N., Groen, A., Kühle, A. and Marcker, K.A. 1987. 5' analysis of the soybean leghemoglobin lbc3 gene: regulatory elements required for promoter activity and organ specificity. EMBO J. 6: 3565-3569.

    Google Scholar 

  • Szczyglowski, K., Szabados, L., Fujimoto, S.Y., Silver, D. and de Bruijn. 1994. Site-specific mutagenesis of the nodule-infected cell expression (NICE) element and the AT-rich element ATREBS2 of the Sesbania rostrata leghemoglobin glb3 promoter. Plant Cell 6: 317-332.

    Google Scholar 

  • Vasak, M. and Hasler, D. 2000. Metallothioneins: new functional and structural insights. Curr. Opin. Chem. Biol. 4: 177-183.

    Google Scholar 

  • Whitelaw, C.A., Le Huquet, J.A., Thurman, D.A. and Tomsett, A.B. 1997. The isolation and characterization of type II metallothionein-like genes from tomato (Lycopersicon esculentum L.). Plant Mol. Biol. 33: 503-511.

    Google Scholar 

  • Yu, L.-H., Umeda, M., Liu, J.-Y., Zhao, N.-M. and Uchimiya, H. 1998. A novel MT gene of rice plants is strongly expressed in the node portion of the stem. Gene 206: 29-35.

    Google Scholar 

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Authors and Affiliations

  1. Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK

    Laurent Laplaze

  2. UMR Amélioration et Santé des Plantes (ASP), Université B. Pascal/INRA 24, avenue des Landais, 63177 , Aubière Cedex, France

    Hassen Gherbi

  3. IRD, UR116, 911 Avenue Agropolis, 34032, Montpellier Cedex 1, France

    Laurent Laplaze, Hassen Gherbi, Emile Duhoux, Florence Auguy, Fathia Guermache, Claudine Franche & Didier Bogusz

  4. Albrecht-von-Haller-Institut für Pflanzenwissenschaften, Biochemie der Pflanze, Universität Göttingen, Untere Karspüle 2, 37073 , Göttingen, Germany

    Katharina Pawlowski

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  1. Laurent Laplaze
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  2. Hassen Gherbi
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  3. Emile Duhoux
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Laplaze, L., Gherbi, H., Duhoux, E. et al. Symbiotic and non-symbiotic expression of cgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca . Plant Mol Biol 49, 81–92 (2002). https://doi.org/10.1023/A:1014415003714

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