Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The Casuarina glauca metallothionein I promoter in nodulated transgenic hairy roots of the actinorhizal plant Datisca glomerata

Behnoosh Rashidi A , Sara Mehrabi A , Kirill Demchenko B and Katharina Pawlowski A C
+ Author Affiliations
- Author Affiliations

A Department of Botany, Stockholm University, 10691 Stockholm, Sweden.

B Laboratory of Anatomy and Morphology, Komarov Botanical Institute, Russian Academy of Sciences, Prof. Popov st. 2, 197376 St Petersburg, Russia.

C Corresponding author. Email: pawlowski@botan.su.se

This paper originates from a presentation at the 16th International Meeting on Frankia and Actinorhizal Plants, Oporto, Portugal, 5–8 September 2010.

Functional Plant Biology 38(9) 728-737 https://doi.org/10.1071/FP10216
Submitted: 16 November 2010  Accepted: 25 April 2011   Published: 16 August 2011

Abstract

The activity of the promoter of a metallothionein gene expressed in actinorhizal nodules of Casuarina glauca Sieber ex Spreng., CgMT1, has previously been analysed in Casaurinaceae and in tobacco (Nicotiana tabacum L.), Arabidopsis and rice. In all these plants, the promoter showed high activity in the root cortex and epidermis, making it a useful tool for the expression of transgenes. Therefore, its activity was now analysed in transgenic root systems of Datisca glomerata (C. Presl) Baill, an actinorhizal plant from a different phylogenetic group than C. glauca, using the same CgMT1::GUS fusion as in previous studies. However, in contrast with all other plant species examined previously, the CgMT1::GUS construct showed no activity at all in D. glomerata hairy roots: the expression pattern in nodules resembled that found in C. glauca nodules. This is probably due to the changed hormone balance in hairy roots since experiments on the CgMT1::GUS construct in transgenic Arabidopsis showed that CgMT1 promoter activity was repressed by auxin or cytokinin, respectively. Yet, in hairy roots of the model legume Lotus japonicus L. induced by the same Agrobacterium rhizogenes strain, the CgMT1 promoter was active in roots and not in nodules. These results indicate that although the expression of pRi T-DNA genes leads to changes in root hormone balance, these changes do not abolish the differences in phytohormone levels or sensitivity between plant species. Therefore, gene expression data obtained using transgenic hairy root systems have to be viewed with care, not only due to the disturbed hormone balance, but also because the effects of the pRI-T-DNA genes can differ between species.

Additional keywords: Agrobacterium rhizogenes, Lotus japonicus, metallothionein, root nodules, roots.


References

Ahmadi N, Dellerme S, Laplaze L, Guermache F, Auguy F, Duhoux E, Bogusz D, Guiderdoni E, Franche C (2003) The promoter of a metallothionein-like gene from the tropical tree Casuarina glauca is active in both annual dicotyledonous and monocotyledonous plants. Transgenic Research 12, 271–281.
The promoter of a metallothionein-like gene from the tropical tree Casuarina glauca is active in both annual dicotyledonous and monocotyledonous plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFynu74%3D&md5=917d3471391e30a86c6e8cd18d9d67acCAS |

Alpizar E, Dechamp E, Espeout S, Royer M, Lecouls AC, Nicole M, Bertrand B, Lashermes P, Etienne H (2006) Efficient production of Agrobacterium rhizogenes-transformed roots and composite plants for studying gene expression in coffee roots. Plant Cell Reports 25, 959–967.
Efficient production of Agrobacterium rhizogenes-transformed roots and composite plants for studying gene expression in coffee roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotFChtLk%3D&md5=b5fd59a21459c6b5c0619f0acbb0785fCAS |

Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiological Reviews 57, 293–319.

Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 53, 159–182.
Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhtbs%3D&md5=c7c56ab2d094213b02bd971102d64150CAS |

Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57, 779–795.
Dual action of the active oxygen species during plant stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFyisrk%3D&md5=2776bdcfa58fe98b5dd129636575e73fCAS |

Desgagné-Penix I, Sponsel VM (2008) Expression of gibberellin 20-oxidase1 (AtGA20ox1) in Arabidopsis seedlings with altered auxin status is regulated at multiple levels. Journal of Experimental Botany 59, 2057–2070.
Expression of gibberellin 20-oxidase1 (AtGA20ox1) in Arabidopsis seedlings with altered auxin status is regulated at multiple levels.Crossref | GoogleScholarGoogle Scholar |

Diaz CL, Gronlund M, Schlaman HRM, Spaink HP (2005) Induction of hairy roots for symbiotic gene expression studies. In ‘Lotus japonicus handbook’. (Ed. AJ Márquez) pp. 261–277. (Springer-Verlag: Germany)

Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Research 19, 1349
A simple and rapid method for the preparation of plant genomic DNA for PCR analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXitVWju74%3D&md5=03b8a85b2953d636934cecb694594b62CAS |

Günther C, Schlereth A, Udvardi M, Ott T (2007) Metabolism of reactive oxygen species is attenuated in leghemoglobin-deficient nodules of Lotus japonicus. Molecular Plant-Microbe Interactions 20, 1596–1603.
Metabolism of reactive oxygen species is attenuated in leghemoglobin-deficient nodules of Lotus japonicus.Crossref | GoogleScholarGoogle Scholar |

Gutierrez-Gonzalvez MG, Stockert JC, Ferrer JM, Tato A (1984) Ruthenium red staining of polyanion containing structures in sections from epoxy-resin embedded tissues. Acta Histochemica 74, 115–200.

Hafeez F, Akkermans ADL, Chaudhary AH (1984) Observations on the ultrastructure of Frankia sp. in root-nodules of Datisca cannabina L. Plant and Soil 79, 383–402.
Observations on the ultrastructure of Frankia sp. in root-nodules of Datisca cannabina L.Crossref | GoogleScholarGoogle Scholar |

Heidstra R, Nilsen G, Martinez-Arbaca F, van Kammen A, Bisseling T (1997) Nod factor-induced expression of leghemoglobin to study the mechanism of NH4NO3 inhibition on root hair deformation. Molecular Plant-Microbe Interactions 10, 215–220.
Nod factor-induced expression of leghemoglobin to study the mechanism of NH4NO3 inhibition on root hair deformation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsFKgs7Y%3D&md5=f66fc33592bd798790ce9ff12f84f799CAS |

Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. California Agricultural Experiment Station Circular 347.

Kawaguchi M, Imaizumi-Anraku H, Koiwa H, Niwa S, Ikuta A, Syono K, Akao S (2002) Root, root hair, and symbiotic mutants of the model legume Lotus japonicus. Molecular Plant-Microbe Interactions 15, 17–26.
Root, root hair, and symbiotic mutants of the model legume Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlGiug%3D%3D&md5=c781f99d10082d5b8bfa5e50d986c213CAS |

Kim H-J, Koh M (2001) The effects of metallothionein on the activity of enzymes involved in removal of reactive oxygen species. Bulletin of the Korean Chemical Society 22, 362–366.

Laplaze L, Gherbi H, Duhoux E, Pawlowski K, Auguy F, Guermache F, Franche C, Bogusz D (2002) Symbiotic and nonsymbiotic expression of cgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca. Plant Molecular Biology 49, 81–92.
Symbiotic and nonsymbiotic expression of cgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtlemtLc%3D&md5=c81fccd561a37a3eb99fb3d6e3ae6adfCAS |

Lee J, Shim D, Song WY, Hwang I, Lee Y (2004) Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Molecular Biology 54, 805–815.
Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVGjurjJ&md5=8543fc74a4f81d8e1f128b2d94b1b76eCAS |

Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. The Plant Journal 38, 203–214.
Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1Kksrw%3D&md5=377f6c4522e8267a2fe2153b6d9dd5feCAS |

Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biology 6, e68
Functional adaptation of a plant receptor kinase paved the way for the evolution of intracellular root symbioses with bacteria.Crossref | GoogleScholarGoogle Scholar |

Maurel C, Barbier-Bryqoo H, Spena A, Tempe G, Guern G (1991) Single rol genes from the Agrobacterium rhizogenes T(L)-DNA alter some of the cellular responses to auxin in Nicotiana tobacum. Plant Physiology 97, 212–216.
Single rol genes from the Agrobacterium rhizogenes T(L)-DNA alter some of the cellular responses to auxin in Nicotiana tobacum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslGquro%3D&md5=6f2048fe35e1303d8bd0ee8bdf6adbe6CAS |

Miles AT, Hawksworth GM, Beattie JH, Rodilla V (2000) Induction, regulation, degradation and biological significance of mammalian metallothioneins. Critical Reviews in Biochemistry and Molecular Biology 35, 35–70.
Induction, regulation, degradation and biological significance of mammalian metallothioneins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVejsbg%3D&md5=a190f11547176dd8569d3f735e0863d2CAS |

Mirza MS, Hahn D, Akkermans ADL (1992) Isolation and characterization of Frankia strains from Coriaria nepalensis. Systematic and Applied Microbiology 15, 289–295.

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
A revised medium for rapid growth and bioassays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=06c472aaff717f5157aa29da67ee5ad0CAS |

Newcomb W, Pankhurst CE (1982) Fine structure of actinorhizal root nodules of Coriaria arborea (Coriariaceae). New Zealand Journal of Botany 20, 93–103.

Nilsson O, Olsson O (1997) Getting to the root: the role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiologia Plantarum 100, 463–473.
Getting to the root: the role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXks1yqsro%3D&md5=9b4522023b8c7f1dc83947d4e4db2f98CAS |

Nilsson O, Moritz T, Sundberg B, Sandberg G, Olsson O (1996) Expression of the Agrobacterium rhizogenes rolC gene in a deciduous forest tree alters growth and development and leads to stem fasciation. Plant Physiology 112, 492–502.

Obertello M, Wall L, Laplaze L, Michel N, Auguy F, Gherbi H, Bogusz D, Franche C (2007) Functional analysis of the metallothionein gene cgMT1 isolated from the actinorhizal tree Casuarina glauca. Molecular Plant-Microbe Interactions 20, 1231–1240.
Functional analysis of the metallothionein gene cgMT1 isolated from the actinorhizal tree Casuarina glauca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKqsbzI&md5=ee0a0290572f2179c999fc7bb2ebbb01CAS |

Omidvar V, Abdullah SN, Izadfard A, Ho CL, Mahmood M (2010) The oil palm metallothionein promoter contains a novel AGTTAGG motif conferring its fruit-specific expression and is inducible by abiotic factors. Planta 232, 925–936.
The oil palm metallothionein promoter contains a novel AGTTAGG motif conferring its fruit-specific expression and is inducible by abiotic factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVejsrvE&md5=9854489b6c17f00c5438a947456794a7CAS |

Pacios-Bras C, Schlaman HR, Boot K, Admiraal P, Langerak JM, Stougaard J, Spaink HP (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Molecular Biology 52, 1169–1180.
Auxin distribution in Lotus japonicus during root nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVCqtL4%3D&md5=6b06debd161a686e1621c41401b22bb4CAS |

Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? The Plant Cell 8, 1899–1913.

Perrine-Walker F, Doumas P, Lucas M, Vaissayre V, Beauchemin NJ, Band LR, Chopard J, Crabos A, Conejero G, Péret B, King JR, Verdeil JL, Hocher V, Franche C, Bennett MJ, Tisa LS, Laplaze L (2010) Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules. Plant Physiology 154, 1372–1380.
Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2ntrzM&md5=31c768773620c289b511ccc842f0825eCAS |

Prinsen E, Chriqui D, Vilaine F, Tepfer M, van Onckelen H (1994) Endogenous phytohormones in tobacco plants transformed with Agrobacterium rhizogenes pRi TL-DNA genes. Journal of Plant Physiology 144, 80–85.

Ross JJ, Reid JB (2010) Evolution of growth-promoting plant hormones. Functional Plant Biology 37, 795–805.
Evolution of growth-promoting plant hormones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKitbbE&md5=d40bb87a22dfc5d9d98341839f39027eCAS |

Samardžić JT, Nikolić DB, Timotijević GS, Jovanović ZS, Milisavljević MĐ, Maksimović VR (2010) Tissue expression analysis of FeMT3, a drought and oxidative stress related metallothionein gene from buckwheat (Fagopyrum esculentum). Journal of Plant Physiology 167, 1407–1411.
Tissue expression analysis of FeMT3, a drought and oxidative stress related metallothionein gene from buckwheat (Fagopyrum esculentum).Crossref | GoogleScholarGoogle Scholar |

Sambrook J, Fritsch EF, Maniatis T (1989) ‘Molecular cloning: a laboratory manual.’ 2nd edn. (Cold Spring Harbor Laboratory: Cold Spring Harbor, NY)

Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO Journal 7, 2621–2629.

Sprent JI (2006) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174, 11–25.
Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation.Crossref | GoogleScholarGoogle Scholar |

Stieger PA, Meyer AD, Kathmann P, Fründt C, Niederhauser I, Barone M, Kuhlemeier C (2004) The orf13 T-DNA gene of Agrobacterium rhizogenes confers meristematic competence to differentiated cells. Plant Physiology 135, 1798–1808.
The orf13 T-DNA gene of Agrobacterium rhizogenes confers meristematic competence to differentiated cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqtrc%3D&md5=f4ab6fc07e61dfc1ff6deb5e1414b057CAS |

Swensen S, Mullin B (1997) Phylogenetic relationships among actinorhizal plants. The impact of molecular systematics and implications for the evolution of actinorhizal symbiosis. Plant Physiology 99, 565–573.
Phylogenetic relationships among actinorhizal plants. The impact of molecular systematics and implications for the evolution of actinorhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivVWqsb8%3D&md5=0af2513a01fb9876524f72dd553f2121CAS |

Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiology 141, 373–378.
Reactive oxygen species signaling in response to pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aksbs%3D&md5=c7a1536d909de717277cba6f6852445fCAS |

Xue T, Li X, Xhu W, Wu C, Yang G, Zheng C (2009) Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast. Journal of Experimental Botany 60, 339–349.
Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvF2qurk%3D&md5=ec15823e593da426de4c987f59a1c25fCAS |

Yang Z, Wu Y, Li Y, Ling HQ, Chu C (2009) OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice. Plant Molecular Biology 70, 219–229.
OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktFShsrY%3D&md5=f5f8e8065360743869362107b03a3946CAS |

Yuan J, Chen D, Ren Y, Zhang X, Zhao J (2008) Characteristic and expression analysis of a metallothionein gene, OsMT2b, down-regulated by cytokinin suggests functions in root development and seed embryo germination or rice. Plant Physiology 146, 1637–1650.
Characteristic and expression analysis of a metallothionein gene, OsMT2b, down-regulated by cytokinin suggests functions in root development and seed embryo germination or rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvVWju7k%3D&md5=b58181fd243a98587fd65cbdc6402055CAS |

Zhu W, Zhao DX, Miao Q, Xue TT, Li XZ, Zheng CC (2009) Arabidopsis thaliana metallothionein, AtMT2a, mediates ROS balance during oxidative stress. Journal of Plant Biology 52, 585–592.
Arabidopsis thaliana metallothionein, AtMT2a, mediates ROS balance during oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFSrurzM&md5=ba0946af5adf9897a2c4cedfd2bf38d0CAS |