A transgenic dTph1 insertional mutagenesis system for forward genetics in mycorrhizal phosphate transport of Petunia

Plant Journal

Volumn 54, Issue 6, 2008, Pages 1115-1127

  Wegmüller, Sarah ^a,g   Svistoonoff, Sergio ^a,d   Reinhardt, Didier ^b   Stuurman, Jeroen ^c,e   Amrhein, Nikolaus ^a   Bucher, Marcel ^a,f  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^e KEYGENE N V   (Netherlands)

^f UNIVERSITY OF COLOGNE   (Germany)

^g UNIVERSITY OF APPLIED SCIENCES WESTERN SWITZERLAND   (Switzerland)

Author keywords

Forward genetics; Luciferase; Mycorrhiza; Petunia; Phosphate transporter; Transposon mutagenesis

Indexed keywords

PHOSPHATE; PHOSPHATE TRANSPORTER; PLANT DNA; VEGETABLE PROTEIN;

ARTICLE; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETICS; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOLECULAR CLONING; MYCORRHIZA; PETUNIA; PLANT ROOT; PROMOTER REGION; SYMBIOSIS; TRANSGENIC PLANT; TRANSPOSON;

CLONING, MOLECULAR; DNA TRANSPOSABLE ELEMENTS; DNA, PLANT; GENE EXPRESSION REGULATION, PLANT; GENETIC MARKERS; MUTAGENESIS, INSERTIONAL; MYCORRHIZAE; PETUNIA; PHOSPHATE TRANSPORT PROTEINS; PHOSPHATES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; SYMBIOSIS;

FUNGI; PETUNIA; PETUNIA X HYBRIDA;

EID: 44849117894     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03474.x     Document Type: Article

References (71)

1. van Aarle, I.M., Cavagnaro, T.R., Smith, S.E., Smith, F.A. Dickson, S. (2005) Metabolic activity of Glomus intraradices in Arum- and Paris-type arbuscular mycorrhizal colonization. New Phytol. 166, 611 618.
2. Alonso, J.M. Ecker, J.R. (2006) Moving forward in reverse: genetic technologies to enable genome-wide phenomic screens in Arabidopsis. Nat. Rev. Genet. 7, 524 536.
3. Ane, J.M., Kiss, G.B., Riely, B.K., Penmetsa, R.V., Oldroyd, G.E.D., Ayax, C., Levy, J., Debelle, F., Baek, J.M. Kalo, P. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science, 303, 1364 1367.
4. Ausubel, F.M., Bahnsen, K. Hanson, M. (1980) Cell and tissue culture of haploid and diploid Petunia'Mitchell'. Plant Mol. Biol. Newsletter, 1, 26 31.
5. Barker, S.J., Stummer, B., Gao, L., Dispain, I., O'Connor, P.J. Smith, S.E. (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation. Plant J. 15, 791 797.
6. Bevan, M. (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12, 8711 8722.
7. Brugliera, F., Holton, T.A., Stevenson, T.W., Farcy, E., Lu, C.-Y. Cornish, E.C. (1994) Isolation and characterization of a cDNA clone corresponding to the Rt locus of Petunia hybrida. Plant J. 5, 81 92.
8. Brundrett, M.C., Piche, Y. Peterson, R.L. (1984) A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can. J. Bot. 62, 2128 2134.
9. Bucher, M., Rausch, C. Daram, P. (2001) Molecular and biochemical mechanisms of phosphorus uptake into plants. J. Plant Nutr. Soil Sci. 164, 209 217.
10. Chen, A., Hu, J., Sun, S. Xu, G. (2007) Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol. 173, 817 831.
11. David-Schwartz, R., Badani, H., Smadar, W., Levy, A.A., Galili, G. Kapulnik, Y. (2001) Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae. Plant J. 27, 561 569.
12. David-Schwartz, R., Gadkar, V., Wininger, S., Bendov, R., Galili, G., Levy, A.A. Kapulnik, Y. (2003) Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization. Mol. Plant-Microbe Interact. 16, 382 388.
13. De Keukeleire, P. (2001) Analysis by transposon display of the behavior of the dTph1 element family during ontogeny and inbreeding of Petunia hybrida. Mol. Genet. Genomics, 265, 72 81.
14. De Wilde, C., Van Houdt, H., De Buck, S., Angenon, G., De Jaeger, G. Depicker, A. (2000) Plants as bioreactors for protein production: avoiding the problem of transgene silencing. Plant Mol. Biol. 43, 347 359.
15. Dellaporta, S.L., Wood, J. Hicks, J.B. (1983) A rapid method for DNA extraction from plant tissue. Plant Mol. Biol. Rep. 1, 19 21.
16. Depicker, A., Stachel, S., Dhaese, P., Zambryski, P. Goodman, H.M. (1982) Nopaline synthase: transcript mapping and DNA sequence. J. Mol. Appl. Genet. 1, 561 573.
17. Deroles, S.C. Gardner, R.C. (1988) Expression and inheritance of kanamycin resistance in a large number of transgenic Petunias generated by Agrobacterium-mediated transformation. Plant Mol. Biol. 11, 355 364.
18. Doodeman, M., Boersma, E.A., Koomen, W. Bianchi, F. (1984) Genetic analysis of instability in Petunia hybrida. I: a highly unstable mutation induced by a transposable element inserted at the An 1 locus for flower colour. Theor. Appl. Genet. 67, 345 355.
19. Drissner, D., Kunze, G., Callewaert, N., Gehrig, P., Tamasloukht, M.B., Boller, T., Felix, G., Amrhein, N. Bucher, M. (2007) Lyso-phosphatidylcholine is a signal in the arbuscular mycorrhizal symbiosis. Science, 318, 265 268.
20. Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P. Kiss, G.B. (2002) A receptor kinase gene regulating symbiotic nodule development. Nature, 417, 962 966.
21. Fillatti, J.J., Kiser, J., Rose, R. Comai, L. (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Bio-technology, 5, 726 730.
22. Gerats, T. Vandenbussche, M. (2005) A model system for comparative research: Petunia. Trends Plant Sci. 10, 251 256.
23. Gerats, A.G.M., Huits, H., Vrijlandt, E., Marana, C., Souer, E. Beld, M. (1990) Molecular characterization of a nonautonomous transposable element (dTph1) of Petunia. Plant Cell, 2, 1121 1128.
24. Hoagland, D.R. Broyer, T.C. (1936) General nature of the process of salt accumulation by roots with description of experimental methods 1. Plant Physiol. 11, 471 507.
25. Holton, T.A., Brugliera, F. Tanaka, Y. (1993) Cloning and expression of flavonol synthase from Petunia hybrida. Plant J. 4, 1003 1010.
26. van Houwelingen, A., Souer, E., Spelt, K., Kloos, D., Mol, J. Koes, R. (1998) Analysis of flower pigmentation mutants generated by random transposon mutagenesis in Petunia hybrida. Plant J. 13, 39 50.
27. Imaizumi-Anraku, H., Takeda, N., Charpentier, M., Perry, J., Miwa, H., Umehara, Y., Kouchi, H., Murakami, Y., Mulder, L. Vickers, K. (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature, 433, 527 531.
28. Javot, H., Penmetsa, R.V., Terzaghi, N., Cook, D.R. Harrison, M.J. (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. USA, 104, 1720 1725.
29. Jefferson, R.A., Kavanagh, T.A. Bevan, M.W. (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901 3907.
30. Karandashov, V., Nagy, R., Wegmuller, S., Amrhein, N. Bucher, M. (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. USA, 101, 6285 6290.
31. Kistner, C. Parniske, M. (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci. 7, 511 518.
32. Kroon, J., Souer, E., de Graaff, A., Xue, Y., Mol, J. Koes, R. (1994) Cloning and structural analysis of the anthocyanin pigmentation locus Rt of Petunia hybrida: characterization of insertion sequences in two mutant alleles. Plant J. 5, 69 80.
33. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361 1364.
34. Maeda, D., Ashida, K., Iguchi, K., Chechetka, S.A., Hijikata, A., Okusako, Y., Deguchi, Y., Izui, K. Hata, S. (2006) Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol. 47, 807 817.
35. Marschner, H. (1995) Mineral Nutrition of Higher Plants, 2nd edn. London : Academic Press.
36. Martirani, L., Stiller, J., Mirabella, R., Alfano, F., Lamberti, A., Radutoiu, S.E., Iaccarino, M., Gresshoff, P.M. Chiurazzi, M. (1999) T-DNA tagging of nodulation- and root-related genes in Lotus japonicus: expression patterns and potential for promoter trapping and insertional mutagenesis. Mol. Plant-Microbe Interact. 12, 275 284.
37. Millar, A.J., Short, S.R., Hiratsuka, K., Chua, N.H. Kay, S.A. (1992) Firefly luciferase as a reporter of regulated gene expression in higher plants. Plant Mol. Biol. Rep. 10, 324 337.
38. Misson, J., Thibaud, M.C., Bechtold, N., Raghothama, K. Nussaume, L. (2004) Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol. Biol. 55, 727 741.
39. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc. Natl Acad. Sci. USA, 101, 4701 4705.
40. Murashige, T. Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473 494.
41. Nagy, R., Karandashov, V., Chague, V., Kalinkevich, K., Tamasloukht, M., Xu, G., Jakobsen, I., Levy, A.A., Amrhein, N. Bucher, M. (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J. 42, 236 250.
42. Ohno, T. Zibilske, L.M. (1991) Determination of low concentrations of phosphorous in soil extracts using malachite green. Soil Sci. Soc. Am. J. 55, 892 895.
43. Oldroyd, G.E.D. (2001) Dissecting symbiosis: developments in Nod factor signal transduction. Ann. Bot. 87, 709 718.
44. Oldroyd, G.E.D. Downie, J.A. (2006) Nuclear calcium changes at the core of symbiosis signalling. Curr. Opin. Plant Biol. 9, 351 357.
45. Paszkowski, U. (2006) Tansley review. A journey through signaling in arbuscular mycorrhizal symbioses 2006. New Phytol. 172, 35 46.
46. Paszkowski, U., Jakovleva, L. Boller, T. (2006) Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. Plant J. 47, 165 173.
47. Pearse, A.G.E. (1968) Histochemistry: Theoretical and Applied, Vol. 2. London : Churchill.
48. 33P. New Phytol. 124, 489 494.
49. Poulsen, K.H., Nagy, R., Gao, L.L., Smith, S.E., Bucher, M., Smith, F.A. Jakobsen, I. (2005) Physiological and molecular evidence for Pi uptake via the symbiotic pathway in a reduced mycorrhizal colonization mutant in tomato associated with a compatible fungus. New Phytol. 168, 445 454.
50. Quattrocchio, F., Wing, J., van der Woude, K., Souer, E., de Vetten, N., Mol, J. Koes, R. (1999) Molecular analysis of the anthocyanin2 gene of Petunia and its role in the evolution of flower color. Plant Cell, 11, 1433 1444.
51. Rausch, C., Daram, P., Brunner, S., Jansa, J., Laloi, M., Leggewie, G., Amrhein, N. Bucher, M. (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature, 414, 462 470.
52. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
53. Schauser, L. (1998) Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Mol. Gen. Genet. 259, 414 423.
54. Scholte, M., d'Erfurth, I., Rippa, S., Mondy, S., Cosson, V., Durand, P., Breda, C., Trinh, H., Rodriguez-Llorente, I. Kondorosi, E. (2002) T-DNA tagging in the model legume Medicago truncatula allows efficient gene discovery. Mol. Breed. 10, 203 215.
55. Sekhara Reddy, D.M.R., Schorderet, M., Feller, U. Reinhardt, D. (2007) A Petunia mutant affected in intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi. Plant J. 51, 739 750.
56. Shin, H., Shin, H.S., Dewbre, G.R. Harrison, M.J. (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J. 39, 629 642.
57. Smith, S.E. Read, D.J. (1997) Mycorrhizal Symbiosis, 2nd edn. Cambridge : Academic Press Ltd.
58. Smith, S.E., Smith, F.A. Jakobsen, I. (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 133, 16 20.
59. Spelt, C., Quattrocchio, F., Mol, J.N.M. Koes, R. (2000) Anthocyanin1 of Petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell, 12, 1619 1632.
60. Spelt, C., Quattrocchio, F., Mol, J. Koes, R. (2002) ANTHOCYANIN1 of Petunia controls pigment synthesis, vacuolar pH, and seed coat development by genetically distinct mechanisms. Plant Cell, 14, 2121 2135.
61. Stracke, S., Kistner, C., Yoshida, S. et al. (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature, 417, 959 962.
62. Stuurman, J. Kuhlemeier, C. (2005) Stable two-element control of dTph1 transposition in mutator strains of Petunia by an inactive ACT1 introgression from a wild species. Plant J. 41, 945 955.
63. Stuurman, J., Hoballah, M.E., Broger, L., Moore, J., Basten, C. Kuhlemeier, C. (2004) Dissection of floral pollination syndromes in Petunia. Genetics, 168, 1585 1599.
64. Takahashi, M., Terada, Y., Nakai, I., Nakanishi, H., Yoshimura, E., Mori, S. Nishizawa, N.K. (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell, 15, 1263 1280.
65. Tisserant, B., Gianinazzi-Pearson, V., Gianinazzi, S. Gollotte, A. (1993) In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol. Res. 97, 245 250.
66. Ulian, E.C., Magill, J.M. Smith, R.H. (1994) Expression and inheritance pattern of two foreign genes in Petunia. Theor. Appl. Genet. 88, 433 440.
67. Vandenbussche, M., Theissen, G., Van de Peer, Y. Gerats, T. (2003) Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res. 31, 4401 4409.
68. Vieweg, M.F., Fruhling, M., Quandt, H.J., Heim, U., Baumlein, H., Puhler, A., Kuster, H. Andreas, M.P. (2004) The promoter of the Vicia faba L. leghemoglobin gene VfLb29 is specifically activated in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots from different legume and nonlegume plants. Mol. Plant-Microbe Interact. 17, 62 69.
69. Xie, M., He, Y. Gan, S. (2001) Bidirectionalization of polar promoters in plants. Nat. Biotechnol. 19, 677 679.
70. Xiong, L., David, L., Stevenson, B. Zhu, J.K. (1999) High throughput screening of signal transduction mutants with luciferase imaging. Plant Mol. Biol. Rep. 17, 159 170.
71. Xu, G., Chague, V., Melamed-Bessudo, C., Kapulnik, Y., Jain, A., Raghothama, K.G., Levy, A.A. Silber, A. (2007) Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. J. Exp. Bot. 58, 2491 2501.