Plant Biol (Stuttg) 2002; 4(6): 754-761
DOI: 10.1055/s-2002-37407
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Mtha1, a Plasma Membrane H+-ATPase Gene from Medicago truncatula, Shows Arbuscule-Specific Induced Expression in Mycorrhizal Tissue

F. Krajinski 1,2 , B. Hause 3 , V. Gianinazzi-Pearson 4 , P. Franken 1,5
  • 1 Max-Planck-Institute for Terrestrial Microbiology, and Laboratory for Microbiology, Philipps-University, Karl-von-Frisch-Strasse, 35043 Marburg, Germany
  • 2 Present address: LG Molecular Genetics, University of Hannover, Herrenhäuser Strasse 2, 30419 Hannover, Germany
  • 3 Institute of Plant Biochemistry, Department of Secondary Metabolism, P.O. Box 110432, 06018 Halle, Germany
  • 4 UMR 1088 INRA/University of Burgundy, BBCE-IPM, INRA-CMSE, BP 86510, 21065 Dijon Cedex, France
  • 5 Institute for Vegetable and Ornamental Plants, Grossbeeren, Germany
Further Information

Publication History

Received: September 27, 2002

Accepted: December 11, 2002

Publication Date:
24 February 2003 (online)

Abstract

Transport processes between plant and fungal cells are key elements in arbuscular mycorrhiza (AM), where H+-ATPases are considered to be involved in active uptake of nutrients from the symbiotic interface. Genes encoding H+-ATPases were identified in the genome of Medicago truncatula and three cDNA fragments of the H+-ATPase gene family (Mtha1 - 3) were obtained by RT-PCR using RNA from M. truncatula mycorrhizal roots as template. While Mtha2 and Mtha3 appeared to be constitutively expressed in roots and unaffected by AM development, transcripts of Mtha1 could only be detected in AM tissues and not in controls. Further analyses by RT-PCR revealed that Mtha1 transcripts are not detectable in shoots and phosphate availability did not affect RNA accumulation of the gene. Localization of transcripts by in situ hybridization on AM tissues showed that Mtha1 RNA accumulates only in cells containing fungal arbuscules. This is the first report of arbuscule-specific induced expression of a plant H+-ATPase gene in mycorrhizal tissues.

References

  • 01 Bauer,  D.,, Müller,  H.,, Reich,  J.,, Riedel,  H.,, Ahrenkiel,  V.,, Warthoe,  P.,, and Strauss,  M.. (1993);  Identification of differentially expressed mRNA species by an improved display technique (DDRT-PCR).  Nucleic Acids Research. 21 4272-4280
  • 02 Boisson-Dernier,  A.,, Chabaud,  M.,, Garcia,  F.,, Becard,  G.,, Rosenberg,  C.,, and Barker,  D. G.. (2001);  Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations.  Molecular Plant-Microbe Interactions. 14 695-700
  • 03 Dellaporta,  S. L.,, Wood,  J.,, and Hicks,  J. B.. (1983);  Maize DNA minipreps.  Maize Genetics Cooperation News Letters. 57 26
  • 04 Dumas-Gaudot,  E.,, Guillaume,  P.,, Tahiri-Alaoui,  A.,, Gianinazzi-Pearson,  V.,, and Gianinazzi,  S.. (1994);  Changes in polypeptide patterns in tobacco roots colonized by two Glomus species.  Mycorrhiza. 4 215-221
  • 05 Ewing,  N. N., and Bennett,  A. B.. (1994);  Assessment of the number and expression of P-type H+-ATPase genes in tomato.  Plant Physiology. 106 547-557
  • 06 Ferrol,  N.,, Pozo,  M. J.,, Antelo,  M.,, and Azcon-Aguilar,  C.. (2002);  Arbuscular mycorrhizal symbiosis regulates plasma membrane H+-ATPase gene expression in tomato plants.  Journal of Experimental Botany. 53 1683-1687
  • 07 Franken,  P., and Gnädinger,  F.. (1994);  Analysis of parsley arbuscular endomycorrhiza: infection development and mRNA levels of defense-related genes.  Molecular Plant-Microbe Interactions. 7 612-620
  • 08 Garcia-Garrido,  J. M., and Ocampo,  J. A.. (2002);  Regulation of the plant defence response in arbuscular mycorrhizal symbiosis.  Journal of Experimental Botany. 53 1377-1386
  • 09 Gianinazzi-Pearson,  V.,, Arnould,  C.,, Oufattole,  M.,, Arango,  M.,, and Gianinazzi,  S.. (2000);  Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco.  Planta. 211 609-613
  • 10 Gianinazzi-Pearson,  V.,, Dumas-Gaudot,  E.,, Gollotte,  A.,, Tahhiri-Alaoui,  A.,, and Gianinazzi,  S.. (1996);  Cellular and molecular defence-related root response to invasion by arbuscular mycorrhizal fungi.  The New Phytologist. 133 45-57
  • 11 Gianinazzi-Pearson,  V.,, Smith,  S. E.,, Gianinazzi,  S.,, and Smith,  F. A.. (1991);  Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas V. Is H+-ATPase a component of ATP-hydrolysing enzyme activities in plant-fungus interfaces?.  The New Phytologist. 117 61-74
  • 12 Guttenberger,  M.. (2000);  Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots.  Planta. 211 299-304
  • 13 Harper,  J. F.,, Manney,  L.,, and Sussman,  M. R.. (1994);  The plasma membrane H+-ATPase gene family in Arabidopsis: genomic sequence of AHA10 which is expressed primarily in developing seeds.  Molecular and General Genetics. 244 572-587
  • 14 Harrison,  M. J.,, Dewbre,  G. R.,, and Liu,  J. Y.. (2002);  A phosphate transporter from Medicago truncatula involved in the acquisiton of phosphate released by arbuscular mycorrhizal fungi.  Plant Cell. 14 2413-2429
  • 15 Hewitt,  E. J.. (1966) Sand and water culture methods. Tech. Comm. 22 (2nd revised). London; Commonwealth Agricultural Bureau pp. 430-434
  • 16 Jakobsen,  I., and Rosendahl,  L.. (1990);  Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants.  The New Phytologist . 115 77-83
  • 17 Kalampanayil,  B. D., and Wimmers,  L. E.. (2001);  Identification and characterization of a salt-stress-induced plasma membrane H+-ATPase in tomato.  Plant Cell and Environment. 24 999-1005
  • 18 Marschner,  H., and Dell,  B.. (1994);  Nutrient uptake in mycorrhizal symbiosis.  Plant and Soil. 159 89-102
  • 19 Marx,  C.,, Dexheimer,  J.,, Gianinazzi-Pearson,  V.,, and Gianinazzi,  S.. (1982);  Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas IV. Ultracytoenzymological evidence (ATPase) for active transfer processes in the host-arbuscular interface.  The New Phytologist. 90 37-43
  • 20 Mito,  N.,, Wimmers,  L. E.,, and Bennett,  A. B.. (1996);  Sugar regulates mRNA abundance of H+-ATPase gene family members in tomato.  Plant Physiology. 112 1229-1236
  • 21 Moriau,  L.,, Michelet,  B.,, Bogaerts,  P.,, Lambert,  L.,, Michel,  A.,, Oufattole,  M.,, and Boutry,  M.. (1999);  Expression analysis of two gene subfamilies encoding the plasma membrane H+-ATPase in Nicotiana plumbaginifolia reveals the major transport functions of this enzyme.  The Plant Journal. 19 31-41
  • 22 Murphy,  P. J.,, Langride,  P.,, and Smith,  S. E.. (1997);  Cloning plant genes differentially expressed during colonization of roots of Hordeum vulgare by the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. .  The New Phytologist. 135 291-301
  • 23 Oufattole,  M.,, Arango,  M.,, and Boutry,  M.. (2000);  Identification and expression of three new Nicotiana plumbaginifolia genes which encode isoforms of a plasma-membrane H+-ATPase, and one of which is induced by mechanical stress.  Planta. 210 715-722
  • 24 Page,  R. D. M.. (1996);  TREEVIEW: An application to display phylogenetic trees on personal computers.  Computer Applications in Bioscience. 12 357-358
  • 25 Palmgren,  M. G.. (2001);  Plant plasma membrane H+-ATPases: Powerhouses for nutrient uptake.  Annual Reviews in Plant Physiology and Plant Molecular Biology. 52 817-845
  • 26 Paszkowski,  U.,, Kroken,  S.,, Roux,  C.,, and Briggs,  S. P.. (2002);  Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis.  Proceedings of the National Academy of Sciences of the USA. 99 13324-13329
  • 27 Perez,  C.,, Michelet,  B.,, Ferrant,  V.,, Bogaerts,  P.,, and Boutry,  M.. (1992);  Differential expression within a three-gene subfamily encoding a plasma membrane H+-ATPase in Nicotiana plumbaginifolia. .  Journal of Biological Chemistry. 267 1204-1211
  • 28 Rausch,  C.,, Daram,  P.,, Brunner,  S.,, Jansa,  J.,, Laloi,  M.,, Leggewie,  G.,, Amrhein,  N.,, and Bucher,  M.. (2001);  A phosphate transporter expressed in arbuscule-containing cells in potato.  Nature. 414 462-466
  • 29 Robson,  G. D.,, Prebble,  E.,, Rickers,  A.,, Hosking,  S.,, Denning,  D. W.,, Trinci,  A. P. J.,, and Robertson,  W.. (1996);  Polarized growth of fungal hyphae is defined by an alkaline pH gradient.  Fungal Genetics and Biology. 20 289-298
  • 30 Sambrook,  J.,, Fritsch,  E. F.,, and Maniatis,  T.. (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor; Cold Spring Harbor Press
  • 31 Schaller,  A., and Oecking,  C.. (1999);  Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants.  The Plant Cell. 11 263-272
  • 32 Smith,  S. E., and Read,  D. J.. (1997) Mycorrhizal symbiosis. London; Academic Press
  • 33 Smith,  S. E., and Smith,  F. A.. (1990);  Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport.  The New Phytologist. 114 1-38
  • 34 Strimmer,  K., and von Haeseler,  A.. (1996);  Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies.  Molecular Biology and Evolution. 13 964-969
  • 35 Thompson,  J. D.,, Higgins,  D. G.,, and Gibson,  T. J.. (1994);  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.  Nucleic Acids Research. 22 4673-4680
  • 36 Trouvelot,  A.,, Kough,  J. L.,, and Gianinazzi-Pearson,  V.. (1986) Mesure du taux de mycorhization VA d'un système radiculaire. Recherche des méthodes d'estimation ayant une signification fonctionnelle. The Mycorrhizae: Physiology and Genetics. Gianinazzi-Pearson, V. and Gianinazzi, S., eds. Paris; INRA Presse pp. 217-221
  • 37 Zhang,  J. S.,, Xie,  C.,, Li,  Z. Y.,, and Chen,  S. Y.. (1999);  Expression of the plasma membrane H+-ATPase gene in response to salt stress in a rice salt-tolerant mutant and its original variety.  Theoretical and Applied Genetics. 99 1006-1011

P. Franken

Institute for Vegetable and Ornamental Plants

Theodor-Echtermeyer-Weg 1
14979 Grossbeeren
Germany

Email: franken@igzev.de

Section Editor: J. Cullimore