Skip to main content
Springer Nature Link
Log in

Molecular and cell biology of arbuscular mycorrhizal symbiosis

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

See More

The roots of most extant plants are able to become engaged in an interaction with a small group of fungi of the fungal order Glomales (Glomeromycota). This interaction—arbuscular mycorrhizal (AM) symbiosis—is the evolutionary precursor of most other mutualistic root-microbe associations. The molecular analysis of this interaction can elucidate basic principles regarding such associations. This review summarizes our present knowledge about cellular and molecular aspects of AM. Emphasis is placed on morphological changes in colonized cells, transfer of nutrients between both interacting partners, and plant defence responses. Similarities to and differences from other associations of plant and microorganisms are highlighted regarding defence reactions and signal perception.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

AM:

Arbuscular mycorrhiza(l)

CCaMK:

Calcium and calmodulin-dependent protein kinase

DMI :

DOES NOT MAKE INFECTIONS

ER:

Endoplasmatic reticulum

EST:

Expressed sequence tag

GFP:

Green fluorescent protein

NORK:

Nodulation receptor kinase

NFR:

Nod factor receptor

SYM:

Mutants affected in symbioses

SYMRK:

Symbiosis receptor-like kinase

References

  • Ané J-M, Lévy J, Thoquet P, Kulikova O, de Billy F, Penmetsa V, Kim DJ, Debelle F, Rosenberg C, Cook DR, Bisseling T, Huguet T, Denarie J (2002) Genetic and cytogenetic mapping of DMI1, DMI2, and DMI3 genes of Medicago truncatula involved in Nod factor transduction, nodulation, and mycorrhization. Mol Plant Microbe Interact 15:1108–1118

    PubMed  Google Scholar 

  • Ané J-M, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Lévy J, Debellé F, Baek J-M, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    Article  PubMed  Google Scholar 

  • Arines J, Palma JM, Vilarino A (1993) Comparison of protein patterns in non-mycorrhizal and vesicular-arbuscular mycorrhizal roots of red clover. New Phytol 123:736–768

    Google Scholar 

  • Arines J, Quintela M, Vilarino A, Palma JM (1994a) Protein patterns and superoxide dismutase activity in non-mycorrhizal and arbuscular-mycorrhizal Pisum sativum L. plants. Plant Soil 166:37–45

    CAS  Google Scholar 

  • Arines J, Vilarino A, Palma JM (1994b) Involvement of the superoxide dismutase enzyme in the mycorrhization process. Agric Sci Finl 3:303–306

    CAS  Google Scholar 

  • Asamizu E, Nakamura Y, Sato S, Tabata S (2000) Generation of 7137 non-redundant expressed sequence tags from a legume, Lotus japonicus. DNA Res 7:127–130

    PubMed  Google Scholar 

  • Augé R (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Google Scholar 

  • Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:108–124

    Article  CAS  PubMed  Google Scholar 

  • Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y (2003) Carbon eport from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol 131:1496–1507

    Article  CAS  PubMed  Google Scholar 

  • Balestrini R, Romera C, Puigdomenech P, Bonfante P (1994). Location of a cell wall hydroxyproline-rich glycoprotein, cellulose and β–1,3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195:201–209

    Article  CAS  Google Scholar 

  • Barker SJ, Stummer B, Gao L, Dispain I, O’Connor P, Smith SE (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonisation. Isolation and preliminary characterisation. Plant J 15:791–797

    Article  CAS  Google Scholar 

  • Bell CJ, Dixon RA, Farmer AD, Flores R, Inman J, Gonzales RA, Harrison MJ, Paiva NL, Scott AD, Weller JW, May GD (2001) The medicago genome initiative: a model legume database. Nucleic Acids Res 29:114–117

    Article  CAS  PubMed  Google Scholar 

  • Benabdellah K, Azcon-Aguilar C, Ferrol N (1998) Soluble and membrane symbiosis-related polypeptides associated with the development of arbuscular mycorrhizas in tomato (Lycopersicon esculentum). New Phytol 140:135–143

    Article  CAS  Google Scholar 

  • Benabdellah K, Azcon-Aguilar C, Ferrol N (2000) Alterations in the plasma membrane polypeptide pattern of tomato roots (Lycopersicon esculentum) during the development of arbuscular mycorrhiza. J Exp Bot 51:747–754

    Article  CAS  PubMed  Google Scholar 

  • Bestel-Corre G, Gianinazzi S, Dumas-Gaudot E (2004) Impact of sewage sludges on Medicago truncatula symbiotic proteome. Phytochemistry 65:1651–1659

    Article  CAS  PubMed  Google Scholar 

  • Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Dominguez L, Sersic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:345–346

    Article  PubMed  Google Scholar 

  • Blancaflor E, Zhao L, Harrison M (2001) Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplasma 217:154–165

    CAS  PubMed  Google Scholar 

  • Blee KA, Anderson AJ (1996) Defense-related transcript accumulation in Phaseolus vulgaris L. colonized by the arbuscular mycorrhizal fungus Glomus intraradices Schenk and Smith. Plant Physiol 110:675–699

    CAS  PubMed  Google Scholar 

  • Blilou I, Bueno P, Ocampo JA, García-Garrido JM (2000) Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal fungus Glomus mosseae. Mycol Res 104:722–725

    Article  CAS  Google Scholar 

  • Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant-Microbe Interact 14:695–700

    CAS  PubMed  Google Scholar 

  • Boller T (1987) Hydrolytic enzymes in plant disease resistance. In: Kosuge T, Nester EW (eds) Plant-microbe interactions, vol 2. Macmillan, New York, pp 385–413

  • Bonanomi A, Wiemken A, Boller T, Salzer P (2001) Local induction of a mycorrhiza-specific class III chitinase gene in cortical root cells of Medicago truncatula containing developing or mature arbuscules. Plant Biol 3:194–200

    Article  CAS  Google Scholar 

  • Bonfante P, Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol 130:3–21

    Google Scholar 

  • Bonfante P, Bergero R, Uribe X, Romera C, Rigau J, Puigdomenech P (1996) Transcriptional activation of a maize α–tubulin gene in mycorrhizal maize and transgenic tobacco plants. Plant J 9:737–743

    Article  CAS  Google Scholar 

  • Bradbury SM, Peterson RL, Bowley SR (1991) Interactions between three alfalfa nodulation genotypes and two Glomus species. New Phytol 119:115–120

    Google Scholar 

  • Burleigh SH, Harrison MJ (1997) A novel gene whose expression in Medicago truncatula is suppressed in response to colonization by vesicular-arbuscular mycorrhizal fungi and to phosphate nutrition. Plant Mol Biol 34:199–208

    Article  CAS  PubMed  Google Scholar 

  • Buuren ML van , Maldonado-Mendoza IE, Trieu AT, Blaylock LA, Harrison MJ (1999) Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis formed between Medicago truncatula and Glomus versiforme. Mol Plant-Microbe Interact 12:171–181

    PubMed  Google Scholar 

  • Calantzis C, Morandi D, Gianinazzi-Pearson V (1998) Cellular interactions between G. mosseae and a myc− 1nod− mutant in Medicago truncatula. In: Ahonen-Jonnarth U, Danell E, Fransson P, Karen O, Lindahl B, Rangel I, Finlay R (eds) Abstract 2nd international Conference on Mycorrhizae. SLU Service/Repro, Uppsala, 1998, pp 38

  • Carling DE, Brown MF (1982) Anatomy and physiology of vesicular-arbuscular and nonmycorrhizal roots. Phytopathology 72:1108–1114

    Google Scholar 

  • Catoira R, Galera C, Billy Fd, Penmetsa R, Journet E-P, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12:1647–1665

    Article  CAS  PubMed  Google Scholar 

  • Chabaud M, Larsonneau C, Marmouget C, Huguet T (1996) Transformation of barrel medic (Medicago truncatula Gaertn.) by Agrobacterium tumefaciens and regeneration via somatic embryogenesis of transgenic plants with the MtENOD12 nodulin promoter fused to the gus reporter gene. Plant Cell Rep 15:305–310

    Article  CAS  Google Scholar 

  • Chabaud M, Venard C, Defaux-Petras A, Becard G, Barker DG (2002) Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol 156:265–273

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cordier C, Pozo M, Barea J, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant-Microbe Interact 11:1017–1028

    CAS  Google Scholar 

  • Dassi B, Samra A, Dumas-Gaudot E, Gianinazzi S (1999) Different polypeptide profiles from tomato roots following interactions with arbuscular mycorrhizal (Glomus mosseae) or pathogenic (Phytophthora parasitica) fungi. Symbiosis 26:65–77

    CAS  Google Scholar 

  • David R, Itzhaki H, Ginzberg I, Gafni Y, Galili G, Kapulnik Y (1998) Suppression of tobacco basic chitinase gene expression in response to colonization by the arbuscular mycorrhizal fungus Glomus intraradices. Mol Plant-Microbe Interact 11:489–497

    CAS  PubMed  Google Scholar 

  • David-Schwartz R, Badani H, Smadar W, Levy AA, 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

    Article  CAS  PubMed  Google Scholar 

  • David-Schwartz R, Gadkar V, Wininger S, Bendov R, Galili G, Levy AA, 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

    CAS  PubMed  Google Scholar 

  • Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowski K (2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytol 163:381–392

    Article  CAS  Google Scholar 

  • Douds DD, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 107–129

    Google Scholar 

  • Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal mutants (myc−) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci 60:215–222

    Article  Google Scholar 

  • Dumas-Gaudot E, Guillaume P, Tahiri-Alaoui A, Gianinazzi-Pearson V, Gianinazzi S (1994) Changes in polypeptide patterns in tobacco roots colonised by Glomus species. Mycorrhiza 4:215–221

    Article  CAS  Google Scholar 

  • Dumas-Gaudot E, Gollotte A, Cordier C, Gianinazzi S, Gianinazzi-Pearson V (2000) Modulation of host defence systems. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 173–200

    Google Scholar 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    Article  CAS  PubMed  Google Scholar 

  • Ferrol N, Barea JM, Azcon-Aguilar C (2000) The plasma membrane H+-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr Genet 37:112–118

    Article  CAS  PubMed  Google Scholar 

  • Fester T, Strack D, Hause B (2001) Reorganization of tobacco root plastids during arbuscule development. Planta 213:864–868

    CAS  PubMed  Google Scholar 

  • Fester T, Kiess M, Strack D (2002) A mycorrhiza-responsive protein in wheat roots. Mycorrhiza 12:219–222

    Article  CAS  PubMed  Google Scholar 

  • Franken P, Requena N (2001) Molecular approaches to arbuscular mycorrhiza functioning. The mycota IX: fungal associations, Springer, Berlin Heidelberg New York

    Google Scholar 

  • Frühling M, Roussel H, Gianinazzi-Pearson V, Puhler A, Perlick AM (1997) The Vicia faba leghemoglobin gene VfLb29 is induced in root nodules and in roots colonized by the arbuscular mycorrhizal fungus Glomus fasciculatum. Mol Plant-Microbe Interact 10:124–131

    PubMed  Google Scholar 

  • García-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386

    Article  PubMed  Google Scholar 

  • García-Garrido JM, Toro N, Ocampo JA (1993) Presence of specific polypeptides in onion roots colonized by Glomus mosseae. Mycorrhiza 2:175–177

    Google Scholar 

  • Genre A, Bonfante P (1997) A mycorrhizal fungus changes microtubule orientation in tobacco root cells. Protoplasma 199:30–38

    Google Scholar 

  • Genre A, Bonfante P (1998) Actin versus tubulin configuration in arbuscule-containing cells from mycorrhizal tobacco roots. New Phytol 140:745–752

    Article  CAS  Google Scholar 

  • Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871–1883

    Article  PubMed  Google Scholar 

  • Gianinazzi-Pearson V, Smith SE, Gianinazzi S, Smith FA (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? New Phytol 117:61–76

    CAS  Google Scholar 

  • Gianinazzi-Pearson V, Tahiri-Alaoui A, Antoniw JF, Gianinazzi S, Dumas E (1992) Weak expression of the pathogenesis related PR-b1 gene and localization of related protein during symbiotic endomycorrhizal interactions in tobacco roots. Endocyt Cell Res 8:177–185

    Google Scholar 

  • Gianinazzi-Pearson V, Dumas-Gaudot E, Gollotte A, Tahiri-Alaoui A, Gianinazzi S (1996) Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol 133:45–57

    Google Scholar 

  • Gianinazzi-Pearson V, Arnould C, Oufattole M, Arango M, Gianinazzi S (2000) Differential activation of H+ -ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211:609–613

    Article  CAS  PubMed  Google Scholar 

  • Gollotte A, Gianinazzi-Pearson V, Giovannetti M, Sbrana C, Avio L, Gianinazzi S (1993) Cellular localization and cytochemical probing of resistance reactions to arbuscular mycorrhizal fungi in a ‘locus a’ mutant of Pisum sativum (L.). Planta 191:112–122

    Article  CAS  Google Scholar 

  • Guenoune D, Galili S, Phillips D, Volpin H, Chet I, Okon Y, Kapulnik Y (2001) The defense response elicited by the pathogen Rhizoctonia solani is suppressed by colonization of the AM-fungus Glomus intraradices. Plant Sci 160:925–932

    Article  CAS  PubMed  Google Scholar 

  • Guttenberger M (2000) Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211:299–304

    Article  CAS  PubMed  Google Scholar 

  • Hans J, Hause B, Strack D, Walter MH (2004) Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-D-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol 134:614–624

    Article  CAS  PubMed  Google Scholar 

  • Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J 9:491–503

    Article  CAS  PubMed  Google Scholar 

  • Harrison M (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50:361–389

    Article  CAS  PubMed  Google Scholar 

  • Harrison M, Dixon R (1994) Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. Plant J 6:9–20

    Article  CAS  Google Scholar 

  • Harrison MJ, Van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629

    Article  CAS  PubMed  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    Article  CAS  PubMed  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  CAS  PubMed  Google Scholar 

  • Hayashi M, Miyahara A, Sato S, Kato T, Yoshikawa M, Taketa M, Hayashi M, Pedrosa A, Onda R, Imaizumi-Anraku H, Bachmair A, Sandal N, Stougaard J, Murooka Y, Tabata S, Kawasaki S, Kawaguchi M, Harada K (2001) Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F2 population. DNA Res 8:301–310

    CAS  PubMed  Google Scholar 

  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    PubMed  Google Scholar 

  • Hildebrandt U, Schmelzer E, Bothe H (2002) Expression of nitrate transporter genes in tomato colonized by an arbuscular mycorrhizal fungus. Physiol Plant 115:125–136

    Article  CAS  PubMed  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299

    Article  CAS  PubMed  Google Scholar 

  • Hohnjec N, Perlick AM, Puhler A, Kuster H (2003) The Medicago truncatula sucrose synthase gene MtSucS1 is activated both in the infected region of root nodules and in the cortex of roots colonized by arbuscular mycorrhizal fungi. Mol Plant-Microbe Interact 16:903–915

    CAS  PubMed  Google Scholar 

  • Imhof S (1999) Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jacq.) Pers. (Gentianaceae). Mycorrhiza 9:33–39

    Article  Google Scholar 

  • Jacobi LM, Petrova OS, Tsyganov VE, Borisov AY, Tikhonovich IA (2003a) Effect of mutations in the pea genes Sym33 and Sym40. I. Arbuscular mycorrhiza formation and function. Mycorrhiza 13:3–7

    CAS  PubMed  Google Scholar 

  • Jacobi LM, Zubkova LA, Barmicheva EM, Tsyganov VE, Borisov AY, Tikhonovich IA (2003b) Effect of mutations in the pea genes Sym33 and Sym40. II. Dynamics of arbuscule development and turnover. Mycorrhiza 13:9–16

    CAS  PubMed  Google Scholar 

  • Jacquelinet-Jeanmougin J, Gianinazzi-Pearson V, Gianinazzi S (1987) Endomycorrhizas in the Gentianaceae. II. Ultrastructural aspects of symbiont relationships in Gentiana lutea L. Symbiosis 3:269–286

    Google Scholar 

  • Journet EP, van Tuinen D, Gouzy J, Crespeau H, Carreau V, Farmer MJ, Niebel A, Schiex T, Jaillon O, Chatagnier O, Godiard L, Micheli F, Kahn D, Gianinazzi-Pearson V, Gamas P (2002) Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res 30:5579–5592

    Article  PubMed  Google Scholar 

  • Kaldorf M, Schmelzer E, Bothe H (1998) Expression of maize and fungal nitrate reductase genes in arbuscular mycorrhiza. Mol Plant Microbe Interact 11:439–448

    CAS  PubMed  Google Scholar 

  • Kato T, Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S (2003) Structural analysis of a Lotus japonicus genome. V. Sequence features and mapping of sixty-four TAC clones which cover the 6.4 Mb regions of the genome. DNA Res 10:277–285

    Google Scholar 

  • Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518

    Article  CAS  PubMed  Google Scholar 

  • Kjoller R, Rosendahl S (1996) The presence of the arbuscular mycorrhizal fungus Glomus intraradices influences enzymatic activities of the root pathogen Aphanomyces euteiches in pea roots. Mycorrhiza 6:487–491

    Google Scholar 

  • Kling M, Gianinazzi-Pearson V, Lherminier J, Jakobsen I (1996) The development and functioning of mycorrhizas in pea mutants. In: First International Conference on Mycorrhizae, Program and abstracts, Berkeley, CA, USA, p 71

  • Köhler R, Hanson M (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J Cell Sci 113:81–89

    PubMed  Google Scholar 

  • Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker D, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962

    Article  CAS  PubMed  Google Scholar 

  • Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211:85–90

    Article  CAS  PubMed  Google Scholar 

  • Krajinski F, Hause B, Gianinazzi-Pearson V, Franken P (2002) Mtha1, a plasma membrane H+ -ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol 4:754–761

    Article  CAS  Google Scholar 

  • Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748

    Article  CAS  PubMed  Google Scholar 

  • Kulikova O, Gualtieri G, Geurts R, Kim DJ, Cook D, Huguet T, de Jong JH, Fransz PF, Bisseling T (2001) Integration of the FISH pachytene and genetic maps of Medicago truncatula. Plant J 27:49–58

    Article  CAS  PubMed  Google Scholar 

  • Lambais MR (2000) Regulation of plant defence-related genes in arbuscular mycorrhizae. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. American Phytopathological Society, Minnesota, pp 45–59

    Google Scholar 

  • Lambais MR, Mehdy MC (1993) Suppression of endochitinases, β-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhiza under different soil phosphate conditions. Mol Plant-Microbe Interact 6:75–83

    CAS  Google Scholar 

  • Lambais MR, Mehdy MC (1998) Spatial distribution of chitinases and β-1,3-glucanase transcripts in bean arbuscular mycorrhizal roots under low and high soil phosphate conditions. New Phytol 140:33–42

    Article  CAS  Google Scholar 

  • Lamblin AF, Crow JA, Johnson JE, Silverstein KA, Kunau TM, Kilian A, Benz D, Stromvik M, EndrŽ G, VandenBosch KA, Cook DR, Young ND, Retzel EF (2003) MtDB: a database for personalized data mining of the model legume Medicago truncatula transcriptome. Nucleic Acids Res 31:196–201

    Article  CAS  PubMed  Google Scholar 

  • Leake JR (1994) The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol 127:171–216

    Google Scholar 

  • Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet E-P, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    Article  PubMed  Google Scholar 

  • Linderman RG (2000) Effects of mycorrhizas on plant tolerances to diseases. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 345–365

    Google Scholar 

  • Liu J, Blaylock LA, Endre G, Choc J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123

    Article  CAS  PubMed  Google Scholar 

  • Long SR (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885–1898

    Article  CAS  PubMed  Google Scholar 

  • Madsen E, Madsen L, Radutoiu S, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640

    Article  CAS  PubMed  Google Scholar 

  • Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant Microbe Interact 14:1140–1148

    CAS  PubMed  Google Scholar 

  • Martin-Laurent F, Van Tuinen D, Dumas-Gaudot E, Gianinazzi-Pearson V, Gianinazzi S, Franken P (1997) Differential display analysis of RNA accumulation in arbuscular mycorrhiza of pea and isolation of a novel symbiosis-regulated plant gene. Mol Gen Genet 256:37–44

    Article  CAS  PubMed  Google Scholar 

  • Marx C, Dexheimer J, Gianinazzi-Pearson V, 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. New Phytol 90:37–43

    CAS  Google Scholar 

  • Matsubara Y, Uetake Y, Peterson RL (1999) Entry and colonization of Asparagus offizinalis roots by arbuscular mycorrhizal fungi with emphasis on changes in host microtubules. Can J Bot 77:1159–1167

    Article  Google Scholar 

  • Meyer J, Dehne H-W (1986) The influence of VA mycorrhizae on biotrophic leaf pathogens. In: Physiological and genetical aspects of mycorrhizae. Proceedings of the First European Symposium on Mycorrhizae, Dijon, pp 781–786

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GED, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705

    Article  CAS  PubMed  Google Scholar 

  • Morandi D, Bailey JA, Gianinazzi-Pearson V (1984) Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol Plant Pathol 24:357–364

    CAS  Google Scholar 

  • Morandi D, Sagan M, Prado-Vivant E, Duc G (2000) Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants. Mycorrhiza 10:37–42

    Article  CAS  Google Scholar 

  • Murphy PJ, Langridge P, Smith SE (1997) Cloning plant genes differentially expressed during colonisation of Hordeum vulgare L. by the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 135:291–301

    Article  CAS  Google Scholar 

  • Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7:869–885

    Article  CAS  PubMed  Google Scholar 

  • Park KS, Moyne AL, Tuzun S, Kim CH, Kloepper JW (1997) Induction of PR-1 promoter in a transgenic reporter system by selected PGPR strains which induce resistance. In: Ogoshi A, Kobayashi K, Homma Y, Kodama F, Kondo N, Akino S (eds) Plant growth promoting bacteria: present strains and future prospects. Nakanishi Printing, Sapporo, pp 251–255

    Google Scholar 

  • Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421

    Article  CAS  PubMed  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13,324–13,329

    Google Scholar 

  • Pawlowska TE, Taylor JW (2004) Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427:733–737

    Article  CAS  PubMed  Google Scholar 

  • Peipp H, Maier W, Schmidt J, Wray V, Strack D (1997) Arbuscular mycorrhizal fungus-induced changes in the accumulation of secondary compounds in barley roots. Phytochemistry 44:581–587

    Article  CAS  Google Scholar 

  • Peretto R, Bettini V, Favaron F, Alghisi P, Bonfante P (1995) Polygalacturonase activity and location in arbuscular mycorrhizal roots of Allium porrum L. Mycorrhiza 5:157–163

    Article  CAS  Google Scholar 

  • Perotto S, Brewin NJ, Bonfante P (1994) Colonization of pea roots by the mycorrhizal fungus Glomus versiforme and Rhizobium bacteria: Immunological comparison using monoclonal antibodies as probes for plant cell surface components. Mol Plant-Microbe Interact 7:91–98

    Google Scholar 

  • Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201

    Google Scholar 

  • Perry JA, Wang TL, Welham TJ, Gardner S, Pike JM, Yoshida S, Parniske M (2003) A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiol 131:866–871

    Article  CAS  PubMed  Google Scholar 

  • Peterson RL, Bonfante P (1994) Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. Plant Soil 159:79–88

    Google Scholar 

  • Peterson RL, Guinel FC (2000) The use of plant mutants to study regulation of colonization by AM fungi. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 147–171

    Google Scholar 

  • Pozo M, Azcón-Aguilar C, Dumas-Gaudot E, Barea J (1999) β-1,3-glucanase in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci 141: 149–157

    Article  CAS  Google Scholar 

  • Pozo M, Cordier C, Dumas-Gautod E, Gianinazzi S, Barea J, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534

    Article  CAS  PubMed  Google Scholar 

  • Radutoiu S, Madsen L, Madsen E, Felle H, Umehara Y, Gronlund M, Sato S, Nakamura Y, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592

    Article  CAS  PubMed  Google Scholar 

  • Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37

    Article  CAS  PubMed  Google Scholar 

  • 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 414:462–466

    Article  CAS  PubMed  Google Scholar 

  • Ravnskov S, Wu Y, Graham JH (2003) Arbuscular mycorrhizal fungi differentially affect expression of genes coding for sucrose synthases in maize roots. New Phytol 157:539–545

    Article  CAS  Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921

    Article  CAS  PubMed  Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843

    CAS  PubMed  Google Scholar 

  • Repetto O, Bestel-Corre G, Dumas-Gaudot E, Berta G, Gianinazzi-Pearson V, Gianinazzi S (2003) Targeted proteomics to identify cadmium-induced protein modifications in Glomus mosseae-inoculated pea roots. New Phytol 157:555–567

    Article  CAS  Google Scholar 

  • Requena N, Breuninger M, Franken P, Ocon A (2003) Symbiotic status, phosphate, and sucrose regulate the expression of two plasma membrane H+ -ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiol 132:1540–1549

    Article  CAS  PubMed  Google Scholar 

  • van Rhijn P, Fang Y, Galili S, Shaul O, Atzmon N, Wininger S, Eshed Y, Lum M, Li Y, To V, Fujishige N, Kapulnik Y, Hirsch AM (1997) Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved. Proc Natl Acad Sci USA 94:5467–5472

    Article  PubMed  Google Scholar 

  • Rhody D, Stommel M, Roeder C, Mann P, Franken P (2003) Differential RNA accumulation of two beta-tubulin genes in arbuscular mycorrhizal fungi. Mycorrhiza 13:137–142

    Article  CAS  PubMed  Google Scholar 

  • Salzer P, Corbière H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208:319–325

    Article  CAS  Google Scholar 

  • Salzer P, Bonanomi A, Beyer K, Vögeli-Lange R, Aeschbacher R, Lange J, Wiemken A, Kim D, Cook D, Boller T (2000) Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. Mol Plant-Microbe Interact 13:763–777

    CAS  PubMed  Google Scholar 

  • Samra A, Dumas-Gaudot E, Gianinazzi S (1997) Detection of symbiosis-related polypeptides during the early stages of the establishment of arbuscular mycorrhiza between Glomus mosseae and Pisum sativum roots. New Phytol 135:711–722

    Article  CAS  Google Scholar 

  • Sanders FE, Tinker BP, Black RLB, Palmerly SM (1977) The development of endomycorrhizal root systems. I. Speed of infection and growth-promoting effects with four species of vesicular–arbuscular endophyte. New Phytol 78:257–268

    Google Scholar 

  • Schellenbaum L, Gianinazzi S, Gianinazzi-Pearson V (1992) Comparison of acid soluble protein synthesis in roots of endomycorrhizal wild type Pisum sativum and corresponding isogenic mutants. J Plant Physiol 141:2–6

    Google Scholar 

  • Schüßler A (2001) Molecular phylogeny, taxonomy, and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi. Plant Soil 244:75–83

    Article  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Google Scholar 

  • Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves. Mol Plant-Microbe Interact 12:1000–1007

    CAS  PubMed  Google Scholar 

  • Simon L, Bousquet J, Lévesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69

    Article  Google Scholar 

  • Simoneau P, Louisy-Louis N, Plenchette C, Strullu DG (1994) Accumulation of new polypeptides in Ri T-DNA-transformed roots of tomato (Lycopersicon esculentum) during the development of vesicular-arbuscular mycorrhizae. Appl Environ Microbiol 60:1810–1813

    CAS  Google Scholar 

  • Slezack S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol Plant-Microbe Interact 13:238–241

    CAS  PubMed  Google Scholar 

  • Slezack S, Negrel J, Bestel-Corre G, Dumas-Gaudot E, Gianinazzi S (2001) Purification and partial amino acid sequencing of a mycorrhiza-related chitinase isoform from Glomus mosseae-inoculated roots of Pisum sativum L. Planta 213:781–787

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  CAS  PubMed  Google Scholar 

  • Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962

    Article  CAS  PubMed  Google Scholar 

  • Tahiri-Alaoui A, Dumas-Gaudot E, Gioaninazzi S (1993) Immunocytochemical localisation of pathogenesis-related PR-1 proteins in tobacco root tissues infected in vitro by the black root rot fungus Chalara elegans. Physiol Mol Plant Pathol 42:69–82

    Article  CAS  Google Scholar 

  • Tamasloukht MB, Sejalon-Delmas N, Kluever A, Jauneau A, Roux C, Becard G, Franken P (2003) Root factors induce mitochondrial-related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol 131:1468–1478

    Article  CAS  PubMed  Google Scholar 

  • Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from early devonian. Mycologia 87:560–573

    Google Scholar 

  • Timonen S, Peterson RL (2002). Cytoskeleton in mycorrhizal symbiosis. Plant Soil 244:199–210

    Article  CAS  Google Scholar 

  • Trouvelot S, van Tuinen D, Hijri M, Gianinazzi-Pearson V (1999) Visualization of ribosomal DNA loci in spore interphasic nuclei of glomalean fungi by fluorescence in situ hybridization. Mycorrhiza 8:203–206

    Article  CAS  Google Scholar 

  • Uchiumi T, Shimoda Y, Tsuruta T, Mukoyoshi Y, Suzuki A, Senoo K, Sato S, Kato T, Tabata S, Higashi S, Abe M (2002) Expression of symbiotic and nonsymbiotic globin genes responding to microsymbionts on Lotus japonicus. Plant Cell Physiol 43:1351–1358

    Article  CAS  PubMed  Google Scholar 

  • Vierheilig H, Iseli B, Alt M, Raikhel N, Wiemken A, Boller T (1996). Resistance of Urtica dioica to mycorrhizal colonization: a possible involvement of Urtica dioica agglutinin. Plant Soil 183:131–136

    CAS  Google Scholar 

  • Volpin H, Elkind Y, Okon Y, Kapulnik Y (1994) A vesicular arbuscular mycorrhizal fungus Glomus intraradix induces a defence response in alfalfa roots. Plant Physiol 104:683–689

    CAS  PubMed  Google Scholar 

  • Walter M.H, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-D-xylulose-5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31:243–254

    Article  CAS  PubMed  Google Scholar 

  • Watson BS, Asirvatham VS, Wang L, Sumner LW (2003) Mapping the proteome of barrel medic (Medicago truncatula). Plant Physiol 131:1104–1123

    Article  PubMed  Google Scholar 

  • Wegel E, Schauser L, Sandal N, Stougaard J, Parniske M (1998) Mycorrhiza mutants of Lotus japonicus define genetically independent steps during symbiotic infection. Mol Plant-Microbe Interact 11:933–936

    CAS  Google Scholar 

  • Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Kuster H, Krajinski F (2003) Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol Plant-Microbe Interact 16:306–314

    CAS  PubMed  Google Scholar 

  • Wyss P, Mellor RB, Wiemken A (1990) Vesicular-arbuscular mycorrhizas of wild-type soybean and non-nodulating mutants with Glomus mosseae contain symbiosis-specific polypeptides (mycorrhizins), immunologically cross-reactive with nodulins. Planta 182:22–26

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Strack for critical reading of the manuscript and S. Schaarschmidt for help in preparing Fig. 3. We apologize to those colleagues whose work was not cited because of space limitations. Our work is supported by the Deutsche Forschungsgemeinschaft (DFG) within the Focus Program “Molecular Basics of Mycorrhizal Symbioses”.

Author information

Authors and Affiliations

  1. Department of Secondary Metabolism, Leibniz Institute of Plant Biochemistry, PB 110432, D-06018, Halle, Germany

    Bettina Hause & Thomas Fester

Authors
  1. Bettina Hause
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Thomas Fester
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Bettina Hause.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hause, B., Fester, T. Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221, 184–196 (2005). https://doi.org/10.1007/s00425-004-1436-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1436-x

Keywords