Abstract
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 interactionβarbuscular mycorrhizal (AM) symbiosisβis 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.



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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
AnΓ© J-M, LΓ©vy 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 15:1108β1118
AnΓ© J-M, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, LΓ©vy J, DebellΓ© F, Baek J-M, Kalo P, Rosenberg C, Roe BA, Long SR, DΓ©nariΓ© J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364β1367
Arines J, Palma JM, Vilarino A (1993) Comparison of protein patterns in non-mycorrhizal and vesicular-arbuscular mycorrhizal roots of red clover. New Phytol 123:736β768
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 166:37β45
Arines J, Vilarino A, Palma JM (1994b) Involvement of the superoxide dismutase enzyme in the mycorrhization process. Agric Sci Finl 3:303β306
Asamizu E, Nakamura Y, Sato S, Tabata S (2000) Generation of 7137 non-redundant expressed sequence tags from a legume, Lotus japonicus. DNA Res 7:127β130
AugΓ© R (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3β42
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 128:108β124
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 131:1496β1507
Balestrini R, Romera C, Puigdomenech P, Bonfante P (1994). Location of a cell wall hydroxyproline-rich glycoprotein, cellulose and Ξ²β1,3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195:201β209
Barker SJ, Stummer B, Gao L, Dispain I, OβConnor P, Smith SE (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonisation. Isolation and preliminary characterisation. Plant J 15:791β797
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 29:114β117
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 140:135β143
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 51:747β754
Bestel-Corre G, Gianinazzi S, Dumas-Gaudot E (2004) Impact of sewage sludges on Medicago truncatula symbiotic proteome. Phytochemistry 65:1651β1659
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 419:345β346
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 217:154β165
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 110:675β699
Blilou I, Bueno P, Ocampo JA, GarcΓa-Garrido JM (2000) Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal fungus Glomus mosseae. Mycol Res 104:722β725
Boisson-Dernier A, Chabaud M, Garcia F, BΓ©card 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 14:695β700
Boller T (1987) Hydrolytic enzymes in plant disease resistance. In: Kosuge T, Nester EW (eds) Plant-microbe interactions, vol 2. Macmillan, New York, pp 385β413
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 3:194β200
Bonfante P, Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol 130:3β21
Bonfante P, Bergero R, Uribe X, Romera C, Rigau J, Puigdomenech P (1996) Transcriptional activation of a maize Ξ±βtubulin gene in mycorrhizal maize and transgenic tobacco plants. Plant J 9:737β743
Bradbury SM, Peterson RL, Bowley SR (1991) Interactions between three alfalfa nodulation genotypes and two Glomus species. New Phytol 119:115β120
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 34:199β208
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 12:171β181
Calantzis C, Morandi D, Gianinazzi-Pearson V (1998) Cellular interactions between G. mosseae and a mycβ 1nodβ 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 72:1108β1114
Catoira R, Galera C, Billy Fd, Penmetsa R, Journet E-P, Maillet F, Rosenberg C, Cook D, Gough C, DΓ©nariΓ© J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12:1647β1665
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 15:305β310
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 156:265β273
Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3:31β40
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 11:1017β1028
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 26:65β77
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 11:489β497
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 27:561β569
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 16:382β388
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 163:381β392
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 107β129
Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal mutants (mycβ) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci 60:215β222
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 4:215β221
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 173β200
Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962β966
Ferrol N, Barea JM, Azcon-Aguilar C (2000) The plasma membrane H+-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr Genet 37:112β118
Fester T, Strack D, Hause B (2001) Reorganization of tobacco root plastids during arbuscule development. Planta 213:864β868
Fester T, Kiess M, Strack D (2002) A mycorrhiza-responsive protein in wheat roots. Mycorrhiza 12:219β222
Franken P, Requena N (2001) Molecular approaches to arbuscular mycorrhiza functioning. The mycota IX: fungal associations, Springer, Berlin Heidelberg New York
FrΓΌhling 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 10:124β131
GarcΓa-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377β1386
GarcΓa-Garrido JM, Toro N, Ocampo JA (1993) Presence of specific polypeptides in onion roots colonized by Glomus mosseae. Mycorrhiza 2:175β177
Genre A, Bonfante P (1997) A mycorrhizal fungus changes microtubule orientation in tobacco root cells. Protoplasma 199:30β38
Genre A, Bonfante P (1998) Actin versus tubulin configuration in arbuscule-containing cells from mycorrhizal tobacco roots. New Phytol 140:745β752
Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871β1883
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 plantβfungus interfaces? New Phytol 117:61β76
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 8:177β185
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 133:45β57
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 211:609β613
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 βlocus aβ mutant of Pisum sativum (L.). Planta 191:112β122
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 160:925β932
Guttenberger M (2000) Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211:299β304
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 134:614β624
Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J 9:491β503
Harrison M (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50:361β389
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 6:9β20
Harrison MJ, Van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626β629
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 14:2413β2429
Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213β1220
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 8:301β310
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 293:1129β1133
Hildebrandt U, Schmelzer E, Bothe H (2002) Expression of nitrate transporter genes in tomato colonized by an arbuscular mycorrhizal fungus. Physiol Plant 115:125β136
Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297β299
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 16:903β915
Imhof S (1999) Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jacq.) Pers. (Gentianaceae). Mycorrhiza 9:33β39
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 13:3β7
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 13:9β16
Jacquelinet-Jeanmougin J, Gianinazzi-Pearson V, Gianinazzi S (1987) Endomycorrhizas in the Gentianaceae. II. Ultrastructural aspects of symbiont relationships in Gentiana lutea L. Symbiosis 3:269β286
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 30:5579β5592
Kaldorf M, Schmelzer E, Bothe H (1998) Expression of maize and fungal nitrate reductase genes in arbuscular mycorrhiza. Mol Plant Microbe Interact 11:439β448
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 10:277β285
Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511β518
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 6:487β491
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
KΓΆhler R, Hanson M (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J Cell Sci 113:81β89
Kosuta S, Chabaud M, Lougnon G, Gough C, DΓ©nariΓ© J, Barker D, BΓ©card G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952β962
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 211:85β90
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 4:754β761
Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745β748
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 27:49β58
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 45β59
Lambais MR, Mehdy MC (1993) Suppression of endochitinases, Ξ²-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhiza under different soil phosphate conditions. Mol Plant-Microbe Interact 6:75β83
Lambais MR, Mehdy MC (1998) Spatial distribution of chitinases and Ξ²-1,3-glucanase transcripts in bean arbuscular mycorrhizal roots under low and high soil phosphate conditions. New Phytol 140:33β42
Lamblin AF, Crow JA, Johnson JE, Silverstein KA, Kunau TM, Kilian A, Benz D, Stromvik M, EndrΕ½ 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 31:196β201
Leake JR (1994) The biology of myco-heterotrophic (βsaprophyticβ) plants. New Phytol 127:171β216
LΓ©vy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet E-P, Rosenberg C, DebellΓ© F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361β1364
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 345β365
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 15:2106β2123
Long SR (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885β1898
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 425:637β640
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 14:1140β1148
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 256:37β44
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 90:37β43
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 77:1159β1167
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 781β786
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 101:4701β4705
Morandi D, Bailey JA, Gianinazzi-Pearson V (1984) Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol Plant Pathol 24:357β364
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 10:37β42
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 135:291β301
Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7:869β885
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 251β255
Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414β421
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 99:13,324β13,329
Pawlowska TE, Taylor JW (2004) Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427:733β737
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 44:581β587
Peretto R, Bettini V, Favaron F, Alghisi P, Bonfante P (1995) Polygalacturonase activity and location in arbuscular mycorrhizal roots of Allium porrum L. Mycorrhiza 5:157β163
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 7:91β98
Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180β201
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 131:866β871
Peterson RL, Bonfante P (1994) Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. Plant Soil 159:79β88
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 147β171
Pozo M, AzcΓ³n-Aguilar C, Dumas-Gaudot E, Barea J (1999) Ξ²-1,3-glucanase in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci 141: 149β157
Pozo M, Cordier C, Dumas-Gautod E, Gianinazzi S, Barea J, AzcΓ³n-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525β534
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 425:585β592
Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23β37
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 414:462β466
Ravnskov S, Wu Y, Graham JH (2003) Arbuscular mycorrhizal fungi differentially affect expression of genes coding for sucrose synthases in maize roots. New Phytol 157:539β545
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920β1921
Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841β11843
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 157:555β567
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 132:1540β1549
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 94:5467β5472
Rhody D, Stommel M, Roeder C, Mann P, Franken P (2003) Differential RNA accumulation of two beta-tubulin genes in arbuscular mycorrhizal fungi. Mycorrhiza 13:137β142
Salzer P, CorbiΓ¨re H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208:319β325
Salzer P, Bonanomi A, Beyer K, VΓΆgeli-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 13:763β777
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 135:711β722
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 vesicularβarbuscular endophyte. New Phytol 78:257β268
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 141:2β6
SchΓΌΓler A (2001) Molecular phylogeny, taxonomy, and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi. Plant Soil 244:75β83
SchΓΌΓler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413β1421
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 12:1000β1007
Simon L, Bousquet J, LΓ©vesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67β69
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 60:1810β1813
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 13:238β241
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 213:781β787
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego
Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16β20
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 417:959β962
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 42:69β82
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 131:1468β1478
Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from early devonian. Mycologia 87:560β573
Timonen S, Peterson RL (2002). Cytoskeleton in mycorrhizal symbiosis. Plant Soil 244:199β210
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 8:203β206
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 43:1351β1358
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 183:131β136
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 104:683β689
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 31:243β254
Watson BS, Asirvatham VS, Wang L, Sumner LW (2003) Mapping the proteome of barrel medic (Medicago truncatula). Plant Physiol 131:1104β1123
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 11:933β936
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 16:306β314
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 182:22β26
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 βMolecular Basics of Mycorrhizal Symbiosesβ.
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Hause, B., Fester, T. Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221, 184β196 (2005). https://doi.org/10.1007/s00425-004-1436-x
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DOI: https://doi.org/10.1007/s00425-004-1436-x
