Skip to main content
Log in

A Medicago truncatula mutant hyper-responsive to mycorrhiza and defective for nodulation

  • Short Note
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

One key strategy for the identification of plant genes required for mycorrhizal development is the use of plant mutants affected in mycorrhizal colonisation. In this paper, we report a new Medicago truncatula mutant defective for nodulation but hypermycorrhizal for symbiosis development and response. This mutant, called B9, presents a poor shoot and, especially, root development with short laterals. Inoculation with Glomus intraradices results in significantly higher root colonisation of the mutant than the wild-type genotype A17 (+20% for total root length, +16% for arbuscule frequency in the colonised part of the root, +39% for arbuscule frequency in the total root system). Mycorrhizal effects on shoot and root biomass of B9 plants are about twofold greater than in the wild-type genotype. The B9 mutant of M. truncatula is characterised by considerably higher root concentrations of the phytoestrogen coumestrol and by the novel synthesis of the coumestrol conjugate malonyl glycoside, absent from roots of wild-type plants. In conclusion, this is the first time that a hypermycorrhizal plant mutant affected negatively for nodulation (Myc++, Nod −/+ phenotype) is reported. This mutant represents a new tool for the study of plant genes differentially regulating mycorrhiza and nodulation symbioses, in particular, those related to autoregulation mechanisms.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

References

  • Barker SJ, Stummer B, Gao L, Dispain I, O'Connor PJ, Smith SE (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation. Plant J 15:791–797. doi:10.1046/j.1365-313X.1998.00252.x

    Article  CAS  Google Scholar 

  • Bécard G, Douds DD, Pfeffer PE (1992) Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols. Appl Environ Microbiol 58:821–825

    PubMed  PubMed Central  Google Scholar 

  • Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Denarie J (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12:1647–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David-Schwartz R, Badani H, Smadar W, Levy A, Galili G, Kapulnik Y (2001) Identification of a novel genetically controlled step in mycorrhizal colonisation: plant resistance to infection by fungal spores but not extra-radical spores. Plant J 27:561–569. doi:10.1046/j.1365-313X.2001.01113.x

    Article  CAS  PubMed  Google Scholar 

  • David-Schwartz R, Gadkar V, Smadar W, Bendov R, Galili G, Levy A, Kapulnik Y (2003) Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonisation. Mol Plant Microbe Interact 16:382–388. doi:10.1094/MPMI.2003.16.5.382

    Article  CAS  PubMed  Google Scholar 

  • Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal plant mutants (Myc) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci 60:215–222. doi:10.1016/0168-9452(89)90169-6

    Article  Google Scholar 

  • Feet WF, Osman SF (1982) Inhibition of bacteria by the soybean isoflavonoids glyceollin and coumestrol. Phytopathology 72:775–760

    Google Scholar 

  • Graham TL, Graham MY (1991) Glyceollin elicitors induce major but distinctly different shifts in Isoflavonoid metabolism in proximal and distal soybean cell populations. Mol Plant Microbe Interact 4:60–68

    Article  CAS  Google Scholar 

  • Graham TL, Kim JE, Graham MY (1990) Role of constitutive isoflavone conjugates in the accumulation of glyceollin in soybean infected with Phytophthora megasperma. Mol Plant Microbe Interact 3:157–166

    Article  CAS  Google Scholar 

  • Harborne JB (1994) For the content of “Flavonoids”. In: Buckingham J (eds) Dictionary of Natural Products. Chapman and Hall, New York, pp 449-468 and 673-700

  • Harrison MJ, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant Microbe Interact 6:643–654

    Article  CAS  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. In: (eds) Technical Commmunication No. 22. Commonwealth Agricultural Bureau, London, pp 430-434

  • Hsieh M-C, Graham TL (2001) Partial purification and characterization of a soybean ß-glucosidase with high specific activity towards isoflavone conjugates. Phytochemistry 58:995–1005

    Article  CAS  PubMed  Google Scholar 

  • Kosslak RM, Bookland R, Barkei J, Paaren HE, Appelbaum ER (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci USA 84:7428–7432. doi:10.1073/pnas.84.21.7428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin LZ, He XG, Lindenmaier M, Yang J, Cleary M, Qiu SX, Cordell GA (2000) LC–ESI–MS study of the flavonoid glycoside malonates of red clover (Trifolium pratense). J Agric Food Chem 48:354–365. doi:10.1021/jf991002+

    Article  CAS  PubMed  Google Scholar 

  • Lohse S, Schliemann W, Ammer C, Kopka J, Strack D, Fester T (2005) Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of Medicago truncatula. Plant Physiol 139:329–340. doi:10.1104/pp.105.061457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyon FM, Wood RKS (1975) Production of phaseollin, coumestrol and related compounds in bean leaves inoculated with Pseudomonas spp. Physiol Plant Pathol 6:117–124. doi:10.1016/0048-4059(75)90039-9

    Article  CAS  Google Scholar 

  • Mabry TJ, Markham KR, Thomas MB (1970) The systematic identification of flavonoids. Springer, New York

    Book  Google Scholar 

  • Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Pühler A, Perlick A, Küster H (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant Microbe Interact 17:1063–1077. doi:10.1094/MPMI.2004.17.10.1063

    Article  CAS  PubMed  Google Scholar 

  • Marsh JF, Schultze M (2001) Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytol 150:525–532. doi:10.1046/j.1469-8137.2001.00140.x

    Article  Google Scholar 

  • Meixner C, Ludwig-Muller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715. doi:10.1007/s00425-005-0003-4

    Article  CAS  PubMed  Google Scholar 

  • Modolo LV, Blount JW, Achnine L, Naoumkina MA, Wang X, Dixon RA (2007) A functional genomics approach to (iso) flavonoid glycosylation in the model legume Medicago truncatula. Plant Mol Biol 64:499–518. doi:10.1007/s11103-007-9167-6

    Article  CAS  PubMed  Google Scholar 

  • Morandi D (1996) Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant Soil 185:241–251. doi:10.1007/BF02257529

    Article  CAS  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. doi:10.1016/0048-4059(84)90009-2

    Article  CAS  Google Scholar 

  • Morandi D, Branzanti B, Gianinazzi-Pearson V (1992) Effect of some plant flavonoids on in vitro behaviour of an arbuscular mycorrhizal fungus. Agronomie 12:811–816. doi:10.1051/agro:19921012

    Article  Google Scholar 

  • Morandi D, Sagan M, PradoVivant 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. doi:10.1007/s005720050285

    Article  CAS  Google Scholar 

  • Morandi D, Prado E, Sagan M, Duc G (2005) Characterisation of new symbiotic Medicago truncatula (Gaertn.) mutants, and phenotypic or genotypic complementary information on previously described mutants. Mycorrhiza 15:283–289. doi:10.1007/s00572-004-0331-4

    Article  PubMed  Google Scholar 

  • O'Neill NR (1996) Defense expression in protected tissues of Medicago sativa is enhanced during compatible interactions with Colletotrichum trifolii. Phytopathology 86:1045–1050. doi:10.1094/Phyto-86-1045

    Article  Google Scholar 

  • Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421. doi:10.1016/j.pbi.2004.05.011

    Article  CAS  PubMed  Google Scholar 

  • Penmetsa RV, Cook DR (2000) Production and characterization of diverse developmental mutants of Medicago truncatula. Plant Physiol 123:1387–1397. doi:10.1104/pp.123.4.1387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Phillips DA, Tsai SM (1992) Flavonoids as plant signals to rhizosphere microbes. Mycorrhiza 1:55–58. doi:10.1007/BF00206136

    Article  CAS  Google Scholar 

  • Reddy S, 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. doi:10.1111/j.1365-313X.2007.03175.x

    Article  Google Scholar 

  • Sagan M, Morandi D, Tarenghi E, Duc G (1995) Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn) after gamma-ray mutagenesis. Plant Sci 111:63–71. doi:10.1016/0168-9452(95)04229-N

    Article  CAS  Google Scholar 

  • Scervino J, Ponce M, Erra-Bassels R, Vierheilig H, Ocampo J, Godeas A (2005a) Flavonoids exclusively present in mycorrhizal roots of white clover exhibit different effects on arbuscular mycorrhizal fungi than flavonoids exclusively present in non-mycorrhizal roots of white clover. J Plant Interact 15:22–30

    Google Scholar 

  • Scervino J, Ponce M, Erra-Bassels R, Vierheilig H, Ocampo J, Godeas A (2005b) Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycol Res 109:789–794. doi:10.1017/S0953756205002881

    Article  CAS  PubMed  Google Scholar 

  • Scervino J, Ponce M, Erra-Bassels R, Vierheilig H, Ocampo J, Godeas A (2005c) Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomus species in presence of roots flavonoids. J Plant Physiol 162:625–633. doi:10.1016/j.jplph.2004.08.010

    Article  CAS  PubMed  Google Scholar 

  • Scervino J, Ponce M, Erra-Bassels R, Vierheilig H, Ocampo J, Godeas A (2007) The effect of flavones and flavonols on colonization of tomato plants by arbuscular mycorrhizal fungi of the genera Gigaspora and Glomus. Can J Microbiol 53:702–709. doi:10.1139/W07-036

    Article  CAS  PubMed  Google Scholar 

  • Shrihari PC, Sakamoto K, Inubushi K, Akao S (2000) Interaction between supernodulating or non-nodulating mutants of soybean and two arbuscular mycorrhizal fungi. Mycorrhiza 10:101–106. doi:10.1007/s005720000064

    Article  Google Scholar 

  • Siqueira JO, Nair MG, Hammerschmidt R, Safir GR (1991a) Significance of phenolic compounds in plant-soil-microbial systems. Crit Rev Plant Sci 10:63–121. doi:10.1080/07352689109382307

    Article  CAS  Google Scholar 

  • Siqueira JO, Safir GR, Nair MG (1991b) Stimulation of vesicular-arbuscular mycorrhiza formation and growth of white clover by flavonoid compounds. New Phytol 118:87–93. doi:10.1111/j.1469-8137.1991.tb00568.x

    Article  CAS  Google Scholar 

  • Solaiman MZ, Senoo K, Kawaguchi M, ImaizumiAnraku H, Akao S, Tanaka A, Obata H (2000) Characterization of mycorrhizas formed by Glomus sp on roots of hypernodulating mutants of Lotus japonicus. J Plant Res 113:443–448. doi:10.1007/PL00013953

    Article  Google Scholar 

  • Tiller SA, Parry AD, Edwards R (1994) Changes in the accumulation of flavonoid and isoflavonoid conjugates associated with plant-age and nodulation in alfalfa (Medicago sativa). Physiol Plant 91:27–36. doi:10.1111/j.1399-3054.1994.tb00655.x

    Article  CAS  Google Scholar 

  • Tinwell H, Soames AR, Foster JR, Ashby J (2000) Estradiol-type activity of coumestrol in mature and immature ovariectomized rat uterotrophic assays. Environ Health Perspect 108:631–634. doi:10.2307/3434883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai SM, Phillips DA (1991) Flavonoids released naturally from alfalfa promote development of symbiotic Glomus spores in vitro. Appl Environ Microbiol 57:1485–1488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vierheilig H (2004) Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176. doi:10.1139/b04-015

    Article  CAS  Google Scholar 

  • Vierheilig H, Bago B, Albrecht C, Poulin MJ, Piche Y (1998) Flavonoids and arbuscular-mycorrhizal fungi. In: Manthey J, Buslig B (eds) Flavonoids in the living system. Plenum, New York, pp 9–33

    Chapter  Google Scholar 

  • Vierheilig H, Steinkellner S, Khaosaad T, Garcia-Garrido J (2008) The biocontrol effect of mycorrhization on soil-borne fungal pathogens and the autoregulation of the AM symbiosis: one mechanism, two effects? In: Varma A (ed) Mycorrhiza: genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer, Heidelberg, Germany, pp 307–320

    Chapter  Google Scholar 

  • Zuanazzi JAS, Clergeot PH, Quirion JC, Husson HP, Kondorosi A, Ratet P (1998) Production of Sinorhizobium meliloti nod gene activator and repressor flavonoids from Medicago sativa roots. Mol Plant Microbe Interact 11:784–794. doi:10.1094/MPMI.1998.11.8.784

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dominique Morandi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morandi, D., le Signor, C., Gianinazzi-Pearson, V. et al. A Medicago truncatula mutant hyper-responsive to mycorrhiza and defective for nodulation. Mycorrhiza 19, 435–441 (2009). https://doi.org/10.1007/s00572-009-0242-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-009-0242-5

Keywords

Navigation