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Microtubule organization in root cells ofMedicago truncatula during development of an arbuscular mycorrhizal symbiosis withGlomus versiforme

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Summary

The colonization of plants by arbuscular mycorrhizal fungi has been shown to induce changes in cytoplasmic organization and morphology of root cells. Because of their role in a variety of cellular functions in plants, it is likely that microtubules are involved either in the signaling events leading to the establishment of the symbiosis or in changes in host cell morphology and cytoplasmic architecture. Recent studies of the arbuscular mycorrhizal symbiosis have shown that root cortical cells reorganize their microtubules upon colonization. These studies, however, have focused primarily on the cells containing hyphal coils or arbuscules and did not include descriptions of microtubule changes in adjacent cells. To probe further into the potential role of the microtubule cytoskeleton in the establishment of arbuscular mycorrhizal symbiosis, we examined the three-dimensional arrangement of microtubules in roots of the model legumeMedicago truncatula colonized by the arbuscular mycorrhizal fungusGlomus versiforme by indirect immunofluorescence and confocal microscopy. Our data show extensive remodeling of the microtubule cytoskeleton from the early stages of arbuscule development until arbuscule collapse and senescence. While confirming some of the microtubule patterns shown in other mycorrhizal systems, our results also reveal that cortical cells adjacent to those containing arbuscules or adjacent to intercellular hyphae reorganize their microtubules. This indicates that the cortical cells initiate the modification of their cytoskeleton prior to entry of the fungus and is consistent with signal exchange between the symbionts prior to fungal penetration of the cells.

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Abbreviations

WGA:

wheat germ agglutinin

References

  • Alexander T, Toth R, Meier R, Weber HC (1989) Dynamics of arbuscule development and degeneration in onion, bean and tomato with reference to vesicular-arbuscular mycorrhizae in grasses. Can J Bot 67: 2505–2513

    Google Scholar 

  • Arnon DI, Hoagland DR (1940) Crop production in artificial culture solutions and in soils with special reference to factors influencing yields and absorption of inorganic nutrients. Soil Sci 50: 463–483

    Google Scholar 

  • Balestrini R, Berta G, Bonfante P (1992) The plant nucleus in mycorrhizal roots: positional and structural modifications. Biol Cell 75: 235–243

    Google Scholar 

  • —, José-Estanyol M, Puigdoménech P, Bonfante P (1997) Hydroxyproline-rich glycoprotein mRNA accumulation in maize root cells colonized by an arbuscular mycorrhizal fungus as revealed by in situ hybridization. Protoplasma 198: 36–42

    Google Scholar 

  • —, Perotto S, Gasverde E, Dahiya P, Guldmann LL, Brewin NJ, Bonfante P (1999) Transcription of a gene encoding a lectinlike glycoprotein is induced in root cells harboring arbuscular mycorrhizal fungi inPisum sativum. Mol Plant Microbe Interact 12: 785–791

    Google Scholar 

  • Baluska F, Volkmann D, Barlow PW (1996) Complete disintegration of the microtubule cytoskeleton precedes auxin-mediated reconstruction in post-mitotic maize root cells. Plant Cell Physiol 37: 1013–1021

    Google Scholar 

  • Barker DG, Bianchi S, Blondon F, Dattée Y, Duc G, Essad S, Flament P, Gallusci P, Génier G, Guy P, Muel X, Tourneur J, Dénarié J, Huguet T (1990)Medicago truncatula, a model plant for studying the molecular genetics of theRhizobium-legume symbiosis. Plant Mol Biol Rep 8: 40–49

    Google Scholar 

  • Barker SJ, Tagu D (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Regul 19: 144–154

    Google Scholar 

  • Baskin TI, Wilson JE, Cork A, Williamson RE (1994) Morphology and microtubule organization in Arabidopsis roots exposed to oryzalin or taxol. Plant Cell Physiol 35: 935–942

    Google Scholar 

  • Blancaflor EB, Hasenstein KH (1993) Organization of cortical microtubules in graviresponding maize roots. Planta 191: 231–237

    Google Scholar 

  • — — (1995a) Growth and microtubule orientation of maize roots subjected to osmotic stress. Int J Plant Sci 156: 794–802

    Google Scholar 

  • — — (1995b) Time course and auxin sensitivity of cortical microtubule reorientation in maize roots. Protoplasma 185: 72–82

    Google Scholar 

  • —, Jones DL, Gilroy S (1998) Alterations in the cytoskeleton accompany aluminum induced growth inhibition and morphological changes in primary roots ofZea mays L. Plant Physiol 118: 159–172

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Bonfante-Fasolo P (1984) Anatomy and morphology of VA mycorrhizae. In: Powell CL, Bagyaraj DJ (eds) VA mycorrhizae. CRC Press, Boca Raton, Fla, pp 5–33

    Google Scholar 

  • Brown RC, Lemmon BE (1995) Methods in plant immunolight microscopy. Methods Plant Cell Biol A 49: 85–107

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Cleary AL, Hardham AR (1993) Pressure induced reorientation of cortical microtubules in epidermal cells ofLolium rigidum leaves. Plant Cell Physiol 34: 1003–1008

    Google Scholar 

  • Cook DR (1999)Medicago truncatula: a model in the making. Curr Opin Plant Biol 2: 301–304

    Google Scholar 

  • Fisher DD, Cyr RJ (1998) Extending the microtubule/microfibril paradigm: cellulose synthesis is required for normal cortical microtubule alignment in elongating cells. Plant Physiol 116: 1043–1051

    Google Scholar 

  • Geitmann A, Emons AMC (2000) The cytoskeleton in plant and fungal cell tip growth. J Microsc 198: 218–245

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • — — (1999) Cytoskeleton-related proteins in tobacco mycorrhizal cells: γ-tubulin and clathrin localisation. Eur J Histochem 43: 105–111

    Google Scholar 

  • Gianinazzi-Pearson V, Smith SE, Gianinazzi S, Smith FA (1991) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. New Phytol 117: 61–74

    Google Scholar 

  • Hardham AR, Mitchell HJ (1998) Use of molecular cytology to study the structure and biology of phytopathogenic and mycorrhizal fungi. Fung Genet Biol 24: 252–284

    Google Scholar 

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

    Google Scholar 

  • —, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesiculararbuscular mycorrhizal associations in roots ofMedicago truncatula. Mol Plant Microbe Interact 6: 643–654

    Google Scholar 

  • Hasenstein KH, Blancaflor EB, Lee JS (1999) The microtubule cytoskeleton does not integrate auxin transport and gravitropism in maize roots. Physiol Plant 105: 729–738

    Google Scholar 

  • Hush JM, Overall RL (1991) Electrical and mechanical fields orient cortical microtubules in higher plant tissues. Cell Biol Int Rep 15: 551–560

    Google Scholar 

  • —, Hawes CR, Overall RL (1990) Interphase microtubule reorientation precedes a new cell polarity in wounded pea roots. J Cell Sci 96: 47–61

    Google Scholar 

  • Hwang J-U, Suh S, Yi H, Kim J, Lee Y (1997) Actin filaments modulate both stomatal opening and inward K+-channel activities in guard cells ofVicia faba L. Plant Physiol 115: 335–342

    Google Scholar 

  • Kost B, Mathur J, Chua N-H (1999) Cytoskeleton in plant development. Curr Opin Plant Biol 2: 462–470

    Google Scholar 

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

    Google Scholar 

  • Murphy PJ, Langridge P, Smith SE (1997) Cloning plant genes differentially expressed during colonization of roots ofHordeum vulgare by the vesicular-arbuscular mycorrhizal fungusGlomus intraradices. New Phytol 135: 291–301

    Google Scholar 

  • Nick P (1998) Signaling to the microtubular cytoskeleton in plants. Int Rev Cytol 184: 33–80

    Google Scholar 

  • Niini SS, Tarkka MT, Raudaskoski M (1996) Tubulin and actin protein patterns in Scots pine (Pinus sylvestris) roots and developing ectomycorrhiza withSuillus bovinus. Physiol Plant 96: 186–192

    Google Scholar 

  • Peterson RL, Uetake Y, Armstrong LN (2000) Interactions between fungi and the plant cytoskeleton. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. American Phytopathological Society Press, St Paul, Minn, pp 157–178

    Google Scholar 

  • Rosewarne G, Barker S, Smith S, Smith F, Schachtman D (1999) ALycopersicon esculentum phosphate transporter (LePT1) involved in phosphorous uptake from a vesicular-arbuscular mycorrhizal fungus. New Phytol 144: 507–516

    Google Scholar 

  • Roussel H, Bruns S, Gianinazzi-Pearson V, Hahlbrock K, Franken P (1997) Induction of a membrane intrinsic protein-encoding mRNA in arbuscular mycorrhiza and elicitor-stimulated cell suspension cultures of parsley. Plant Sci 126: 203–210

    Google Scholar 

  • Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma-membrane. Annu Rev Physiol Plant Mol Biol 45: 527–544

    Google Scholar 

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

    Google Scholar 

  • Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51: 527–588

    Google Scholar 

  • Thion L, Mazars C, Nacry P, Bouchez D, Moreau M, Ranjeva R, Thuleau P (1998) Plasma membrane depolarization-activated calcium channels, stimulated by microtubule-depolymerizing drugs in wild-typeArabidopsis thaliana protoplasts, display constitutively large activities and a longer half-life inton2 mutant cells affected in the organization of cortical microtubules. Plant J 13: 603–610

    Google Scholar 

  • Uetake Y, Peterson RL (1997) Changes in actin filament arrays in protocorm cells of the orchid species,Spiranthes sinensis, induced by the symbiotic fungusCeratobasidium cornigerum. Can J Bot 75: 1661–1669

    Google Scholar 

  • — — (1998) Association between microtubules and symbiotic fungal hyphae in protocorm cells of the orchid species,Spiranthes sinensis. New Phytol 140: 715–722

    Google Scholar 

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

    Google Scholar 

  • Wymer C, Lloyd C (1996) Dynamic microtubules: implications for cell wall patterns. Trends Plant Sci 1: 222–228

    Google Scholar 

  • Zandomeni K, Schopfer P (1994) Mechanosensory microtubule reorientation in the epidermis of maize coleoptiles subjected to bending stress. Protoplasma 182: 96–101

    Google Scholar 

Download references

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Authors and Affiliations

  1. Plant Biology Division, The Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, 73401, Ardmore, OK, USA

    Elison B. Blancaflor, Liming Zhao & Maria J. Harrison

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  1. Elison B. Blancaflor
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  2. Liming Zhao
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  3. Maria J. Harrison
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Blancaflor, E.B., Zhao, L. & Harrison, M.J. Microtubule organization in root cells ofMedicago truncatula during development of an arbuscular mycorrhizal symbiosis withGlomus versiforme . Protoplasma 217, 154–165 (2001). https://doi.org/10.1007/BF01283396

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