Skip to main content
SpringerLink
Log in

Arbuscular mycorrhizal fungi induce differential activation of the plasma membrane and vacuolar H+ pumps in maize roots

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Roots undergo multiple changes as a consequence of arbuscular mycorrhizal (AM) interactions. One of the major alterations expected is the induction of membrane transport systems, including proton pumps. In this work, we investigated the changes in the activities of vacuolar and plasma membrane (PM) H+ pumps from maize roots (Zea mays L.) in response to colonization by two species of AM fungi, Gigaspora margarita and Glomus clarum. Both the vacuolar and PM H+-ATPase activities were inhibited, while a concomitant strong stimulation of the vacuolar H+-PPase was found in the early stages of root colonization by G. clarum (30 days after inoculation), localized in the younger root regions. In contrast, roots colonized by G. margarita exhibited only stimulation of these enzymatic activities, suggesting a species-specific phenomenon. However, when the root surface H+ effluxes were recorded using a noninvasive vibrating probe technique, a striking activation of the PM H+-ATPases was revealed specifically in the elongation zone of roots colonized with G. clarum. The data provide evidences for a coordinated regulation of the H+ pumps, which depicts a mechanism underlying an activation of the root H+-PPase activity as an adaptative response to the energetic changes faced by the host root during the early stages of the AM interaction.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bago B, Donaire JP, Azcón-Aguilar C (1997) ATPases activities of root from mycorrhizal sunflower (Helianthus annuus) and onion (Allium cepa) plants. New Phytol 136:305–311. doi:10.1046/j.1469-8137.1997.00741.x

    Article  CAS  Google Scholar 

  • Bago B, Azcon-Aguilar C, Piché Y (1998) Architecture and developmental dynamics of the external mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown under monoxenic conditions. Mycologia 90:52–62. doi:10.2307/3761011

    Article  Google Scholar 

  • Bécard G, Fortin J (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol 108:211–218. doi:10.1111/j.1469-8137.1988.tb03698.x

    Article  Google Scholar 

  • Benabdellah K, Azcón-Aguilar C, Ferrol N (1999) Plasma membrane ATPase and H+ transport activities in microsomal membranes from mycorrhizal tomato roots. J Exp Bot 50:1343–1349. doi:10.1093/jexbot/50.337.1343

    Article  CAS  Google Scholar 

  • Berta G, Fusconi A, Trotta A (1993) VA mycorrhizal infection and the morphology and function of root systems. Environ Exp Bot 33:159–173. doi:10.1016/0098-8472(93)90063-L

    Article  Google Scholar 

  • Bestel-Corre G, Dumas-Gaudot E, Poinsot V, Dieu M, Dierick JF, van Tuinen D, Remacle J, Gianinazzi-Pearson V, Gianinazzi S (2002) Proteome analysis and identification of symbiosis-related proteins from Medicago truncatula Gaertn. by two-dimensional electrophoresis and mass spectrometry. Electrophoresis 23:122–137

    Article  CAS  PubMed  Google Scholar 

  • Bonfante-Fasolo P, Perotto S (1992) Plant and endomycorrhizal fungi: the cellular and molecular basis of their interaction. In: Verma DPS (ed) Molecular signals in plant-microbe communications. CRC, Boca Raton, FL, pp 445–470

    Google Scholar 

  • Buch-Pedersen MJ, Rudashevskaya EL, Berner TS, Venema K, Palmgren MG (2006) Potassium as an intrinsic uncoupler of the plasma membrane H+-ATPase. J Biol Chem 281:38285–38292. doi:10.1074/jbc.M604781200

    Article  CAS  PubMed  Google Scholar 

  • Cappellazzo G, Lanfranco L, Fitz M, Wipf D, Bonfante P (2008) Characterization of an amino acid permease from the Endomycorrhizal fungus Glomus mosseae. Plant Physiol 147:429–437. doi:10.1104/pp.108.117820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carystinos GD, MacDonald HR, Monroy AF, Dhindsa RS, Poole RJ (1995) Vacuolar H+-translocating pyrophosphatase is induced by anoxia or chilling in seedlings of rice. Plant Physiol 108:641–649. doi:10.1104/pp.108.2.641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark RB (1975) Characterization of phosphatase of intact maize roots. J Agric Food Chem 23:458–460. doi:10.1021/jf60199a002

    Article  CAS  PubMed  Google Scholar 

  • Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loução MA, Jakobsen I (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792. doi:10.1104/pp.106.090522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies JM, Darley CP, Sanders D (1997) Energetics of the plasma membrane pyrophosphatase. Trends Plant Sci 2:9–10. doi:10.1016/S1360-1385(97)82732-X

    Article  Google Scholar 

  • De Michelis MI, Spanswick RM (1986) H+-pumping driven by vanadate sensitive ATPase in membrane vesicles from corns roots. Plant Physiol 81:542–547

    Article  PubMed  PubMed Central  Google Scholar 

  • Drozdowicz YM, Rea PA (2001) Vacuolar H+-pyrophosphatases: from evolutionary backwaters into mainstream. Trends Plant Sci 6:206–211. doi:10.1016/S1360-1385(01)01923-9

    Article  CAS  PubMed  Google Scholar 

  • Façanha AR, De Meis L (1995) Inhibition of maize root H+-ATPase by fluoride and fluoroaluminate complexes. Plant Physiol 108:241–246

    Article  PubMed  PubMed Central  Google Scholar 

  • Façanha AR, De Meis L (1998) Reversibility of H+-ATPase and H+-Pyrophosphatase in tonoplast vesicles from maize coleoptiles and seeds. Plant Physiol 116:1487–1495. doi:10.1104/pp.116.4.1487

    Article  Google Scholar 

  • Feijó JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK (1999) Growing pollen tubes posses a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J Cell Biol 144:483–496. doi:10.1083/jcb.144.3.483

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferrol N, Pozo MJ, Antelo M, Azcón-Aguilar C (2002) Arbuscular mycorrhizal symbiosis regulates plasma membrane H+-ATPase gene expression in tomato plants. J Exp Bot 53:1683–1687. doi:10.1093/jxb/erf014

    Article  CAS  PubMed  Google Scholar 

  • Fieschi M, Alloatti G, Sacco S, Berta G (1992) Membrane-potential hyperpolarization in vesicular arbuscular mycorrhizae of Allium porrum L.: A non-nutritional long-distance effect of the fungus. Protoplasma 168:136–140. doi:10.1007/BF01666259

    Article  Google Scholar 

  • Fiske CF, Subbarow Y (1925) The colorometric determination of phosphorus. J Biol Chem 66:375–400

    CAS  Google Scholar 

  • Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214. doi:10.1016/j.febslet.2007.03.050

    Article  CAS  PubMed  Google Scholar 

  • Gianinazzi S (1991) Vesicular-arbuscular (endo-) mycorrhizas: cellular, biochemical and genetic aspects. Agric Ecosyst Environ 35:105–119

    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  PubMed Central  Google Scholar 

  • Gianinazzi-Pearson V, Brechenmacher L (2004) Functional genomics of arbuscular mycorrhiza: decoding the symbiotic cell programme. Can J Bot 82:1228–1234. doi:10.1139/b04-096

    Article  CAS  Google Scholar 

  • Gianinazzi-Pearson V, Smith SE, Gianinazzi S, Smith FA (1991) Enzymatic studies on the metabolism of vesicular–arbuscular mycorrhiza. V. Is H+-ATPase a component of ATP-Hydrolysing enzyme activities in plant-fungi interfaces? New Phytol 117:61–74. doi:10.1111/j.1469-8137.1991.tb00945.x

    Article  CAS  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. doi:10.1007/s004250000323

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques to measure vesicular–arbuscular mycorrhizal infection in roots. New Phytol 84:484–500. doi:10.1111/j.1469-8137.1980.tb04556.x

    Article  Google Scholar 

  • Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during preinfection stages. New Phytol 125:587–593. doi:10.1111/j.1469-8137.1993.tb03907.x

    Article  Google Scholar 

  • Giovannetti M, Sbrana C, Citernesi AS, Avio L (1996) Analysis of factors involved in fungal recognition responses to host derived signals by arbuscular mycorrhizal fungi. New Phytol 133:65–71. doi:10.1111/j.1469-8137.1996.tb04342.x

    Article  Google Scholar 

  • Graham JH, Eissenstat DM (1994) Host genotype and the formation and function of VA mycorrhizae. Plant Soil 159:179–185

    Article  Google Scholar 

  • Guttenberger M (2000) Arbuscules of vesicular–arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211:112–118. doi:10.1007/s004250000324

    Article  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. doi:10.1046/j.1365-313X.1996.09040491.x

    Article  CAS  PubMed  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42. doi:10.1146/annurev.micro.58.030603.123749

    Article  CAS  PubMed  Google Scholar 

  • Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–1301. doi:10.1104/pp.104.056572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Statist 5:299–314. doi:10.2307/1390807

    Google Scholar 

  • Jahn T, Baluska F, Michalke W, Harper JF, Volkmann D (1998) Plasma membrane H+-ATPase in the root apex: evidence for strong expression in xylem parenchyma and asymmetric localization within cortical and epidermal cells. Physiol Plant 104:311–316. doi:10.1034/j.1399-3054.1998.1040304.x

    Article  CAS  Google Scholar 

  • James EK, Reis VM, Olivares FL, Baldani J, Döbereiner J (1994) Infection of sugar cane by the nitrogen-fixing bacterium Acetobacter diazotrophicus. J Exp Bot 45:757–766. doi:10.1093/jxb/45.6.757

    Article  CAS  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. doi:10.1055/s-2002-37407

    Article  CAS  Google Scholar 

  • Kunkel JG, Cordeiro S, Xu J, Shipley AM, Feijó JA (2006) The use of non-invasive ion-selective microelectrode techniques for the study of plant development. In: Volkov V (ed) Plant electrophysiology—theory and methods. Springer, Berlin, pp 109–137

    Chapter  Google Scholar 

  • Lambais MR (2006) Unraveling the signaling and signal transduction mechanisms controlling arbuscular mycorrhiza development. Scientia Agricola 63:405–413. doi:10.1590/S0103-90162006000400013

    Article  CAS  Google Scholar 

  • Li H, Smith FA, Dickson S, Holloway RE, Smith SE (2008) Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? New Phytol 178:852–862. doi:10.1111/j.1469-8137.2008.02410.x

    Article  PubMed  Google Scholar 

  • Lichko L, Okorokov L (1991) Purification and some properties of membrane bound and soluble pyrophosphatase of yeast vacuoles. Yeast 7:805–812. doi:10.1002/yea.320070805

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Marx C, Dexheimer J, Gianinazzi-Pearson V, Gianinazzi S (1982) Enzymatic studies on the metabolism of vesicular–arbuscular mycorrhiza. IV. Ultracitoenzymological evidence (ATPase) for active transfer processes in the host-arbuscular interface. New Phytol 90:37–43. doi:10.1111/j.1469-8137.1982.tb03238.x

    Article  CAS  Google Scholar 

  • Mcarthur DAJ, Knowles NR (1993) Influence of vesicular–arbuscular mycorrhizal fungi on the response of potato to phosphorus deficiency. Plant Physiol 101:147–160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mito N, Wimmers LE, Bennett AB (1996) Sugar regulates mRNA abundance of H+-ATPase gene family members in tomato. Plant Physiol 112:1229–1236. doi:10.1104/pp.112.3.1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morsomme P, Boutry M (2000) The plant plasma membrane H+-ATPase: structure, function and regulation. Biochim Biophys Acta 1465:1–16. doi:10.1016/S0005-2736(00)00128-0

    Article  CAS  PubMed  Google Scholar 

  • Murphy PJ, Langridge P, Smith SE (1996) Cloning plant genes differentially expressed during colonization of roots of Hordeum vulgare by the vesicular–arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 135:291–301. doi:10.1046/j.1469-8137.1997.00652.x

    Article  Google Scholar 

  • Nakanishi Y, Maeshima M (1998) Molecular cloning of vacuolar H+-pyrophosphatase and its developmental expression in growing hypocotyl of mung bean. Plant Physiol 116:589–597. doi:10.1104/pp.116.2.589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olivares FL, James EK, Baldani JI, Döbereiner J (1997) Infection of mottled stripe disease susceptible and resistant varieties of sugar cane by the endophytic diazotroph Herbaspirillum. New Phytol 135:723–737. doi:10.1046/j.1469-8137.1997.00684.x

    Article  Google Scholar 

  • Okorokov LA, Silva FE, Okorokova-Façanha AL (2001) Ca2+ and H+ homeostasis in fission yeast: a role of Ca2+/H+ exchange and distinct V-H+-ATPases of the secretory pathway organelles. FEBS Lett 505:321–324. doi:10.1016/S0014-5793(01)02852-6

    Article  CAS  PubMed  Google Scholar 

  • Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845. doi:10.1146/annurev.arplant.52.1.817

    Article  CAS  PubMed  Google Scholar 

  • Park S, Li J, Pittman JK, Berkowitz GA, Yang H, Undurraga S, Morris J, Hirschi KD, Gaxiola RA (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci U S A 102:18830–18835. doi:10.1073/pnas.0509512102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philips JM, Hayman DS (1970) Improved procedure 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 

  • Portillo F (2000) Regulation of plasma membrane H+-ATPase in fungi and plants. Biochim Et Biophys Acta-Rev Biomembr 1469:31–42

    Article  CAS  Google Scholar 

  • Poulsen KH, Nagy R, Gao LL, Smith SE, Bucher M, Smith FA, Jakobsen I (2005) Physiological and molecular evidence for pi uptake via the symbiotic pathway in a reduced mycorrhizal colonization mutant in tomato associated with a compatible fungus. New Phytol 168:445–454. doi:10.1111/j.1469-8137.2005.01523.x

    Article  CAS  PubMed  Google Scholar 

  • Ramos AC, Martins MA, Façanha AR (2005) ATPase and pyrophosphatase activities in corn root microsomes colonized with arbuscular mycorrhizal fungi. Braz J Soil Sci 29:207–213

    CAS  Google Scholar 

  • Ramos AC, Façanha AR, Feijó JA (2008a) Ion dynamics during the polarized growth of arbuscular mycorrhizal fungi: from presymbiosis to symbiosis. In: Varma A, Hock B (eds) Mycorrhiza. Springer, Germany, pp 241–261

    Chapter  Google Scholar 

  • Ramos AC, Façanha AR, Feijó JA (2008b) A proton (H+) flux signature of the presymbiotic development of the arbuscular mycorrhizal fungi. New Phytol 178:177–188. doi:10.1111/j.1469-8137.2007.02344.x

    Article  CAS  PubMed  Google Scholar 

  • Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274

    Article  CAS  PubMed  PubMed Central  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. doi:10.1038/35106601

    Article  CAS  PubMed  Google Scholar 

  • Rosewarne GM, Smith FA, Schachtman DP, Smith SE (2007) Localization of proton-ATPase genes expressed in arbuscular mycorrhizal tomato plants. Mycorrhiza 17:249–258. doi:10.1007/s00572-006-0101-6

    Article  CAS  PubMed  Google Scholar 

  • Schaller A, Oecking C (1999) Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263–272

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schüβler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936

    Article  Google Scholar 

  • Siciliano V, Genre A, Balestrini R, Cappellazzo G, deWit PJGM, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144:1455–1466. doi:10.1104/pp.107.097980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Smith FA (1990) Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol 144:1–38

    Article  Google Scholar 

  • Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482. doi:10.1104/pp.104.048231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valot B, Dieu M, Recorbet G, Raes M, Gianinazzi S, Dumas-Gaudot E (2005) Identification of membrane-associated proteins regulated by the arbuscular mycorrhizal symbiosis. Plant Mol Biol 59:565–580

    Article  CAS  PubMed  Google Scholar 

  • Willians K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734

    Google Scholar 

  • Wright DP, Read DJ, Scholes JD (1998a) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891. doi:10.1046/j.1365-3040.1998.00351.x

    Article  Google Scholar 

  • Wright DP, Scholes JD, Read DJ (1998b) Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21:209–216. doi:10.1046/j.1365-3040.1998.00280.x

    Article  Google Scholar 

  • Xing T, Higgins VJ, Blumwald E (1996) Regulation of plant defense response to fungal pathogens: two types of protein kinases in the reversible phosphorylation of the host plasma membrane H+-ATPase. Plant Cell 8:555–564

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zandonadi DB, Canellas LP, Facanha AR (2007) Indolacetic and humic acids induce lateral root development through a concentrated plasmalemma and tonoplast H+-pumps activation. Planta 225:1583–1595. doi:10.1007/s00425-006-0454-2

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by CAPES (Brazil) and by Post-Doctoral fellowship (SFRH/BPD/21061/2004) conceded to ACR by Fundação para a Ciência e Tecnologia and Instituto Gulbenkian de Ciência (Portugal). ARF is supported by grants from International Foundation for Science (IFS) (C/3483-1) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (475522/01-0 and 479286/03-5). The authors would like to acknowledge Dr. Carlos Tadokoro and Dr Rui Gardner for the manuscript revision, and Dr. Mark Seldon for the critical review and helpful suggestions of the manuscript. We also thank the Microscopy Center “Raul Dodsworth Machado” (UENF-BRAZIL) and Quíssila Batista for the help in preparing the samples for microscopy analysis.

Author information

Authors and Affiliations

  1. Developmental Biology Center, Instituto Gulbenkian de Ciência, Pt-2780-156, Oeiras, Portugal

    Alessandro C. Ramos & José A. Feijó

  2. Centro de Ciências e Tecnologia Agropecuária, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, 28013-600, Brazil

    Marco A. Martins

  3. Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, 28015-620, Brazil

    Anna L. Okorokova-Façanha, Fábio Lopes Olivares, Lev A. Okorokov & Arnoldo R. Façanha

  4. Centro de Estatística e Aplicações da Universidade de Lisboa, Campo Grande Ed C6, 1749-016, Lisbon, Portugal

    Nuno Sepúlveda

  5. Theoretical Immunology Group, Instituto Gulbenkian de Ciência, Pt-2780-156, Oeiras, Portugal

    Nuno Sepúlveda

  6. Faculdade de Ciências, Universidade de Lisboa, DBV, Campo Grande Ed. C2, 1749-016, Lisbon, Portugal

    José A. Feijó

Authors
  1. Alessandro C. Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marco A. Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anna L. Okorokova-Façanha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fábio Lopes Olivares
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lev A. Okorokov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nuno Sepúlveda
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. José A. Feijó
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Arnoldo R. Façanha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arnoldo R. Façanha.

Electronic supplementary material

ESM

a Light microscopy (LM) of cross-section of maize roots var UENF 506-6 colonized by G. clarum at 30 days after inoculation. Note the presence of intraradical hyphae mainly at the outer cortex colonizing intercellular parenchymatic cells (arrowhead) and penetrating through the cortical cells (arrow). Note that hyphae-infected cells are hypertrophic. cc cortical cell, magnification 750×. b Transmission electron microscopy (TEM) showing intraradical hyphae of G. Clarum penetrating parenchymatic cortical cell (arrow) during the earlier steps of the mycorrhizal interaction with maize roots. ld lipid droplets, ie intercellular space, cc cortical cells, magnification 3,000×. c LM of cross-section of maize roots var. UENF 506-6 colonized by G. Clarum at more advanced stage of the symbiotic establishment. Note a significant proportion of colonization of the cortical tissue by VAM structures including arbuscules, magnification 200×. d TEM from previous photomicrograph showing a portion of an arbuscule and intracellular hyphae into a hypertrophic cortical cell (star) (GIF 150 KB)

High resolution image file (EPS 1.13 MB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ramos, A.C., Martins, M.A., Okorokova-Façanha, A.L. et al. Arbuscular mycorrhizal fungi induce differential activation of the plasma membrane and vacuolar H+ pumps in maize roots. Mycorrhiza 19, 69–80 (2009). https://doi.org/10.1007/s00572-008-0204-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-008-0204-3

Keywords

Search

Navigation