Skip to main content
SpringerLink
Log in

Plant potassium content modifies the effects of arbuscular mycorrhizal symbiosis on root hydraulic properties in maize plants

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

Abstract

It is well known that the arbuscular mycorrhizal (AM) symbiosis helps the host plant to overcome several abiotic stresses including drought. One of the mechanisms for this drought tolerance enhancement is the higher water uptake capacity of the mycorrhizal plants. However, the effects of the AM symbiosis on processes regulating root hydraulic properties of the host plant, such as root hydraulic conductivity and plasma membrane aquaporin gene expression, and protein abundance, are not well defined. Since it is known that K+ status is modified by AM and that it regulates root hydraulic properties, it has been tested how plant K+ status could modify the effects of the symbiosis on root hydraulic conductivity and plasma membrane aquaporin gene expression and protein abundance, using maize (Zea mays L.) plants and Glomus intraradices as a model. It was observed that the supply of extra K+ increased root hydraulic conductivity only in AM plants. Also, the different pattern of plasma membrane aquaporin gene expression and protein abundance between AM and non-AM plants changed with the application of extra K+. Thus, plant K+ status could be one of the causes of the different observed effects of the AM symbiosis on root hydraulic properties. The present study also highlights the critical importance of AM fungal aquaporins in regulating root hydraulic properties of the host plant.

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

  • Alguacil MM, Kohler J, Caravaca F, Roldán A (2009) Differential effects of Pseudomonas mendoica and Glomus intraradices on lettuce plants. Physiological response and aquaporin PIP2 gene expression under elevated atmospheric CO2 and drought. Microb Ecol 58:942–951

    Article  Google Scholar 

  • Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297

    Article  Google Scholar 

  • Aroca R, Amodeo G, Fernández-Illescas S, Herman EM, Chaumont F, Chrispeels MJ (2005) The role of aquaporins and mmebrane damage in chilling and hydrogen peroxide indiced changes in the hydraulic conductance of maize roots. Plant Physiol 137:341–353

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Alguacil MM, Vernieri P, Ruiz-Lozano JM (2008a) Plant responses to drought stress and exogenous ABA application is modulated differently by mycorrhization in tomato and an ABA-deficient mutant. Microb Ecol 56:704–719

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Vernieri P, Ruiz-Lozano JM (2008b) Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J Exp Bot 59:2029–2041

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Bago A, Sutka M, Paz JA, Cano C, Amodeo G, Ruiz-Lozano JM (2009) Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Mol Plant Microb Interact 22:1169–1178

    Article  CAS  Google Scholar 

  • Bago B, Pfeffer PE, Zipfel W, Lammers P, Shachar-Hill Y (2002) Tracking metabolism and imaging transport in arbuscular mycorrhizal fungi. Metabolism and transport in AM fungi. Plant Soil 244:189–197

    Article  CAS  Google Scholar 

  • Bárzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta MC, Carvajal M, Ruiz-Lozano JM (2012) Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann Bot (on-line first) doi:10.1093/aob/mcs007

  • Benabdellah K, Ruiz-Lozano JM, Aroca R (2009) Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Mol Biol 70:647–661

    Article  PubMed  CAS  Google Scholar 

  • Benlloch-González M, Fournier JM, Benlloch M (2010) K+ deprivation induces xylem water and K+ transport in sunflower: evidence for a co-ordinated control. J Exp Bot 61:157–164

    Article  PubMed  Google Scholar 

  • Berreck M, Haselwandter K (2001) Effect of the arbuscular mycorrhizal symbiosis upon uptake of cesium and other cations by plants. Mycorrhiza 10:275–280

    Article  CAS  Google Scholar 

  • Cabañero FJ, Carvajal M (2007) Different cation stresses affect specifically osmotic root hydraulic conductance, involving aquaporins, ATPase and xylem loading of ions in Capsicum annum L. plants. J Plant Physiol 164:1300–1310

    Article  PubMed  Google Scholar 

  • Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530

    Article  CAS  Google Scholar 

  • Dell’Amico J, Torrecillas A, Rodríguez P, Morte A, Sánchez-Blanco MJ (2002) Responses of tomato plants associated with the arbuscular mycorrhizal fungus Glomus clarum during drought and recovery. J Agric Sci 138:387–393

    Google Scholar 

  • Dietz S, von Bülow J, Beitz E, Nehls U (2011) The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: Lessons for symbiotic functions. New Phytol 190:927–940

    Article  PubMed  CAS  Google Scholar 

  • Dupré de Boulois H, Voets L, Delvaux B, Jakobsen I, Declerck S (2006) Transport of radiocaesium by arbuscular mycorrhizal fungi to Medicago truncatula under in vitr conditions. Environ Microbiol 8:1926–1934

    Article  Google Scholar 

  • Egilla JN, Davies FT Jr, Drew MC (2001) Effect of potassium on drought resistance of Hibiscus rosa-sinensis cv. Leprechaun: Plant growth, leaf macro- and micronutrient content and root longevity. Plant Soil 229:213–224

    Article  CAS  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  PubMed  CAS  Google Scholar 

  • Fan MS, Bai RQ, Zhao XF, Zhnag JH (2007) Aerenchyma formed under phosphorus deficiency contributes to the reduced root hydraulic conductivity in maize roots. J Integr Plant Biol 49:598–604

    Article  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Goicoechea N, Merino S, Sánchez-Díaz M (2004) Contribution of arbuscular mycorrhizal fungi (AMF) to the adaptations exhibited by the deciduous shrub Anthyllis cytisoides under water deficit. Physiol Plant 122:453–464

    Article  CAS  Google Scholar 

  • Graham JH, Syvertsen JP (1984) Influence of vesicular-arbuscular mycorrhiza on the hydraulic conductivity of roots of two citrus rootstocks. New Phytol 97:277–284

    Article  Google Scholar 

  • Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F (2006) Localization and quatification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol 62:305–323

    Article  PubMed  CAS  Google Scholar 

  • Jang JY, Rhee JY, Kim DG, Chung GC, Lee JH, Kang H (2007) Ectopic expression of a foreign aquaporin disrupts the natural expression pattern of endogenous aquaporin genes and alters plant responses to different stress conditions. Plant Cell Physiol 48:1331–1339

    Article  PubMed  CAS  Google Scholar 

  • Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J, Vinh J, Heyes J, Franck KI, Schäffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:713–725

    Google Scholar 

  • Khalvati MA, Hu Y, Mozafar A, Schmidhalter U (2005) Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol 7:706–712

    Article  PubMed  CAS  Google Scholar 

  • Krishna H, Singh SK, Sharma RR, Khawale RN, Grover M, Patel VB (2005) Biochemical changes in micropropagated grape (Vitis vinifera L.) plantlets due to arbuscular-mycorrhizal fungi (AMF) inoculation during ex vitro acclimatization. Sci Hortic 106:554–567

    Article  CAS  Google Scholar 

  • Levy Y, Syvertsen JP, Nemec S (1983) Effect of drought stress and vesicular-arbuscular mycorrhiza on Citrus transpiration and hydraulic conductivity of roots. New Phytol 93:61–66

    Article  Google Scholar 

  • Li YS, Mao XT, Tian QY, Li LH, Zhang WH (2009) Phosphorous deficiency-induced reduction in root hydraulic conductivity in Medicago falcata is associated with ethylene production. Environ Exp Bot 67:172–177

    Article  CAS  Google Scholar 

  • Liu HY, Sun WN, Su WA, Tang ZC (2006) Co-regulation of water channels and potassium channels in rice. Physiol Plant 128:58–69

    Article  CAS  Google Scholar 

  • Marulanda A, Azcón R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533

    Article  CAS  Google Scholar 

  • Marulanda A, Azcón R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232:533–543

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Kado RT, Guern J, Chrispeels MJ (1995) Phosphorylation regulates the water channel activity of the seed-specific aquaporin alpha-TIP. EMBO J 14:3028–3035

    PubMed  CAS  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  PubMed  CAS  Google Scholar 

  • Miller RM, Hetrick BAD, Wilson GWT (1997) Mycorrhizal fungi affect root stele tissue in grasses. Can J Bot 75:1778–1784

    Article  Google Scholar 

  • Muries B, Faize M, Carvajal M, Martínez-Ballesta MC (2011) Identification and differential induction of the expression of aquaporins by salinity in broccoli plants. Mol Biosyst 7:1322–1335

    Article  PubMed  CAS  Google Scholar 

  • Oddo E, Inzerillo S, La Bella F, Grisafi F, Salleo S, Nardini A (2011) Short-term effects of potassium fertilization on the hydraulic conductance of Laurus nobilis L. Tree Physiol 31:131–138

    Article  PubMed  Google Scholar 

  • Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ Exp Bot 57:177–186

    Article  CAS  Google Scholar 

  • Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F (2009) Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiol 149:2000–2012

    Article  PubMed  CAS  Google Scholar 

  • Park W, Scheffler BE, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol 10:142

    Article  PubMed  Google Scholar 

  • Peng YH, Lin WL, Cai WM, Arora R (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226:729–740

    Article  PubMed  CAS  Google Scholar 

  • Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750

    Article  PubMed  CAS  Google Scholar 

  • Porcel R, Azcón R, Ruiz-Lozano JM (2004) Evaluation of the role of genes encoding for D-(1)-pyrroline-5-carboxylate synthetase (P5CS) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. Physiol Mol Plant Pathol 65:211–221

    Article  CAS  Google Scholar 

  • Porcel R, Aroca R, Azcón R, Ruiz-Lozano JM (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol Biol 60:389–404

    Article  PubMed  CAS  Google Scholar 

  • Porras-Soriano A, Soriano-Martín ML, Porras-Piedra A, Azcón R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359

    Article  PubMed  CAS  Google Scholar 

  • Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schäffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol 152:1418–1430

    Article  PubMed  CAS  Google Scholar 

  • Querejeta JI, Allen MF, Alguacil MM, Roldán A (2007) Plant isotopic composition provides insight mechanisms underlying growth stimulation by AM fungi in a semiarid environment. Funct Plant Biol 34:683–691

    Article  CAS  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 culture of parsley. Plant Sci 126:203–210

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Aroca R (2010) Modulation of aquaporin genes by the arbuscular mycorrhizal symbiosis in relation to osmotic stress tolerance. In: Symbioses and stress: joint ventures in biology, cellular origin, life in extreme habitats. Edited by Seckbach J, Grube M. Springer Science + Business Media; pp 359–374

  • Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95:472–478

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Gómez M, Azcón R (1995) Influence of different Glomus species on the time-course of physiological plant-responses of lettuce to progressive drought stress periods. Plant Sci 110:37–44

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Palma JM (1996) Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytol 134:327–333

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Aroca R (2006) Does the enhanced tolerance of arbuscular mycorrhizal plants to water déficit involve modulation of drought-induced plant genes? New Phytol 171:693–698

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Lozano JM, Alguacil MM, Bárzana G, Vernieri P, Aroca R (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Mol Biol 70:565–579

    Article  PubMed  CAS  Google Scholar 

  • Ruth B, Khalvati M, Schmidhalter U (2011) Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant Soil 342:459–468

    Article  CAS  Google Scholar 

  • Sánchez-Blanco MJ, Ferrández T, Morales MA, Morte A, Alarcón JJ (2004) Variations in water status, gas exchange, and growth in Rosmarinus officinalis plants infected with Glomus deserticola under drought conditions. J Plant Physiol 161:675–682

    Article  PubMed  Google Scholar 

  • Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869–876

    Article  PubMed  CAS  Google Scholar 

  • Sorieul M, Santoni V, Maurel C, Luu DT (2011) Mechanisms and effects of retention of over-expressed aquaporin AtPIP2;1 in the endoplasmatic reticulum. Traffic 12:473–482

    Article  PubMed  CAS  Google Scholar 

  • Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51:1531–1542

    Article  PubMed  CAS  Google Scholar 

  • Tazawa M, Sutou E, Shibasaka M (2001) Onion root water transport sensitive to water channel and K+ channel inhibitors. Plant Cell Physiol 42:28–36

    Article  PubMed  CAS  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken Ph, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JPW, Gianinazzi-Pearson V, Martin F (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769

    Article  PubMed  CAS  Google Scholar 

  • Uehlein N, Fileschi K, Eckert M, Bienert GP, Bertl A, Kaldenhoff R (2007) Arbuscular mycorrhizal symbiosis and plant aquaporins expression. Phytochemistry 68:122–129

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín (CSIC), Profesor Albareda 1, 18008, Granada, Spain

    Mohamed Najib El-Mesbahi, Rosario Azcón, Juan Manuel Ruiz-Lozano & Ricardo Aroca

Authors
  1. Mohamed Najib El-Mesbahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rosario Azcón
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan Manuel Ruiz-Lozano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ricardo Aroca
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ricardo Aroca.

Rights and permissions

Reprints and permissions

About this article

Cite this article

El-Mesbahi, M.N., Azcón, R., Ruiz-Lozano, J.M. et al. Plant potassium content modifies the effects of arbuscular mycorrhizal symbiosis on root hydraulic properties in maize plants. Mycorrhiza 22, 555–564 (2012). https://doi.org/10.1007/s00572-012-0433-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-012-0433-3

Keywords

Search

Navigation