Skip to main content
SpringerLink
Log in

Relative importance of an arbuscular mycorrhizal fungus (Rhizophagus intraradices) and root hairs in plant drought tolerance

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

Abstract

Both arbuscular mycorrhizal (AM) fungi and root hairs play important roles in plant uptake of water and mineral nutrients. To reveal the relative importance of mycorrhiza and root hairs in plant water relations, a bald root barley (brb) mutant and its wild type (wt) were grown with or without inoculation of the AM fungus Rhizophagus intraradices under well-watered or drought conditions, and plant physiological traits relevant to drought stress resistance were recorded. The experimental results indicated that the AM fungus could almost compensate for the absence of root hairs under drought-stressed conditions. Moreover, phosphorus (P) concentration, leaf water potential, photosynthetic rate, transpiration rate, stomatal conductance, and water use efficiency were significantly increased by R. intraradices but not by root hairs, except for shoot P concentration and photosynthetic rate under the drought condition. Root hairs even significantly decreased root P concentration under drought stresses. These results confirm that AM fungi can enhance plant drought tolerance by improvement of P uptake and plant water relations, which subsequently promote plant photosynthetic performance and growth, while root hairs presumably contribute to the improvement of plant growth and photosynthetic capacity through an increase in shoot P concentration.

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

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381

    Article  Google Scholar 

  • Baldwin JP, Tinker PB, Nye PH (1972) Uptake of solutes by multiple root systems from soil. 2. Theoretical effects of rooting density and pattern on uptake of nutrients from soil. Plant Soil 36:693–708

    Article  CAS  Google Scholar 

  • Baon JB, Smith SE, Alston AM (1994) Growth responses and phosphorus uptake of rye with long and short root hairs: interactions with mycorrhizal infection. Plant Soil 167:247–254

    Article  CAS  Google Scholar 

  • Barber SA (1984) Soil nutrient bioavailability—a mechanistic approach. Wiley-Interscience, New York

    Google Scholar 

  • Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250

    Article  CAS  Google Scholar 

  • Baylis GTS (1975) The magnolioidmycorrhiza and mycotrophy in root systems derived from it. In: Sanders FE, Mosse B, Tinker PB (eds) Endomycorrhizas. Academic Press, New York, pp 373–389

    Google Scholar 

  • Biermann B, Linderman RG (1981) Quantifying vesicular-arbuscular mycorrhizae: a proposed method towards standardization. New Phytol 87:63–67

    Article  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341

    Article  PubMed  CAS  Google Scholar 

  • Brechenmacher L, Lee J, Sachdev S, Song Z, Nguyen THN, Joshi T, Oehrle N, Libault M, Mooney B, Xu D, Cooper B, Stacey G (2009) Establishment of a protein reference map for soybean root hair cells. Plant Physiol 149:670–682

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Brown LK, George TS, Barrett GE, Hubbard SF, White PJ (2013) Interactions between root hair length and arbuscular mycorrhizal colonisation in phosphorus deficient barley (Hordeum vulgare). Plant Soil 372:195–205

    Article  CAS  Google Scholar 

  • Brown LK, George TS, Thompson JA, Wright G, Lyon J, Dupuy L, Hubbard SF, White PJ (2012) What are the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)? Ann Bot 110:319–328

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen BD, Roos P, Borggaard OK, Zhu YG, Jakobsen I (2005) Mycorrhiza and root hairs in barley enhance acquisition of phosphorus and uranium from phosphate rock but mycorrhiza decreases root to shoot uranium transfer. New Phytol 165:591–598

    Article  PubMed  CAS  Google Scholar 

  • Davies FT, Potter JR, Linderman RG (1993) Drought resistance of mycorrhizal pepper plants independent of leaf P-concentration response in gas exchange and water relations. Physiol Plant 87:45–53

    Article  CAS  Google Scholar 

  • Davies FT, Potter JR, Linderman RG (1992) Mycorrhiza and repeated drought exposure affect drought resistance and extraradical hyphae development of pepper plants independent of plant size and nutrient content. J Plant Physiol 139:289–294

    Article  Google Scholar 

  • Denby K, Gehring C (2005) Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. Trends Biotechnol 23:547–552

    Article  PubMed  CAS  Google Scholar 

  • Duan TY, Facelli E, Smith SE, Smith FA, Nan ZB (2011) Differential effects of soil disturbance and plant residue retention on function of arbuscular mycorrhizal (AM) symbiosis are not reflected in colonization of roots or hyphal development in soil. Soil Biol Biochem 43:571–578

    Article  CAS  Google Scholar 

  • Duncan DB (1955) Multiple range and multiple F-tests. Biometrics 11:1–42

    Article  Google Scholar 

  • Gahoonia TS, Nielsen NE (2003) Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low- and high-P soils. Plant Cell Environ 26:1759–1766

    Article  CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant Soil 235:211–219

    Article  CAS  Google Scholar 

  • Gleeson SK (1993) Optimization of tissue nitrogen and root-shoot allocation. Ann Bot 71:23–31

    Article  CAS  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120:371–380

    Article  CAS  Google Scholar 

  • Jakobsen I, Chen BD, Munkvold L, Lundsgaard T, Zhu YG (2005) Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant Cell Environ 28:928–938

    Article  CAS  Google Scholar 

  • Jones HG (2007) Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance. J Exp Bot 58:119–130

    Article  PubMed  CAS  Google Scholar 

  • Jupp AP, Newman EI (1987) Morphological and anatomical effects of severe drought on the roots of Lolium Perenne L. New Phytol 105:393–402

    Article  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 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Article  Google Scholar 

  • Lan WZ, Wang W, Wang SM, Li LG, Buchanan BB, Lin HX, Gao JP, Luan S (2010) A rice high-affinity potassium transporter (HKT) conceals a calcium-permeable cation channel. Proc Natl Acad Sci U S A 107:7089–7094

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD (2013) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197:617–630

    Article  PubMed  CAS  Google Scholar 

  • Libault M, Brechenmacher L, Cheng JL, Xu D, Stacey G (2010) Root hair systems biology. Trends Plant Sci 15:641–650

    Article  PubMed  CAS  Google Scholar 

  • Loqué D, Yuan L, Kojima S, Gojon A, Wirth J, Gazzarrini S, Ishiyama K, Takahashi H, von Wirén N (2006) Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant J 48:522–534

    Article  PubMed  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 

  • Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004) Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signalling and regulation. J Exp Bot 55:1843–1849

    Article  PubMed  CAS  Google Scholar 

  • Nandy P, Das S, Ghose M, Spooner-Hart R (2007) Effects of salinity on photosynthesis, leaf anatomy, ion accumulation and photosynthetic nitrogen use efficiency in five Indian mangroves. Wetl Ecol Manag 15:347–357

    Article  CAS  Google Scholar 

  • Oldroyd GE, Downie JA (2006) Nuclear calcium changes at the core of symbiosis signaling. Curr Opin Plant Biol 9:351–357

    Article  PubMed  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedure of clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:159–161

    Article  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 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schünmann PH, Richardson AE, Smith FW, Delhaize E (2004) Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). J Exp Bot 55:855–865

    Article  PubMed  Google Scholar 

  • Schüßler A, Walker C (2010) The glomeromycota: a species list with new families and new genera 1–58. Libraries at The Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University. Available at: www.amf-phylogeny.com

  • Schweiger PF, Robson AD, Barrow NJ (1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytol 131:247–254

    Article  Google Scholar 

  • Segal E, Kushnir T, Mualem Y, Shani U (2008) Water uptake and hydraulics of the root hair rhizosphere. Vadose Zone J 7:1027–1034

    Article  Google Scholar 

  • Sheng M, Tang M, Chen H, Yang BW, Zhang FF, Huang YH (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296

    Article  PubMed  CAS  Google Scholar 

  • Subramanian KS, Charest C (1995) Influence of arbuscular mycorrhizae on the metabolism of maize under drought stress. Mycorrhiza 5:273–278

    Article  Google Scholar 

  • Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001

    Article  Google Scholar 

  • Tisdall JM (1991) Fungal hyphae and structural stability of soil. Aust J Soil Res 29:729–743

    Article  Google Scholar 

  • White RG, Kirkegaard JA (2010) The distribution and abundance of wheat roots in a dense, structured subsoil—implications for water uptake. Plant Cell Environ 33:133–148

    Article  PubMed  Google Scholar 

  • Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425

    Article  PubMed  CAS  Google Scholar 

  • Zhu CX, Song BF, Xu HW (2010) Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331:129–137

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are very grateful to Dr. Iver Jakobsen for providing barley seeds and to Dr. Erik Verbruggen for his critical reading of the manuscript. The study was financially supported by the National Natural Science Foundation of China (41371264), Knowledge Innovation Program of the Chinese Academy of Sciences (Project no. KZCX2-YW-BR-17), and the National Key Technology R&D Program (2012BAC25B03).

Author information

Authors and Affiliations

  1. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Tao Li, Xin Zhang, Yongliang Chen & Baodong Chen

  2. Guiyang College of Traditional Chinese Medicine, Guiyang, 550002, China

    Ge Lin

  3. Institute of Plant Nutrition and Resources, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China

    Shubin Zhang

Authors
  1. Tao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ge Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yongliang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shubin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Baodong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Baodong Chen.

Additional information

Tao Li and Ge Lin contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, T., Lin, G., Zhang, X. et al. Relative importance of an arbuscular mycorrhizal fungus (Rhizophagus intraradices) and root hairs in plant drought tolerance. Mycorrhiza 24, 595–602 (2014). https://doi.org/10.1007/s00572-014-0578-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-014-0578-3

Keywords

Search

Navigation