Skip to main content

Host Response to Osmotic Stresses: Stomatal Behaviour and Water Use Efficiency of Arbuscular Mycorrhizal Plants

  • Chapter
  • First Online:
Book cover Arbuscular Mycorrhizas: Physiology and Function

Abstract

Arbuscular mycorrhizal (AM) symbiosis can protect the host plants against the detrimental effects of the water deficit caused by osmotic stresses such as drought and salinity. Stomatal conductance (gs) and water use efficiency (WUE) are among the most studied water relations parameters in the mycorrhizal literature, since they are considered critical to the long-term performance of host plants in semiarid environments. Mycorrhizal effects on gs have been observed in about 50% of experiments involving AM and nonAM plants of similar size. In fact, gs rates usually are higher in AM than in nonAM plants, which implies that AM plants have a lower resistance to vapour transfer from inside the leaves to the atmosphere. AM and nonAM plants have also shown different critical points or thresholds of stomatal behaviour during drought episodes. The higher gs rates in AM plants have been associated with lower xylem-sap abscisic acid (ABA) and lower ABA fluxes to leaves in AM plants. On the other hand, it has been suggested that extraradical hyphae or increased root branching may allow mycorrhizal roots to better explore a particular soil volume, extending soil water depletion zones and giving a mycorrhizal root system more access to available water. In addition, it has been estimated that about half of the promotion of gs by AM fungi can be attributable to the soil colonization by AM fungi. Nevertheless, these results can vary when the host plant shows a water conservative strategy. Moreover, different AM fungal species have been shown to modulate also differently the physiological response, including gs, of host plant to drought. The AM influence on gs can also be modulated by environmental conditions such as irradiance, air temperature or leaf temperature. There are also several reports in the literature showing an increase of plant WUE by the AM symbiosis either under well watered or under osmotic stress conditions. The effects of AM symbiosis on WUE depend on the fungal species involved, without a correlation with the percentage of root infection. These effects have been rather related to higher net photosynthetic rate and optimal quantum yield of photosystem II in AM plants than in nonAM ones and with enhanced activities of carbon assimilatory enzymes such as Rubisco. In any case, specific studies dealing with the effect of AM symbiosis on leaf morphology are needed in order to ascertain how these parameters influence the WUE of the host plant.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ABA:

Abscisic acid

AM:

Arbuscular mycorrhiza

AMF:

Arbuscular mycorrhizal fungus

gs :

Stomatal conductance

LAR:

Leaf area ratio

NAR:

Net assimilation rate

QY:

Optimal quantum yield of photosystem II

SLW:

Specific leaf weight

Ψ:

Water potential

WUE:

Water use efficiency

References

  • Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, Cambridge

    Google Scholar 

  • Allen MF, Boosalis MG (1983) Effects of two species of VA mycorrhizal fungi on drought tolerance of winter wheat. New Phytol 93:67–76

    Article  Google Scholar 

  • Araus JL, Bort J, Steduto P, Villegas D, Royo C (2003) Breeding cereals for Mediterranean conditions: ecophysiology clues for biotechnology application. Ann Appl Biol 142:129–141

    Article  Google Scholar 

  • Aroca R, Irigoyen JJ, Sánchez-Díaz M (2003) Drought enhances maize chilling tolerance II. Photosynthetic traits and protective mechanisms against oxidative stress. Physiol Plant 117:540–549

    Article  CAS  PubMed  Google Scholar 

  • Aroca R, Tognoni F, Irigoyen JJ, Sánchez-Díaz M, Pardossi A (2001) Different root low temperature response of two maize genotypes differing in chilling sensitivity. Plant Physiol Biochem 39:1067–1073

    Article  CAS  Google Scholar 

  • Augé RM (2000) Stomatal behavior of arbuscular mycorrhizal plants. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, The Netherlands, pp. 201–237. ISBN 0-7923-6444-9

    Chapter  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 

  • Augé RM, Duan X (1991) Mycorrhizal fungi and nonhydraulic root signals of soil drying. Plant Physiol 97:821–824

    Article  PubMed  Google Scholar 

  • Augé RM, Duan X, Ebel RC, Stodola AJ (1994) Nonhydraulic signaling of soil drying in mycorrhizal maize. Planta 193:74–82

    Article  Google Scholar 

  • Augé RM, Foster JG, Loescher WH, Stodola AW (1992a) Symplastic sugar and free amino acid molality of Rosa roots with regard to mycorrhizal colonization and drought. Symbiosis 12:1–17

    Google Scholar 

  • Augé RM, Moore JL, Sylvia DM, Cho K (2004a) Mycorrhizal promotion of host stomatal conductance in relation to irradiance and temperature. Mycorrhiza 14:85–92

    Article  PubMed  Google Scholar 

  • Augé RM, Schekel KA, Wample RL (1986) Osmotic adjustment in leaves of VA mycorrhizal nonmycorrhizal rose plants in response to drought stress. Plant Physiol 82:765–770

    Article  PubMed  Google Scholar 

  • Augé RM, Stodola AJ, Brown MS, Bethlenfalvay GJ (1992b) Stomatal response of mycorrhizal cowpea and soybean to short-term osmotic stress. New Phytol 120:117–125

    Article  Google Scholar 

  • Augé RM, Stodola AJ, Ebel RC, Duan XR (1995) Leaf elongation and water relations of mycorrhizal sorghum in response to partial soil drying: two Glomus species at varying phosphorus fertilization. J Exp Bot 46:297–307

    Article  Google Scholar 

  • Augé RM, Stodola AW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97

    Article  Google Scholar 

  • Augé RM, Sylvia DM, Park SJ, Buttery BR, Saxton AM, Moore JL, Cho K (2004b) Partitioning mycorrhizal influence on water relations of Phaseolus vulgaris into soil and plant components. Can J Bot 82:503–514

    Article  Google Scholar 

  • Augé RM, Toler HD, Moore JL, Cho K, Saxton AM (2007) Comparing contributions of soil versus root colonization to variations in stomatal behavior and soil drying in mycorrhizal Sorghum bicolor and Cucurbita pepo. J Plant Physiol 164:1289–1299

    Article  PubMed  Google Scholar 

  • Augé RM, Toler HD, Sams CE, Nasim G (2008) Hydraulic conductance and water potential gradients in squash leaves showing mycorrhiza-induced increases in stomatal conductance. Mycorrhiza 18:115–121

    Article  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Berta G, Trotta A, Fusconi A, Hooker JE, Munro M, Atkinson D, Giovannetti M, Morini S, Fortuna P, Tisserant B, Gianinazzi-Pearson V, Gianinazzi S (1995) Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. Tree Physiol 15:281–293

    Article  PubMed  Google Scholar 

  • Blum A (2005) Drought resistance, water-use efficiency, and yield potential – are they compatible, dissonant, or mutually exclusive? Aust J Agric Res 56:1159–1168

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bray SR, Kitajima K, Sylvia DM (2003) Mycorrhizae differentially alter growth, physiology, and competitive ability of an invasive shrub. Ecol Appl 13:565–574

    Article  Google Scholar 

  • Bryla DR, Duniway JM (1998) The influence of the mycorrhiza Glomus etunicatum on drought acclimation in safflower and wheat. Physiol Plant 104:87–96

    Article  CAS  Google Scholar 

  • Caravaca F, Díaz E, Barea JM, Azcón-Aguilar C, Roldán A (2003) Photosynthetic and transpiration rates of Olea europaea subsp. sylvestris and Rhamnus lycioides as affected by water deficit and mycorrhiza. Biol Plant 46:637–639

    Article  Google Scholar 

  • Cho K, Toler HD, Lee J, Ownley BH, Jean C, Stutz JC, Moore JL, Augé RM (2006) Mycorrhizal symbiosis and response of sorghum plants to combined drought and salinity stresses. J Plant Physiol 163:517–528

    Article  CAS  PubMed  Google Scholar 

  • Craufurd PQ, Wheeler TR, Ellis RH, Summerfield RJ, Williams JH (1999) Effect of temperature and water deficit on water-use efficiency, carbon isotope discrimination, and specific leaf area in peanut. Crop Sci 39:136–142

    Article  Google Scholar 

  • Davies WJ, Tardieu F, Trejo CL (1994) How do chemical signals work in plants that grow in drying soil? Plant Physiol 104:309–314

    CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Druge U, Schonbeck F (1992) Effect of vesicular–arbuscular mycorrhizal infection on transpiration, photosynthesis and growth of flax (Linum usitatissimum L.) in relation to cytokinin levels. J Plant Physiol 141:40–48

    Article  Google Scholar 

  • Duan X, Neuman DS, Reiber JM, Green CD, Saxton AM, Augé RM (1996) Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 47:1541–1550

    Article  CAS  Google Scholar 

  • Ebel RC, Duan X, Still DW, Augé RM (1997) Xylem sap abscisic acid concentration and stomatal conductance of mycorrhizal Vigna unguiculata in drying soil. New Phytol 135:755–761

    Article  CAS  Google Scholar 

  • Ebel RC, Welbaum GE, Gunatilaka M, Nelson T, Augé RM (1996) Arbuscular mycorrhizal symbiosis and nonhydraulic signaling of soil drying in Vigna unguiculata (L.) Walp. Mycorrhiza 6:119–127

    Article  Google Scholar 

  • Estrada-Luna AA, Davies FT Jr, Egilla JN (2000) Mycorrhizal fungi enhancement of growth and gas exchange of micropropagated guava plantlets (Psidium guajava L.) during ex vitro acclimatization and plant establishment. Mycorrhiza 10:1–8

    Article  CAS  Google Scholar 

  • Franks P (2006) Higher rates of leaf gas exchange are associated with higher leaf hydrodynamic pressure gradients. Plant Cell Environ 29:584–592

    Article  PubMed  Google Scholar 

  • Ge Y, Chang J, Li WC, Sheng HY, Yue CL, Shan GYS (2003) Effect of soil moisture on the gas exchange of Changium smyrniodes and Anthriscus sylvestris. Biol Plant 47:605–608

    Article  Google Scholar 

  • Ghannoum O, von Caemmerer S, Conroy JP (2001) Carbon and water economy of australian NAD-ME and NADP-ME C-4 grasses. Aust J Plant Physiol 28:213–223

    CAS  Google Scholar 

  • Goicoechea N, Antolin MC, Sánchez-Díaz M (1997) Gas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought. Physiol Plant 100:989–997

    Article  CAS  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 

  • Green CD, Stodola A, Augé RM (1998) Transpiration of detached leaves from mycorrhizal and nonmycorrhizal cowpea and rose plants given varying abscisic acid, pH, calcium and phosphorus. Mycorrhiza 8:93–99

    Article  CAS  Google Scholar 

  • Hardie K (1985) The effect of removal of extraradical hyphae on water uptake by vesicular-arbuscular mycorrhizal plants. New Phytol 101:677–684

    Article  Google Scholar 

  • Kaya C, Higgs D, Kirnak H, Tas I (2003) Mycorrhizal colonisation improves fruit yield and water use efficiency in watermelon (Citrullus lanatus Thunb.) grown under well-watered and water stressed conditions. Plant Soil 253:287–292

    Article  CAS  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  CAS  PubMed  Google Scholar 

  • Khan IA, Ayub N, Mirza SN, Nizami SN, Azam M (2008) Yield and water use efficiency (WUE) of Cenchrus ciliaris as influenced by vesicular arbuscular mycorrhizae (VAM). Pak J Bot 40:931–937

    Google Scholar 

  • Klingeman WE, van Iersel MW, Kang JG, Augé RM, Moore JL, Flanagan PC (2005) Whole-plant gas exchange measurements of mycorrhizal ‘Iceberg’ roses exposed to cyclic drought. Crop Protect 24:309–317

    Article  Google Scholar 

  • Kothari SK, Marschner H, George E (1990) Effect of VA mycorrhizal fungi and rhizosphere microorganisms on root and shoot morphology, growth and water relations in maize. New Phytol 116:303–311

    Article  Google Scholar 

  • Kramer PJ, Boyer JS (1997) Water relations of plants and soils. Academic, San Diego, CA

    Google Scholar 

  • Kubikova E, Moore JL, Ownlew BH, Mullen MD, Augé RM (2001) Mycorrhizal impact on osmotic adjustment in Ocimum basilicum during a lethal drying episode. J Plant Physiol 158:1227–1230

    Article  CAS  Google Scholar 

  • Loreto F, Centritto M (2008) Leaf carbon assimilation in a water-limited world. Plant Biosyst 142:154–161

    Article  Google Scholar 

  • Lovelock CE, Kyllo D, Winter K (1996) Growth responses to vesicular-arbuscular mycorrhizae and elevated CO2 in seedlings of a tropical tree, Beislchmiedia pendula. Funct Ecol 10:662–667

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Masumoto C, Ishii T, Hatanaka T, Uchida N (2005) Mechanisms of high photosynthetic capacity in BC2F4 lines derived from a cross between Oryza sativa and wild relatives O-rufipogon. Plant Prod Sci 8:539–545

    Article  CAS  Google Scholar 

  • Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31:203–216

    Article  Google Scholar 

  • Munné-Bosch S, Nogués S, Alegre L (1998) Daily patterns of photosynthesis of two Mediterranean Schrubs response to water deficit. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer, Dordrecht, pp 4015–4018

    Google Scholar 

  • Osundina M (1995) Responses of seedlings of Parkia biglobes (African locust bean) to drought and inoculation with vesicular-arbuscular mycorrhiza. Nigerian J Bot 8:1–10

    Google Scholar 

  • Poorter H, Remkes C (1990) Leaf-area ratio and net assimilation rate of 24 wild-species differing in relative growth-rate. Oecologia 83:553–559

    Article  Google Scholar 

  • Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143

    Article  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Querejeta JI, Allen MF, Caravaca F, Roldan A (2006) Differential modulation of host plant delta 13C and delta 18O by native and nonnative arbuscular mycorrhizal fungi in a semiarid environment. New Phytol 169:379–387

    Article  CAS  PubMed  Google Scholar 

  • Querejeta JI, Barea JM, Allen MF, Caravaca F, Roldan A (2003) Differential response of delta 13C and water use efficiency to arbuscular mycorrhizal infection in two aridland woody plant species. Oecologia 135:510–515

    PubMed  Google Scholar 

  • Rood SB, Braatne JH, Hughes FMR (2003) Ecophysiology of riparian cottonwoods: stream flow dependency, water relations and restoration. Tree Physiol 23:1113–1124

    Article  PubMed  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, 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, Azcón R, Gómez M (1995a) Effects of arbuscular mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61:456–460

    CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Gómez M, Azcón R (1995b) 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 L. plants subjected to drought stress. New Phytol 134:327–333

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151:493–502

    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 

  • Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125:350–357

    Article  Google Scholar 

  • Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Cur Op Biotechnol 14:194–199

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Songsri P, Jogloy S, Holbrook CC, Kesmala T, VoraSoot N, Akkasaeng C, Patanothai A (2009) Association of root, specific leaf area, and SPAD chlorophyll meter reading to water use efficiency of peanut under different available soil water. Agric Water Manage 96:790–798

    Article  Google Scholar 

  • Tambussi EA, Bort J, Araus JL (2007) Water use efficiency in C3 cereals under Mediterranean conditions: a review of physiological aspects. Ann Appl Biol 150:307–321

    Article  Google Scholar 

  • Valentine AJ, Mortimer PE, Lintnaar A, Borgo R (2006) Drought responses of arbuscular mycorrhizal grapevines. Symbiosis 41:127–133

    CAS  Google Scholar 

  • van der Heijden MGA (2004) Arbuscular mycorrhizal fungi as support systems for seedling establishment in grasslands. Ecol Lett 7:293–303

    Article  Google Scholar 

  • Varma A (2008) Mycorrhiza. State of the art, genetics and molecular biology, Eco-funcion, biotecnology, eco-physiology, structure and systematics, 3rd edn. Springer, Berlin Heidelberg

    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  CAS  PubMed  Google Scholar 

  • Zhu JK, Hasegawa PM, Bressan R (1997) Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci 16:253–277

    CAS  Google Scholar 

Download references

Acknowledgments

The work was supported by a grant from Ministerio de Ciencia e Inovación, Spain (project AGL2008-00898).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Manuel Ruiz-Lozano .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Ruiz-Lozano, J.M., Aroca, R. (2010). Host Response to Osmotic Stresses: Stomatal Behaviour and Water Use Efficiency of Arbuscular Mycorrhizal Plants. In: Koltai, H., Kapulnik, Y. (eds) Arbuscular Mycorrhizas: Physiology and Function. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9489-6_11

Download citation

Publish with us

Policies and ethics