Skip to main content
SpringerLink
Log in

Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis

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

Abstract

Despite a large body of literature that describes the effects of arbuscular mycorrhizal colonization on plant response to water deficit, reviews of these works have been mainly in narrative form, and it is therefore difficult to quantify the magnitude of the effect. We performed a meta-analysis to examine the effect of mycorrhizal colonization on growth and yield of plants exposed to water deficit stress. Data were compared in the context of annual vs. perennial plants, herbaceous vs. woody plants, field vs. greenhouse conditions, degree of stress, functional group, regions of plant growth, and mycorrhizal and host species. We found that, in terms of biomass measurements, mycorrhizal plants have better growth and reproductive response under water stress compared to non-mycorrhizal plants. When variables such as habit, life cycle, or water stress level are considered, differences in mycorrhizal effect on plant growth between variables are observed. While growth of both annual and perennial plants is improved by symbiosis, perennials respond more favorably to colonization than annuals. Overall, our meta-analysis reveals a quantifiable corroboration of the commonly held view that, under water-deficit conditions, plants colonized by mycorrhizal fungi have better growth and reproductive response than those that are not.

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
Fig. 7
Fig. 8

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Auge RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97. doi:10.1023/a:1004891210871

    Article  CAS  Google Scholar 

  • Beare MH, Hendrix PF, Coleman DC (1994) Water-stable aggregates and organic matter fractions in conventional-tillage and no-tillage soils. Soil Sci Soc Am J 58:777–786

    Article  Google Scholar 

  • Bolgiano NC, Safir GR, Warncke DD (1983) Mycorrhizal infection and growth of onion in the field in relation to phopshorus and water availability. J Am Soc Hort Sci 108:819–825

    CAS  Google Scholar 

  • Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant–pathogen relations? Ecology 82:3057–3068. doi:10.1890/0012-9658(2001)082[3057:damfap]2.0.co;2

    Google Scholar 

  • Chiariello N, Hickman JC, Mooney HA (1982) Endomycorrhizal role for interspecific transfer of phosphorus in a community of annual plants. Science 217:941–943. doi:10.1126/science.217.4563.941

    Article  CAS  PubMed  Google Scholar 

  • Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutrition 23:867–902

    Article  CAS  Google Scholar 

  • Drijber RA, Doran JW, Parkhurst AM, Lyon DJ (2000) Changes in soil microbial community structure with tillage under long-term wheat-fallow management. Soil Biol Biochem 32:1419–1430. doi:10.1016/s0038-0717(00)00060-2

    Article  CAS  Google Scholar 

  • Faber BA, Zasoski RJ, Munns DN, Shackel K (1991) A method for measuring hyphal nutrient and water uptake in mycorrhizal plants. Can J Bot 69:87–94

    Article  Google Scholar 

  • Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128:79–87

    Article  Google Scholar 

  • Graham JH, Eissenstat DM (1998) Field evidence for the carbon cost of citrus mycorrhizas. New Phytol 140:103–110. doi:10.1046/j.1469-8137.1998.00251.x

    Article  Google Scholar 

  • Hartnett DC, Samenus RJ, Fischer LE, Hetrick BAD (1994) Plant demographic responses to mycorhiza symbiosis in tallgrass prairie. Oecologia 99:21–26. doi:10.1007/bf00317079

    Article  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156. doi:10.2307/177062

    Article  Google Scholar 

  • Hempel S, Stein C, Unsicker SB, Renker C, Auge H, Weisser WW, Buscot F (2009) Specific bottom-up effects of arbuscular mycorrhizal fungi across a plant–herbivore–parasitoid system. Oecologia 160:267–277

    Article  PubMed Central  PubMed  Google Scholar 

  • Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Letters 13:394–407. doi:10.1111/j.1461-0248.2009.01430.x

    Article  Google Scholar 

  • Kogel KH, Franken P, Huckelhoven R (2006) Endophyte or parasite—what decides? Curr Opin Plant Biol 9:358–363. doi:10.1016/j.pbi.2006.05.001

    Article  PubMed  Google Scholar 

  • Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097. doi:10.1890/08-1555.1

    Article  PubMed  Google Scholar 

  • Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51:139–148. doi:10.1007/s13199-010-0083-1

    Article  Google Scholar 

  • Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol 168:189–204. doi:10.1111/j.1469-8137.2005.01490.x

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Maldonado-Mendoza I, Lopex-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544

    Article  CAS  PubMed  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizai symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Marulanda A, Barea J-M, Azcon R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Reg 28:115–124

    Article  CAS  Google Scholar 

  • Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowicz VA, Gilbert GS, Maron JL, Mitchell CE, Parker IM, Power AG, Torchin ME, Vazquez DP (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029. doi:10.1890/06-0442

    Article  PubMed  Google Scholar 

  • Mortimer PE, Archer E, Valentine AJ (2005) Mycorrhizal C costs and nutritional benefits in developing grapevines. Mycorrhiza 15:159–165. doi:10.1007/s00572-004-0317-2

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Azcon R, Gomez M (1995) Effects of arbuscular–mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61:456–460

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schussler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421. doi:10.1017/s0953756201005196

    Article  Google Scholar 

  • Trotta A, Varese GC, Gnavi E, Fusconi A, Sampo S, Berta G (1996) Interactions between the soilborne root pathogen Phytophthora nicotianae var. parasitica and the arbuscular mycorrhizal fungus Glomus mosseae in tomato plants. Plant Soil 185:199–209

    Article  CAS  Google Scholar 

Further Reading

  • Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269

    Article  PubMed  Google Scholar 

  • Al-Karaki GN, Al-Raddad A (1997) Drought stress and VA mycorrhizal fungi effects on growth and nutrient uptake of two wheat genotypes differing in drought resistance. Crop Res (Hisar) 13:245–257

    Google Scholar 

  • Al-Karaki GN, Clark RB (1999) Varied rates of mycorrhizal inoculum on growth and nutrient acquisition by barley grown with drought stress. J Plant Nutrition 22:1775–1784

    Article  CAS  Google Scholar 

  • Alguacil MDM, Kohler J, Caravaca F, Roldan A (2009) Differential effects of Pseudomonas mendocina and Glomus intraradices on lettuce plants physiological response and aquaporin PIP2 gene expression under elevated atmospheric CO2 and drought. Microbial Ecol 58:942–951

    Article  Google Scholar 

  • Allen MF, Boosalis MG (1983) Effects of 2 species of VA-mycorrhizal fungi on drought tolerance of winter wheat. New Phytol 93:67–76

    Article  Google Scholar 

  • Asrar A-WA, Elhindi KM (2011) Alleviation of drought stress of marigold (Tagetes erecta) plants by using arbuscular mycorrhizal fungi. Saudi J Biol Sciences 18:93–98

    Article  Google Scholar 

  • Azcon R, Tobar RM (1998) Activity of nitrate reductase and glutamine synthetase in shoot and root of mycorrhizal Allium cepa—effect of drought stress. Plant Sc 133:1–8

    Article  CAS  Google Scholar 

  • Bolandnazar S (2009) The effect of mycorrhizal fungi on onion (Allium cepa L.) growth and yield under three irrigation intervals at field condition. J Food Agric & Environ 7:360–362

    Google Scholar 

  • Bryla DR, Duniway JM (1997) Effects of mycorrhizal infection on drought tolerance and recovery in safflower and wheat. Plant Soil 197:95–103

    Article  CAS  Google Scholar 

  • Busquets M, Calvet C, Camprubi A, Estaun V (2010) Differential effects of two species of arbuscular mycorrhiza on the growth and water relations of Spartium junceum and Anthyllis cytisoides. Symbiosis 52:95–101

    Article  Google Scholar 

  • Busse MD, Ellis JR (1985) Vesicular arbuscular mycorrhizal fungi (Glomus fasciculatum) influence on soybean drought tolerance in high phosphorus soil. Can J Bot 63:2290–2294

    Article  Google Scholar 

  • Caravaca F, Figueroa D, Barea JM, Azcon-Aguilar C, Roldan A (2004) Effect of mycorrhizal inoculation on nutrient acquisition, gas exchange, and nitrate reductase activity of two Mediterranean-autochthonous shrub species under drought stress. J Plant Nutrition 27:57–74

    Article  CAS  Google Scholar 

  • Celebi SZ, Demir S, Celebi R, Durak ED, Yilmaz IH (2010) The effect of arbuscular mycorrhizal fungi (AMF) applications on the silage maize (Zea mays L.) yield in different irrigation regimes. Eur J Soil Biol 46:302–305

    Article  Google Scholar 

  • Davies FT, Olalde-Portugal V, Aguilera-Gomez L, Alvarado MJ, Ferrera-Cerrato RC, Boutton TW (2002) Alleviation of drought stress of Chile ancho pepper (Capsicum annuum L. cv. San Luis) with arbuscular mycorrhiza indigenous to Mexico. Scientia Hort 92:347–359

    Google Scholar 

  • Davies FT, Svenson SE, Cole JC, Phavaphutanon L, Duray SA, OlaldePortugal V, Meier CE, Bo SH (1996) Non-nutritional stress acclimation of mycorrhizal woody plants exposed to drought. Tree Physiol 16:985–993

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Diallo AT, Samb PI, Roy-Macauley H (2001) Water status and stomatal behaviour of cowpea, Vigna unguiculata (L.) Walp, plants inoculated with two Glomus species at low soil moisture levels. Eur J Soil Biol 37:187–196

    Article  Google Scholar 

  • Ellis JR, Larsen HJ, Boosalis MG (1985) Drought resistance of wheat plants inoculated with vesicular–arbuscular mycorrhiza. Plant Soil 86:369–378

    Article  Google Scholar 

  • Fagbola O, Osonubi O, Mulongoy K, Odunfa SA (2001) Effects of drought stress and arbuscular mycorrhiza on the growth of Gliricidia sepium (Jacq). Walp, and Leucaena leucocephala (Lam.) de Wit. in simulated eroded soil conditions. Mycorrhiza 11:215–223

    Article  Google Scholar 

  • Goicoechea N, Merino S, Sanchez-Diaz M (2005) Arbuscular mycorrhizal fungi can contribute to maintain antioxidant and carbon metabolism in nodules of Anthyllis cytisoides L. subjected to drought. J Plant Physiol 162:27–35

    Article  CAS  PubMed  Google Scholar 

  • Harris-Valle C, Esqueda M, Valenzuela-Soto E, Castellanos A (2011) Tolerance to drought and salinity by Cucurbita pepo var. pepo associated with arbuscular mycorrhizal fungi of the Sonoran desert. Agrociencia 45:959–970

    Google Scholar 

  • Hetrick BAD, Kitt DG, Wilson GT (1987) Effects of drought stress on growth response in corn, Sudan grass, and big bluestem to Glomus etunicatum. New Phytol 105:403–410

    Article  Google Scholar 

  • Huang Z, Zou Z, He C, He Z, Zhang Z, Li J (2011) Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three Glomus species under water deficit. Plant Soil 339:391–399

    Article  CAS  Google Scholar 

  • Ide Franzini V, Azcon R, Latanze Mendes F, Aroca R (2010) Interactions between Glomus species and Rhizobium strains affect the nutritional physiology of drought-stressed legume hosts. J Plant Physiol 167:614–619

    Article  Google Scholar 

  • Johnson CR, Hummel RL (1985) Influence of mycorrhiza and drought stress on growth of Poncirus × Citrus seedlings. Hortscience 20:754–755

    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 

  • Kohler J, Caravaca F, Roldan A (2009) Effect of drought on the stability of rhizosphere soil aggregates of Lactuca sativa grown in a degraded soil inoculated with PGPR and AM fungi. Appl Soil Ecol 42:160–165

    Article  Google Scholar 

  • Kungu JB, Lasco RD, Dela Cruz LU, Dela Cruz RE, Husain T (2008) Effect of vesicular arbuscular mycorrhiza (VAM) fungi inoculation on coppicing ability and drought resistance of Senna spectabilis. Pakistan J Bot 40:2217–2224

    Google Scholar 

  • Kwapata MB, Hall AE (1985) Effects of moisture regime and phosphorus on mycorrhizal infection, nutrient uptake, and growth of cowpeas (Vigna unguiculata (L) Walp). Field Crops Res 12:241–250

    Article  Google Scholar 

  • Manoharan PT, Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Sharma MP, Muthuchelian K (2010) Influence of AM fungi on the growth and physiological status of Erythrina variegata Linn. grown under different water stress conditions. Eur J Soil Biol 46:151–156

    Article  Google Scholar 

  • Martin CA, Stutz JC (1994) Growth of Argentine mesquite inoculated with vesicular–arbuscular mycorrhizal fungi. J Arboric 20:134–139

    Google Scholar 

  • Mathur N, Vyas A (2000) Influence of arbuscular mycorrhiza on biomass production, nutrient uptake and physiological changes in Ziziphus mauritiana Lam. under water stress. J Arid Environ 45:191–195

    Article  Google Scholar 

  • Meddich A, Oihabi A, Abbas Y, Bizid E (2000) Effect of arbuscular mycorrhizal fungi on drought resistance of clover. Agronomie 20:283–295

    Article  Google Scholar 

  • Mena-Violante HG, Ocampo-Jimenez O, Dendooven L, Martinez-Soto G, Gonzalez-Castaneda J, Davies FT Jr, Olalde-Portugal V (2006) Arbuscular mycorrhizal fungi enhance fruit growth and quality of Chile ancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorrhiza 16:261–267

    Article  PubMed  Google Scholar 

  • Michelsen A, Rosendahl S (1990) The effect of VA mycorrhizal fungi, phosphorus and drought stress on the growth of Acacia nilotica and Leucaena leucocephala seedlings. Plant Soil 124:7–13

    Article  CAS  Google Scholar 

  • Osonubi O, Bakare ON, Mulongoy K (1992) Interactions between drought stress and vesicular–arbuscular mycorrhiza on the growth of Faidherbia albida (syn Acacia albida) and Acacia nilotica in sterile and nonsterile soils. Biol Fert Soils 14:159–165

    Article  Google Scholar 

  • Panwar JDS (1992) Effect of VAM and Azospirillum inoculation on metabolic changes and grain yield of wheat under moisture stress condition. Indian J Plant Physiol 35:157–161

    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 

  • Quilambo OA, Weissenhorn I, Doddema H, Kuiper PJC, Stulen I (2005) Arbuscular mycorrhizal inoculation of peanut in low-fertile tropical soil II. Alleviation of drought stress. J Plant Nut 28:1645–1662

    Article  CAS  Google Scholar 

  • Roldan A, Carrasco L, Caravaca F (2006) Stability of desiccated rhizosphere soil aggregates of mycorrhizal Juniperus oxycedrus grown in a desertified soil amended with a composted organic residue. Soil Biol Biochem 38:2722–2730

    Article  CAS  Google Scholar 

  • Ruizlozano JM, Gomez M, Azcon 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 

  • Runjin L (1989) Effects of vesicular–arbuscular mycorrhizas and phosphorus on water status and growth of apple. J Plant Nut 12:997–1018

    Article  Google Scholar 

  • Sanchez-Blanco MJ, Ferrandez T, Morales MA, Morte A, Alarcon 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  CAS  PubMed  Google Scholar 

  • Shamshiri MH, Mozafari V, Sedaghati E, Bagheri V (2011) Response of petunia plants (Petunia hybrida cv. Mix) inoculated with Glomus mosseae and Glomus intraradices to phosphorous and drought stress. J Agric Sci Technol 13:929–942

    Google Scholar 

  • Simpson D, Daft MJ (1990) Interactions between water-stress and different mycorrhizal inocula on plant growth and mycorrhizal development in maize and sorghum. Plant Soil 121:179–186

    Article  Google Scholar 

  • Subramanian KS, Santhanakrishnan P, Balasubramanian P (2006) Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci Hortic 107:245–253

    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 

  • Wu Q-S, Xia R-X, Zou Y-N (2006a) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 163:1101–1110

    Article  CAS  PubMed  Google Scholar 

  • Wu Q-S, Xia R-X, Zou Y-N (2008) Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. Eur J Soil Biol 44:122–128

    Article  Google Scholar 

  • Wu Q-S, Zou Y-N, Xia R-X, Wang M-Y (2007) Five Glomus species affect water relations of Citrus tangerine during drought stress. Bot Studies 48:147–154

    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 

  • Wu QS, Zou YN, Xia RX (2006b) Effects of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine) roots. Eur J Soil Biol 42:166–172

    Article  CAS  Google Scholar 

  • Zajicek JM, Hetrick BAD, Albrecht ML (1987) Influence of drought stress and mycorrhiza on growth of 2 native forbs. J Amer Soc Hortic Sci 112:454–459

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. University of Denver, Denver, CO, USA

    Benjamin Jayne & Martin Quigley

  2. F. W. Olin Hall, Room 102, 2190 E. Iliff Ave., Denver, CO, 80208-9010, USA

    Benjamin Jayne

Authors
  1. Benjamin Jayne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin Quigley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamin Jayne.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 147 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jayne, B., Quigley, M. Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis. Mycorrhiza 24, 109–119 (2014). https://doi.org/10.1007/s00572-013-0515-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-013-0515-x

Keywords

Search

Navigation