Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Plant isotopic composition provides insight into mechanisms underlying growth stimulation by AM fungi in a semiarid environment

José I. Querejeta A B C , Michael F. Allen B , María M. Alguacil A and Antonio Roldán A
+ Author Affiliations
- Author Affiliations

A Departamento de Conservación de Suelos y Aguas, Centro de Edafología y Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas (CEBAS-CSIC), PO Box 4195, Campus Universitario de Espinardo 30 100 Murcia, Spain.

B Center for Conservation Biology, The University of California, Riverside, CA 92 521, USA.

C Corresponding author. Email: querejeta@cebas.csic.es

Functional Plant Biology 34(8) 683-691 https://doi.org/10.1071/FP07061
Submitted: 9 March 2007  Accepted: 16 May 2007   Published: 23 July 2007

Abstract

We hypothesised that improved plant water status and enhanced transpiration are key mechanisms involved in plant growth stimulation by native arbuscular mycorrhizal fungi (AMF) in semiarid calcareous soils. Seedlings of the dryland shrubs Pistacia lentiscus L. and Retama sphaerocarpa L. were pre-inoculated with a mixture of eight native Glomus spp. fungi, or left un-inoculated, before transplanting into a degraded site in south-eastern Spain. Pre-inoculated Pistacia and Retama shrubs grew faster after transplanting, despite spontaneous colonisation of control plants by local AMF. Pre-inoculation enhanced shoot water content and shoot δ15N in both shrub species. Increased potassium uptake and improved water relations were key mechanisms behind growth stimulation by native AMF in Pistacia. Shoot δ18O (a proxy measure of stomatal conductance) was significantly less negative in AMF-inoculated than in control Pistacia seedlings, indicating enhanced cumulative transpiration in the former. In contrast, shoot δ18O was unaffected by AMF inoculation in Retama, a leafless leguminous shrub with photosynthetic stems. Growth stimulation by native AMF in Retama was attributed to increased phosphorus uptake, enhanced atmospheric nitrogen fixation and a largely nutrient-mediated improvement of plant water status. Shoot δ13C was not significantly influenced by AMF inoculation in either shrub species, thus suggesting roughly parallel upshifts in photosynthetic and transpiration rates which did not affect plant water use efficiency.

Additional keywords: Pistacia lentiscus, Retama sphaerocarpa, δ13C, δ15N, δ18O.


Acknowledgements

This research was supported by the EU + CICYT co-financed FEDER programme (1FD97–0507 FOREST) and by the Biocomplexity Program (DEB 9981548) of the US National Science Foundation. JI Querejeta acknowledges a Fulbright postdoctoral fellowship and a Ramón y Cajal contract from the Spanish Ministry of Education and Science.


References


Allen EB, Allen MF (1980) Natural re-establishment of vesicular-arbuscular mycorrhizae following stripmine reclamation in Wyoming. Journal of Applied Ecology 17, 139–147.
Crossref | GoogleScholarGoogle Scholar | open url image1

Allen MF (1991) ‘The ecology of mycorrhizae.’ (Cambridge University Press: Cambridge)

Allen MF, Boosalis MG (1983) Effects of 2 species of VA-mycorrhizal fungi on drought tolerances of winter wheat. New Phytologist 93, 67–76.
Crossref | GoogleScholarGoogle Scholar | open url image1

Allen MF, Smith WK, Moore TS, Christensen M (1981) Comparative water relations and photosynthesis of mycorrhizal and non-mycorrhizal Bouteola gracilis HBK Lag ex Steud. New Phytologist 88, 683–693. open url image1

Allen MF, Swenson W, Querejeta JI, Egerton-Warburton LM, Treseder KK (2003) Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi. Annual Review of Phytopathology 41, 271–303.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 3–42.
Crossref | GoogleScholarGoogle Scholar | open url image1

Azcón R, Barea JM (1997) Mycorrhizal dependency of a representative plant species in Mediterranean shrublands (Lavandula spica L.) as a key factor to its use for revegetation strategies in desertification-threatened areas. Applied Soil Ecology 7, 83–92.
Crossref | GoogleScholarGoogle Scholar | open url image1

Azcón-Aguilar C, Palenzuela J, Roldán A, Bautista R, Vallejo R, Barea JM (2003) Analysis of the mycorrhizal potential in the rhizosphere of representative plant species from desertification-threatened Mediterranean shrublands. Applied Soil Ecology 22, 29–37.
Crossref | GoogleScholarGoogle Scholar | open url image1

Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Functional Plant Biology 34, 83–94.
Crossref | GoogleScholarGoogle Scholar | open url image1

Barbour MM, Farquhar GD (2000) Relative humidity and ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves. Plant, Cell & Environment 23, 473–485.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bednarz CW, Oosterhuis DM, Evans RD (1998) Leaf photosynthesis and carbon isotope discrimination of cotton in response to potassium deficiency. Environmental and Experimental Botany 39, 131–139.
Crossref | GoogleScholarGoogle Scholar | open url image1

Caravaca F, Figueroa D, Alguacil MM, Roldán A (2003) Application of composted urban residue enhanced the performance of afforested shrub species in a degraded semiarid land. Bioresource Technology 90, 65–70.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Carpenter AT, Allen MF (1988) Responses of Hedysarum boreale Nutt to mycorrhizas and Rhizobium- Plant and soil nutrient changes in a disturbed shrub steppe. New Phytologist 109, 125–132.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cernusak LA, Arthur DJ, Pate JS, Farquhar GD (2003) Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiology 131, 1544–1554.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cernusak LA, Pate JS, Farquhar GD (2004) Oxygen and carbon isotope composition of parasitic plants and their hosts in southwestern Australia. Oecologia 139, 199–213.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. Journal of Plant Nutrition 23, 867–902. open url image1

Cooper RB, Blaser RE, Brown RH (1967) Potassium nutrition effects on net photosynthesis and morphology of alfalfa. Soil Science 31, 231–235. open url image1

De Niro MJ, Epstein S (1979) Relationship between the oxygen isotope ratios of terrestrial plant cellulose, carbon dioxide, and water. Science 204, 51–53.
Crossref | GoogleScholarGoogle Scholar | open url image1

Domingo F, Gutiérrez L, Brenner AJ, Aguilera C (2002) Limitation to carbon assimilation of two perennial shrub species in semi-arid south-east Spain. Biologia Plantarum 45, 213–220.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ehleringer JR, Philips SL, Comstock JP (1992) Seasonal variation in the carbon isotopic composition of desert plants. Functional Ecology 6, 396–404.
Crossref | GoogleScholarGoogle Scholar | open url image1

Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Plant Science 6, 121–126.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ferrol N, Calvente R, Cano C, Barea JM, Azcón-Aguilar C (2004) Analysing arbuscular mycorrhizal fungal diversity in shrub-associated resource islands from a desertification-threatened semiarid Mediterranean ecosystem. Applied Soil Ecology 25, 123–133.
Crossref | GoogleScholarGoogle Scholar | open url image1

Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–499.
Crossref | GoogleScholarGoogle Scholar | open url image1

Haase P, Pugnaire FI, Fernandez EM, Puigdefabregas J, Clark SC, Incoll LD (1996) An investigation of rooting depth of the semiarid shrub Retama sphaerocarpa (L.) Boiss. by labelling of ground water with a chemical tracer. Journal of Hydrology 177, 23–31.
Crossref | GoogleScholarGoogle Scholar | open url image1

Haase P, Pugnaire FI, Clark SC, Incoll LD (2000) Dynamics of the cohorts of cladodes and related effects on reproduction in the shrub Retama sphaerocarpa in semi-arid south-eastern Spain. Plant Ecology 146, 105–115.
Crossref | GoogleScholarGoogle Scholar | open url image1

Handley LL, Azcón R, Ruiz-Lozano JM, Scrimgeour CM (1999) Plant δ15N associated with arbuscular mycorrhization, drought and nitrogen deficiency. Rapid Communications in Mass Spectrometry 13, 1320–1324.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. Journal of Ecology 90, 371–384.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Annals of Botany 90, 37–42.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Humble GD, Raschke K (1971) Stomatal opening quantitatively related to potassium transport. Plant Physiology 48, 447–453.
PubMed |
open url image1

Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Molecular Ecology 11, 2669–2678.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jaggi M, Saurer M, Fuhrer J, Siegwolf R (2003) Seasonality of δ18O in needles and wood of Picea abies. New Phytologist 158, 51–59.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jonasson S, Medrano H, Flexas J (1997) Variation in leaf longevity of Pistacia lentiscus and its relationship to sex and drought stress inferred from leaf δ13C. Functional Ecology 11, 282–289.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jordan-Meille L, Pellerin S (2004) Leaf area establishment of a maize (Zea mays L.) field crop under potassium deficiency. Plant and Soil 265, 75–92.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 and Soil 253, 287–292.
Crossref | GoogleScholarGoogle Scholar | open url image1

Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84, 2292–2301.
Crossref |
open url image1

Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytologist 147, 233–235.
Crossref | GoogleScholarGoogle Scholar | open url image1

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. Physiologia Plantarum 119, 526–533.
Crossref | GoogleScholarGoogle Scholar | open url image1

Milla R, Palacio-Blasco S, Maestro-Martínez M, Montserrat-Marti G (2006) Phosphorus accretion in old leaves of a Mediterranean shrub growing at a phosphorus-rich site. Plant and Soil 280, 369–372.
Crossref | GoogleScholarGoogle Scholar | open url image1

Miller RM, Miller SP, Jastrow JD, Rivetta CB (2002) Mycorrhizal mediated feedbacks influence net carbon gain and nutrient uptake in Adropogon gerardii. New Phytologist 155, 149–162.
Crossref | GoogleScholarGoogle Scholar | open url image1

Querejeta JI, Barea JM, Allen MF, Caravaca F, Roldán A (2003) Differential response of δ13C and water use efficiency to arbuscular mycorrhizal infection in two aridland woody plant species. Oecologia 135, 510–515.
PubMed |
open url image1

Querejeta JI, Allen MF, Caravaca F, Roldán A (2006) Differential modulation of host plant δ13C and δ18O by native and non-native arbuscular mycorrhizal fungi in a semiarid environment. New Phytologist 169, 379–387.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Requena N, Pérez-Solís E, Azcón-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant–microbe symbioses aids restoration of desertified ecosystems. Applied and Environmental Microbiology 67, 495–498.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiologia Plantarum 95, 472–478.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ruiz-Lozano JM, Azcón R, Gómez M (1995) Effects of arbuscular-mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Applied and Environmental Microbiology 61, 456–460.
PubMed |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shearer G, Kohl DH, Virginia RA, Bryan BA, Skeeters JL, Nielsen ET, Sharifi MR, Rundel PW (1983) Estimates of N2 fixation from variation in the natural abundance of N15 in Sonoran desert ecosystems. Oecologia 56, 365–373.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sheshshayee MS, Bindumadhava H, Ramesh R, Prasad TG, Lakshminarayana MR, Udayakumar M (2005) Oxygen isotope enrichment (Δ18O) as a measure of time-averaged transpiration rate. Journal of Experimental Botany 56, 3033–3039.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stahl PD, Smith WK (1984) Effects of different geographic isolates of Glomus on the water relations of Agropyron smithii. Mycologia 76, 261–267.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tobar R, Azcón R, Barea JM (1994) Improved nitrogen uptake and transport from N15-labeled nitrate by external hyphae of arbuscular mycorrhiza under water stress conditions. New Phytologist 126, 119–122.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tsialtas JT, Handley LL, Kassioumi MT, Veresoglou DS, Gagianas AA (2001) Interspecific variation in potential water use efficiency and its relation to plant species abundance in a water limited grassland. Functional Ecology 15, 605–614.
Crossref | GoogleScholarGoogle Scholar | open url image1

Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant diversity, ecosystem variability and productivity. Nature 396, 69–72.
Crossref | GoogleScholarGoogle Scholar | open url image1

Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1999) ‘Sampling effect’, a problem in biodiversity manipulation? A reply to David A. Wardle. Oikos 87, 408–410.
Crossref | GoogleScholarGoogle Scholar | open url image1

Van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders I (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytologist 172, 739–752.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wang XF, Yakir D, Avishai M (1998) Non-climatic variations in the oxygen isotopic compositions of plants. Global Change Biology 4, 835–849.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wheeler CT, Tilak M, Scrimgeour CM, Hooker JE, Handley LL (2000) Effects of symbiosis with Frankia and arbuscular mycorrhizal fungus on the natural abundance of 15N in four species of Casuarina. Journal of Experimental Botany 51, 287–297.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1