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Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels

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Abstract

Chenopods are generally regarded as non-host plants for mycorrhizal fungi and are believed not to benefit from colonization by mycorrhizal fungi. Perennial Atriplex nummularia Lindl., growing under field conditions, showed a relatively high level of colonization by mycorrhizal fungi (10–30% of root length colonized) in spring and summer. Accordingly, two glasshouse experiments were designed to assess the effects of inoculation with mycorrhizal fungi (with a single species or a mixture of different species) on growth, nutrient uptake, and rhizosphere bacterial community composition of A. nummularia at high and low salinity levels (2.2 and 12 dSm−1). Only low and patchy colonization by mycorrhizal fungi (1–2 of root length colonized) was detected in inoculated plants under glasshouse conditions which was unaffected by salinity. Despite the low colonization, inoculation increased plant growth and affected nutrient uptake at both salinity levels. The effects were higher at an early stage of plant development (6 weeks) than at a later stage (9–10 weeks). Salinity affected the bacterial community composition in the rhizosphere as examined by ribosomal intergenic spacer amplification (RISA) of 16S rDNA, digitization of the band patterns and multivariate analysis. The effects of inoculation with mycorrhizal fungi on growth of A. nummularia may be attributed to (i) direct effects of mycorrhizal fungi on plant nutrient uptake and/or (ii) indirect effects via mycorrhizal-induced changes in the bacterial community composition.

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References

  • LE Aguilera JR. Gutierrez RJ. Moreno (1998) ArticleTitleVesicular arbuscular mycorrhizae associated with saltbushes Atriplexspp. (Chenopodiaceae) in the Chilean arid zone Rev. Chil. Hist. Nat. 71 291–302

    Google Scholar 

  • Aldon EF. (1975). Endomycorrhizae enhance survival and growth of fourwing saltbush on coal mine spoils. USDA For. Serv., Rocky Mt. For. and Range Exp. Stn., Res. Note RM-294. #M1192

  • GN Al-Karaki R. Hammad M. Rusan (2001) ArticleTitleResponse of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress Mycorrhiza 11 43–47 Occurrence Handle10.1007/s005720100098 Occurrence Handle1:CAS:528:DC%2BD3MXjs1yltb0%3D

    Article  CAS  Google Scholar 

  • S Avrahami W. Liesack R. Conrad (2003) ArticleTitleEffects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers Environ. Microbiol. 5 691–705 Occurrence Handle10.1046/j.1462-2920.2003.00457.x Occurrence Handle1:CAS:528:DC%2BD3sXntFyqtr0%3D Occurrence Handle12871236

    Article  CAS  PubMed  Google Scholar 

  • B. Bago C. Azcon-Aguilar (1997) ArticleTitleChanges in rhizosphere pH induced by arbuscular mycorrhiza formation in onion␣(Allium cepa L) Z. Pflanzenern. Bodenkd 160 333–339 Occurrence Handle1:CAS:528:DyaK2sXjvFeqtLw%3D

    CAS  Google Scholar 

  • LR. Bakken (1985) ArticleTitleSeparation and purification of bacteria from soil Appl. Environ. Microbiol. 49 1482–1487

    Google Scholar 

  • JR. Barrow RE. Aaltonen (2001) ArticleTitleEvaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity Mycorrhiza 11 199–205 Occurrence Handle10.1007/s005720100111

    Article  Google Scholar 

  • JR. Barrow P. Osuna (2002) ArticleTitlePhosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt J. Arid. Environ. 51 449–459 Occurrence Handle10.1006/jare.2001.0925

    Article  Google Scholar 

  • MH Beare S Hus DC. Coleman PF. Hendrix (1997) ArticleTitleInfluences of mycelial fungi on soil aggregation and organic matter storage in conventional and no-tillage soils Appl. Soil Ecol. 5 211–219 Occurrence Handle10.1016/S0929-1393(96)00142-4

    Article  Google Scholar 

  • Caroline M., Bagyaraj DJ. (1995). Mycorrhization helper bacteria and their influence on growth of cowpea. In Mycorrhiza.: Biofertilizers for the Future. Eds. A Adholeya and S Singh. pp. 192–196. TERI, New Delhi

  • DJ Chittleborough DJ. Maschmedt MJ. Wright (1976) Soils of the Monarto Town Site CSIRO Division of Soils Adelaide 58

    Google Scholar 

  • JD. Colwell (1963) ArticleTitleThe estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales Aust. J. Exp. Agr. 3 190–197 Occurrence Handle10.1071/EA9630190 Occurrence Handle1:CAS:528:DyaF2cXnvVOhsQ%3D%3D

    Article  CAS  Google Scholar 

  • RH Copeman CA. Martin JC. Stutz (1996) ArticleTitleTomato growth in response to salinity and mycorrhizal fungi from saline or non-saline soils Hortscience 31 341–344

    Google Scholar 

  • RK Dixon HE. Garrett GS. Cox (1989) ArticleTitleBoron fertilization, vesicular–arbuscular mycorrhizal colonization and growth of Citrus Jambhiri Lush J. Plant. Nutr. 12 687–700 Occurrence Handle1:CAS:528:DyaL1MXltFCgsLY%3D

    CAS  Google Scholar 

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

    Google Scholar 

  • JH Graham RT. Leonard JA. Menge (1981) ArticleTitleMembrane-mediated decrease in root exudation responsible for inhibition of vesicular–arbuscular mycorrhiza formation Plant Physiol. 68 548–552 Occurrence Handle1:CAS:528:DyaL3MXlsVOgt7Y%3D

    CAS  Google Scholar 

  • WC. Hanson (1950) ArticleTitleThe photometric determination of phosphorus in fertilizers using the phosphovanado-molybdate complex J. Sci. Food Agr. 1 172–173 Occurrence Handle1:CAS:528:DyaG3MXhslWm

    CAS  Google Scholar 

  • XL He S. Mouratov Y. Steinberger (2002) ArticleTitleSpatial distribution and colonization of arbuscular mycorrhizal fungi under the canopies of desert halophytes Arid. Land. Res. Manage 16 149–160 Occurrence Handle10.1080/153249802317304440

    Article  Google Scholar 

  • MC. Hirrel JW. Gerdemann (1980) ArticleTitleImproved growth of onion and bell pepper in saline soils by two vesicular–arbuscular mycorrhizal fungi Soil Sci. Soc. Am. J. 44 654–658 Occurrence Handle1:CAS:528:DyaL3cXkvFCiurY%3D

    CAS  Google Scholar 

  • MC Hirrel H. Mehravaran JW. Gerdemann (1978) ArticleTitleVesicular–arbuscular mycorrhiza in Chenopodiaceae and Cruciferae: Do they occur? Can. J. Bot. 56 2813–2817

    Google Scholar 

  • I Jakobsen LK. Abbott AD. Robson (1992) ArticleTitleExternal hyphae of vesicular–arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances New Phytol. 120 509–516 Occurrence Handle1:CAS:528:DyaK38Xks12is7w%3D

    CAS  Google Scholar 

  • G-PC Johnson NC. Kenkel T. Booth (1995) ArticleTitleThe distribution and phenology of arbuscular mycorrhizae along an inland salinity gradient Can. J. Bot. 73 1318–1327

    Google Scholar 

  • RH Jongman CJF. ter Braak OFR. Van Tongeren (1995) Data Analysis in Community and Landscape Ecology Cambridge University Press Cambridge, UK

    Google Scholar 

  • S. Juniper LK. Abbott (1993) ArticleTitleVesicular–arbuscular mycorrhizas and soil salinity Mycorrhiza 4 45–57 Occurrence Handle10.1007/BF00204058

    Article  Google Scholar 

  • E Kandeler P Marschner D Tscherko TS. Gahoonia NE. Nielsen (2002) ArticleTitleMicrobial community composition and functional diversity in the rhizosphere of maize Plant Soil 238 301–312 Occurrence Handle10.1023/A:1014479220689 Occurrence Handle1:CAS:528:DC%2BD38Xitl2qsbk%3D

    Article  CAS  Google Scholar 

  • RT. Koide Z. Kabir (2000) ArticleTitleExtraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate New Phytol. 148 511–517 Occurrence Handle10.1046/j.1469-8137.2000.00776.x Occurrence Handle1:CAS:528:DC%2BD3MXpvVaktQ%3D%3D

    Article  CAS  Google Scholar 

  • G Mamatha DJ. Bagyaraj S. Jaganath (2002) ArticleTitleInoculation of field-established mulberry and papaya with arbuscular mycorrhizal fungi and a mycorrhiza helper bacterium Mycorrhiza 12 313–316 Occurrence Handle10.1007/s00572-002-0200-y Occurrence Handle1:STN:280:DC%2BD38jgsFejsg%3D%3D Occurrence Handle12466919

    Article  CAS  PubMed  Google Scholar 

  • P. Marschner K. Baumann (2003) ArticleTitleChanges in bacterial community structure induced by mycorrhizal colonization in split-root maize Plant Soil 251 279–289 Occurrence Handle1:CAS:528:DC%2BD3sXis1Citrs%3D

    CAS  Google Scholar 

  • Marschner P., Timonen S in press Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl. Soil Ecol

  • P Marschner DE. Crowley R. Lieberei (2001) ArticleTitleArbuscular mycorrhizal infection changes the bacterial 16 S rDNA community composition in the rhizosphere of maize Mycorrhiza 11 297–302 Occurrence Handle10.1007/s00572-001-0136-7 Occurrence Handle1:CAS:528:DC%2BD38Xhtlamtbw%3D

    Article  CAS  Google Scholar 

  • P Marschner G Neumann A Kania L. Weiskopf R. Lieberei (2002) ArticleTitleSpatial and temporal dynamics of the microbial community structure in the rhizosphere of cluster roots of white lupin (Lupinus albus L.) Plant Soil 246 167–174 Occurrence Handle1:CAS:528:DC%2BD38XnvFKhtbo%3D

    CAS  Google Scholar 

  • P Marschner E. Kandeler B. Marschner (2003) ArticleTitleStructure and function of the soil microbial community in a long-term fertilizer experiment Soil Biol. Biochem. 35 453–461 Occurrence Handle10.1016/S0038-0717(02)00297-3 Occurrence Handle1:CAS:528:DC%2BD3sXhvFGrt7w%3D

    Article  CAS  Google Scholar 

  • R Miethling K. Ahrends CC. Tebbe (2003) ArticleTitleStructural differences in the rhizosphere communities of legumes are not equally reflected in community-level physiological profiles Soil Biol. Biochem. 35 1405–1410 Occurrence Handle10.1016/S0038-0717(03)00221-9 Occurrence Handle1:CAS:528:DC%2BD3sXntVGnurw%3D

    Article  CAS  Google Scholar 

  • RM. Miller (1979) ArticleTitleSome occurrences of vesicular–arbuscular mycorrhiza in natural and disturbed ecosystems of Red Desert Can. J. Bot. 57 619–623

    Google Scholar 

  • Nannipieri P, Kandeler E., Ruggiero P 2002 Enzyme activities and microbiological and biochemical processes in soil. In Enzymes in the Environment. Activity, Ecology and Application. Eds. R Burns and R Dick. pp. 1–34. Marcel Dekker, USA

  • PJ O’Connor SE. Smith FA. Smith (2001) ArticleTitleArbuscular mycorrhizal associations in the southern Simpson Desert Aust. J. Bot. 49 493–499 Occurrence Handle10.1071/BT00014

    Article  Google Scholar 

  • JC Ojala WM Jarrell JA. Menge ELV. Johnson (1983) ArticleTitleInfluence of mycorrhizal fungi on the mineral nutrition and yield of onion in saline soil Agron. J. 75 255–259 Occurrence Handle1:CAS:528:DyaL3sXitFCktLs%3D

    CAS  Google Scholar 

  • T Pare EG. Gregorich SD. Nelson (2000) ArticleTitleMineralization of nitrogen from crop residues and N recovery by maize inoculated with vesicular–arbuscular mycorrhizal fungi Plant Soil 218 11–20 Occurrence Handle10.1023/A:1014958321933 Occurrence Handle1:CAS:528:DC%2BD3cXhvVGrt7s%3D

    Article  CAS  Google Scholar 

  • TC. Paulitz RG. Linderman (1989) ArticleTitleInteractions between fluorescent pseudomonads and VA mycorrhizal fungi New Phytol. 113 37–45

    Google Scholar 

  • JM. Phillips DS. Hayman (1970) ArticleTitleImproved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection Trans. Br. Mycol. Soc. 55 158–161

    Google Scholar 

  • DR Polonenko CI. Mayfield EB. Dumbroff (1986) ArticleTitleMicrobial responses to salt-induced osmotic-stress. 5. Effects of salinity on growth and displacement of soil bacteria Plant Soil 92 417–425 Occurrence Handle1:CAS:528:DyaL28XhvVehsLo%3D

    CAS  Google Scholar 

  • JA Poss E Pond JA. Menge WM. Jarrell (1985) ArticleTitleEffect of salinity on mycorrhizal onion and tomato in soil with and without additional phosphate Plant Soil 88 307–319 Occurrence Handle1:CAS:528:DyaL2MXmtFCisrw%3D

    CAS  Google Scholar 

  • M Ragab (1993) Distribution pattern of soil microbial population in salt-affected soils. In Towards the Rational Use of High Salinity Tolerance Plants, Vol. 1 H Lieth A A Al-Masoom (Eds) Deliberations about High Salinity Tolerance Plants and Ecosystems Kluwer Academic Publishers Dordrecht, Netherlands 467–472

    Google Scholar 

  • FB Reeves D Wagner T. Moorman J. Kiel (1979) ArticleTitleThe role of endomycorrhizae in revegetation practices in the semi-arid west. I. A comparison of incidence of mycorrhizae in severely disturbed vs natural environments Am. J. Bot. 66 6–13

    Google Scholar 

  • MC Rillig SF. Wright VT. Eviner (2002) ArticleTitleThe role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: Comparing effects of five plant species Plant Soil 238 325–333 Occurrence Handle10.1023/A:1014483303813 Occurrence Handle1:CAS:528:DC%2BD38Xitl2qsbc%3D

    Article  CAS  Google Scholar 

  • M Sardinha T Muller H. Schmeisky RG. Joergensen (2003) ArticleTitleMicrobial performance in soils along a salinity gradient under acidic conditions Appl. Soil Ecol. 23 237–244 Occurrence Handle10.1016/S0929-1393(03)00027-1

    Article  Google Scholar 

  • SM Schwab ELV. Johnson JA. Menge (1982) ArticleTitleThe influence of Simazine on formation of vesicular–arbuscular mycorrhizae in Chenopodium quinona Willd Plant Soil 64 283–287 Occurrence Handle1:CAS:528:DyaL38Xhslyiu74%3D

    CAS  Google Scholar 

  • A. Sengupta S. Chaudhuri (1990) ArticleTitleVesicular arbuscular mycorrhiza (VAM) in pioneer salt marsh plants of the Ganges river delta in West Bengal (India) Plant Soil 122 111–113

    Google Scholar 

  • SE Smith BJ St John FA. Smith JL. Bromley (1986) ArticleTitleEffects of mycorrhizal infection on plant growth, nitrogen and phosphorus nutrition of glasshouse-grown Allium cepaL New Phytol. 103 359–373

    Google Scholar 

  • BK Sohn KY Kim SJ Chung WS Kim SM Park JG Kang YS Rim JS Cho TH. Kim JH. Lee (2003) ArticleTitleEffect of the different timing of AMF inoculation on plant growth and flower quality of chrysanthemum Sci. Hortic. 98 173–183 Occurrence Handle10.1016/S0304-4238(02)00210-8

    Article  Google Scholar 

  • Torres J. (1990). Determinacion e identificacion de micorrizas vesiculo arbusculares (MVA) en plantas lenosas de vivero de interes para la forestacion de zonas aridas. Universidad de Chile, Chile, Memoria de Titulo Ingeniero Forestal. 115 pp

  • EW. Heijden Particlevan der (2001) ArticleTitleDifferential benefits of arbuscular mycorrhizal and ectomycorrhizal infection of Salix repens Mycorrhiza 10 185–193 Occurrence Handle10.1007/s005720000077

    Article  Google Scholar 

  • EW. Heijden Particlevan der TW. Kuyper (2003) ArticleTitleEcological strategies of ectomycorrhizal fungi of Salix repens: Root manipulation versus root replacement Oikos 103 668–680 Occurrence Handle10.1034/j.1600-0706.2003.10638.x

    Article  Google Scholar 

  • C Wamberg S Christensen I Jakobsen AK. Muller SJ. Sorensen (2003) ArticleTitleThe mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum) Soil Biol. Biochem. 35 1349–1357 Occurrence Handle10.1016/S0038-0717(03)00214-1 Occurrence Handle1:CAS:528:DC%2BD3sXntVGntbg%3D

    Article  CAS  Google Scholar 

  • SE Williams AG. Wollum EF. Aldon (1974) ArticleTitleGrowth of Atriplex canescens (Pursh) Nutt. improved by formation of vesicular–arbuscular mycorrhizae Soil Sci. Soc. Am. Proc. 38 962–965

    Google Scholar 

  • GWT. Wilson DC. Hartnett (1998) ArticleTitleInterspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie Am. J. Bot. 85 1732–1738

    Google Scholar 

  • B Yin D Crowley G Sparovek WJ. De Melo J. Borneman (2000) ArticleTitleBacterial functional redundancy along a soil reclamation gradient Appl. Environ. Microbiol. 66 4361–4365 Occurrence Handle10.1128/AEM.66.10.4361-4365.2000 Occurrence Handle1:CAS:528:DC%2BD3cXnt1Cmur4%3D Occurrence Handle11010883

    Article  CAS  PubMed  Google Scholar 

  • HH. Zahran (1997) ArticleTitleDiversity, adaptation and activity of the bacterial flora in saline environments Biol. Fert. Soils 25 211–223 Occurrence Handle10.1007/s003740050306 Occurrence Handle1:CAS:528:DyaK2sXmtV2mu7o%3D

    Article  CAS  Google Scholar 

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  1. H. R. Asghari

    Present address: Semnan Science and Technology Park, P.O. Box 36155-851, Shahrood, Iran

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  1. Soil and Land System, School of Earth and Environmental Science, Waite Campus, The University of Adelaide, SA 5005, DP 636, Australia

    H. R. Asghari, P. Marschner, S. E. Smith & F. A. Smith

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Asghari, H.R., Marschner, P., Smith, S.E. et al. Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant Soil 273, 245–256 (2005). https://doi.org/10.1007/s11104-004-7942-6

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