Skip to main content
SpringerLink
Log in

Seasonal analyses of arbuscular mycorrhizae, nitrogen-fixing bacteria and growth performance of the salt marsh grass Spartina patens

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Seasonal variation of arbuscular mycorrhizal fungi (AMF) in roots of the high salt marsh plant Spartina patens, the diversity of nitrogen-fixing bacteria in the rhizosphere and plant growth performance was studied at key stages of the growing season coinciding with major plant phenological stages, i.e., vegetative growth, reproduction and senescence. AMF colonization was highest during vegetative growth, with values declining during the growing season to the same level seen at plant dormancy. AMF colonization was reduced at lower depths in the sediments where anoxic conditions were observed and in plants treated with the systemic fungicide Benomyl. Only small changes in diversity of nitrogen-fixing bacteria in general and more specifically of those belonging to the ε-subdivision of Proteobacteria were detected during the season or between treatments by PCR-RFLP of nifH gene fragments with DNA as template for amplification; however, greater seasonal changes were displayed when cDNA was used as template for amplification as a proxy for gene expression and thus active bacteria. DGGE analyses of nifH gene fragments representing nitrogen-fixing bacteria of the ε-subdivision of Proteobacteria using both using DNA and cDNA as template showed highly diverse profiles that changed during the season and in response to treatment. Seasonal changes were observed for a suite of plant growth attributes and differences were observed between treatments, with higher values generally obtained on non-treated plants compared to Benomyl-treated plants. These differences were most pronounced during vegetative growth; however, differences between non-treated and Benomyl-treated plants were reduced seasonally and disappeared by the onset of senescence. This study demonstrates seasonal changes in AMF colonization on S. patens and in the community structure of nitrogen-fixing members of the ε-subdivision of Proteobacteria in the plant root zone. Plant growth performance changed seasonally with some effects of Benomyl-treatment.

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

Similar content being viewed by others

References

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

    Google Scholar 

  • Allen MF (1996) The ecology of arbuscular mycorrhizas: a look back into the 20th Century and a peek into the 21st. Mycol Res 100:769–782

    Article  Google Scholar 

  • Allison VJ, Rajaniemi TK, Goldberg DE, Zak DR (2007) Quantifying direct and indirect effects of fungicide on an old-field plant community: an experimental approach. Plant Ecol 190:53–69

    Article  Google Scholar 

  • Ames RN, Reid CPP, Porter LK, Cambardella C (1983) Hyphal uptake and transport of nitrogen from two N-labelled sources by Glomus mosseae, a vesicular- arbusuclar mycorrhizal fungus. New Phytol 95:381–396

    Article  Google Scholar 

  • Bagwell CE, Lovell CR (2000) Microdiversity of culturable diazotrophs from the rhizoplanes of the salt marsh grasses Spartina alterniflora and Juncus roemerianus. Microb Ecol 39:128–136

    Article  CAS  PubMed  Google Scholar 

  • Bagwell CE, Piceno YM, Ashburne-Lucas A, Lovell CR (1998) Physiological diversity of the rhizosphere diazotroph assemblages of selected salt marsh grasses. Appl Environ Microbiol 64:4276–4282

    CAS  PubMed  Google Scholar 

  • Bagwell CE, Dantzler M, Bergholtz PW, Lovell CR (2001) Host-specific ecotype diversity of rhizoplane diazotrophs of the perennial glasswort Saliconia virginica and selected salt marsh grasses. Aquatic Microb Ecol 23:293–300

    Article  Google Scholar 

  • Berholz PW, Bagwell CE, Lovell CR (2001) Physiological diversity of rhizoplane diazotrophs of the saltmeadow cordgrass, Spartina patens: implications for host specific ecotypes. Microb Ecol 42:466–473

    Article  Google Scholar 

  • Bertness MD (1992) The ecology of a New England marsh. Am Sci 80:260–268

    Google Scholar 

  • Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193

    Article  Google Scholar 

  • Bohrer KE, Friese CF, Amon JP (2004) Seasonal dynamics of arbuscular mycorrhizal fungi in differing wetland habitats. Mycorrhiza 14:329–337

    Article  PubMed  Google Scholar 

  • Brundrett MC, Melville L, Peterson RL (1994) Practical methods in mycorrhiza research. Mycologue, Waterloo

    Google Scholar 

  • Burgmann H, Widmer F, Sigler WV, Zeyer J (2004) New molecular screening tools for analysis of free-living diazotrophs in soil. Appl Environ Microbiol 70:240–247

    Article  PubMed  CAS  Google Scholar 

  • Burgmann H, Meier S, Bunge M, Widmer F, Zeyer J (2005) Effects of model root exudates on structure and activity of a soil diazotroph community. Environ Microbiol 7:1711–1724

    Article  CAS  PubMed  Google Scholar 

  • Burke D, Hamerlynck EP, Hahn D (2002a) Interactions among plant species and microorganisms in salt marsh sediments. Appl Environ Microbiol 68:1157–1164

    Article  CAS  Google Scholar 

  • Burke DJ, Hamerlynck EP, Hahn D (2002b) Effect of arbuscular mycorrhizae on soil microbial populations and associated plant performance of the salt marsh grass Spartina patens. Plant Soil 239:141–154

    Article  CAS  Google Scholar 

  • Burke DJ, Hamerlynck EP, Hahn D (2003) Interactions between the salt marsh grass Spartina patens, arbuscular mycorrhizal fungi and sediment bacteria during the growing season. Soil Biol Biochem 35:501–511

    Article  CAS  Google Scholar 

  • Callaway RM (1997) Positive interactions in plant communities and the individualistic-continuum concept. Oecologia 112:143–149

    Article  Google Scholar 

  • Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004) Soil fungi alter interactions between the invader Centaurea maculosa and North American natives. Ecology 85:1062–1071

    Article  Google Scholar 

  • Casamayor EO, Massana R, Benlloch S, Ovreas L, Diez B, Goddard VJ, Gasol JM, Joint I, Rodriguez-Valera F, Pedros-Alio C (2002) Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar system. Environ Microbiol 4:338–348

    Article  PubMed  Google Scholar 

  • Cooke JC, Butler RH, Madole G (1993) Some observations on the vertical distribution of vesicular arbuscular mycorrhizae in roots of salt marsh grasses growing in saturated soils. Mycologia 84:547–550

    Article  Google Scholar 

  • Dai T, Wiegert RG (1997) A field study of photosynthetic capacity and its response to nitrogen fertilization in Spartina alterniflora. Estuar Coast Shelf Sci 45:273–283

    Article  Google Scholar 

  • Daleo P, Fanjul E, Mendez Casariego A, Silliman BR, Bertness MD, Iribarne O (2007) Ecosystem engineers activate mycorrhizal mutualism in salt marshes. Ecol Lett 10:902–908

    Article  PubMed  Google Scholar 

  • DeLaune RD, Feijtel TC, Patrick WH (1989) Nitrogen flows in a Louisiana gulf coast salt marsh: spatial considerations. Biogeochemistry 8:25–37

    Article  CAS  Google Scholar 

  • DeMars BG, Boerner REJ (1995) Mycorrhizal dynamics of three woodland herbs of contrasting phenology along topographic gradients. Am J Bot 82:1426–1431

    Article  Google Scholar 

  • Duineveld BM, Kowalchuk GA, Keijzer A, van Elsas JD, van Veen J (2001) Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl Environ Microbiol 67:172–178

    Article  CAS  PubMed  Google Scholar 

  • Dunbar J, Barns SM, Ticknor LO, Kuske CR (2002) Empirical and theoretical bacterial diversity in four Arizona soils. Appl Environ Microbiol 68:3035–3045

    Article  CAS  PubMed  Google Scholar 

  • Fitter AH, Nichols R (1988) The use of benomyl to control infection by vesicular-arbuscular mycorrhizal fungi. New Phytol 110:201–206

    Article  CAS  Google Scholar 

  • Garcia IV, Mendoza RE (2007) Arbuscular mycorrhizal fungi and plant symbiosis in a saline-sodic soil. Mycorrhiza 17:167–174

    Article  PubMed  Google Scholar 

  • Graham JH, Leonard RT, Menge JA (1981) Membrane mediated decrease in root exudation responsible for phosphorous inhibition of vesicular-arbuscular mycorrhizae formation. Plant Physiol 68:548–552

    Article  CAS  PubMed  Google Scholar 

  • Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491

    Article  CAS  PubMed  Google Scholar 

  • Grogan P, Chapin FS (2000) Nitrogen limitation of production in a Californian annual grassland: The contribution of arbuscular mycorrhizae. Biogeochemistry 49:37–51

    Article  CAS  Google Scholar 

  • Hamel C (2004) Impact of arbuscular mycorrhizal fungi on N and P cycling in the root zone. Can J Soil Sci 84:383–395

    CAS  Google Scholar 

  • Hamel C, Nesser C, Barrantes-Cartin U, Furlan V, Smith DL (1991) Endomycorrhizal fungal species mediate 15N transfer from soybean to maize in non-fumigated soils. Plant Soil 138:41–47

    Article  CAS  Google Scholar 

  • Hart MR, Brookes PC (1996) Soil microbial biomass and mineralization of soil organic matter after 19 years of cumulative field applications of pesticides. Soil Biol Biochem 28:1641–1649

    Article  CAS  Google Scholar 

  • Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80:1187–1195

    Article  Google Scholar 

  • Hayman DS (1986) Mycorrhizae of nitrogen-fixing legumes. MIRCEN J 2:121–145

    Article  Google Scholar 

  • Helgason T, Merryweather JW, Young JPW, Fitter AH (2007) Specificity and resilience in the arbuscular mycorrhizal fungi of a natural woodland community. J Ecol 95:623–630

    Article  CAS  Google Scholar 

  • Hetrick BAD, Harnett DC, Wilson GWT, Gibson DJ (1994) Effects of mycorrhizae, phosphorous availability and plant density on yield relationships among competing tallgrass prairie grasses. Can J Bot 72:168–176

    Article  Google Scholar 

  • Hines ME, Knollmeyer SL, Tugel JB (1989) Sulfate reduction and other sedimentary biogeochemistry in a northern New England salt marsh. Limnol Oceanogr 34:578–590

    CAS  Google Scholar 

  • Hines ME, Evans RS, Sharak Genthner BR, Willis SG, Friedman S, Rooney-Varga JN, Devereux R (1999) Molecular phylogenetic and biogeochemical studies of sulfate-reducing bacteria in the rhizosphere of Spartina alterniflora. Appl Environ Microbiol 65:2209–2216

    CAS  PubMed  Google Scholar 

  • Hoefnagels MH, Broome S, Shafer SR (1993) Vesicular-arbuscular mycorrhizae in salt marshes in North Carolina. Estuaries 16:851–858

    Article  Google Scholar 

  • Hönerlage W, Hahn D, Zeyer J (1995) Detection of mRNA of nprM in Bacillus megaterium ATCC 14581 grown in soil by whole cell hybridization. Arch Microbiol 163:235–241

    Article  Google Scholar 

  • Howard JB, Rees DC (1996) Structural basis of biological nitrogen fixation. Chem Rev 96:2965–2982

    Article  CAS  PubMed  Google Scholar 

  • Huxman TE, Hamerlynck EP, Moore BD, Smith SD, Jordan DN, Zitzer SF, Nowak RS, Coleman JS, Seemann JR (1998) Photosynthetic down-regulation in Larrea tridentata exposed to elevated atmospheric CO2: interaction with drought under glasshouse and field (FACE) exposure. Plant Cell Environ. 21:1153–1161

    Article  Google Scholar 

  • Jacob J, Greitner C, Drake DG (1995) Acclimation of photosynthesis in relation to Rubisco and non-structural carbohydrate contents and in situ carboxylase activity in Scirpus olneyi grown in elevated CO2. Plant Cell Environ. 18:875–884

    Article  CAS  Google Scholar 

  • John MK (1979) Colorimetric determination of phosphorous in soil and plant materials with ascorbic acid. Soil Sci 109:214–220

    Google Scholar 

  • Johnstone C, Block W, Benson EE, Day JG, Staines H, Illian JB (2002) Assessing methods for collecting and transferring viable algae from Signy Island, maritime Antarctic, the United Kingdom. Polar Biol 25:553–556

    Article  Google Scholar 

  • Kisand V, Wikner J (2003) Limited resolution of 16S rDNA DGGE caused by melting properties and closely related DNA sequences. J Microbiol Meth 54:183–191

    Article  CAS  Google Scholar 

  • Knauth S, Hurek T, Brar D, Hurek B (2005) Influence of different Oryza cultivars on expression of nifH gene pools in different roots of rice. Environ Microbiol 7:1725–1733

    Article  CAS  PubMed  Google Scholar 

  • Kormanick PP, McGraw AC (1982) Quantification of vesicular-arbuscular mycorrhizas in plant roots. In: Schenck NC (ed) Methods and principals of mycorrhizal research. The American Phytopathological Society, St Paul, pp 37–45

    Google Scholar 

  • Krom MD, Davison P, Zhang H, Davison W (1994) High-resolution pore-water sampling with a gel sampler. Limnol Oceanogr 39:1967–1972

    Article  Google Scholar 

  • Lovell CR, Friez M, Longshore J, Bagwell CE (2001) Recovery and phylogenetic analysis of nifH sequences from diazotrophic bacteria associated with dead aboveground biomass of Spartina alterniflora. Appl Environ Microbiol 67:5308–5314

    Article  CAS  PubMed  Google Scholar 

  • Lugo MA, Gonzales Maza ME, Cabello MN (2003) Arbuscular mycorrhizal fungi in a mountain grassland II: seasonal variation of colonization studied, along with its relation to grazing and metabolic host type. Mycologia 95:407–415

    Article  Google Scholar 

  • Maddison WP, Maddison DR (1999) MacClade: Analysis of phylogeny and character evolution. Sinauer, Sunderland

    Google Scholar 

  • Mårtensson L, Diez B, Wartiainen I, Zheng W, El-Shehawy R and Rasmussen U (2009) Diazotrophic diversity, nifH gene expression and nitrogenase activity in a rice paddy field in Fujian, China. Plant Soil. doi:10.1007/s11104-11009-19970-11108

  • McClung CR, van Berkum P, Davis RE, Sloger C (1983) Enumeration and localization of N2-fixing bacteria associated with roots of Spartina alterniflora Loisel. Appl Environ Microbiol 45:1914–1920

    PubMed  CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Miller SP (2000) Arbuscular mycorrhizal colonization of semi-aquatic grasses along a wide hydrologic gradient. New Phytol 145:145–155

    Article  Google Scholar 

  • Mortimer RJG, Krom MD, Hall POJ, Hulth S, Ståhl H (1998) Use of gel probes for the determination of high resolution solute distributions in marine and estuarine pore waters. Mar Chem 63:119–129

    Article  CAS  Google Scholar 

  • Mortimer RJG, Davey JT, Krom MD, Watson PG, Frickers PE, Clifton RJ (1999) The effect of macrofauna on porewater profiles and nutrient fluxes in the intertidal zone of the Humber estuary. Estuar Coast Shelf Sci 48:683–699

    Article  CAS  Google Scholar 

  • Nicol GW, Glover A, Prosser JI (2003) Spatial analysis of archaeal community structure in grassland soil. Appl Environ Microbiol 69:7420–7429

    Article  CAS  PubMed  Google Scholar 

  • Patriquin DG, Keddy C (1978) Nitrogenase activity (acetylene reduction) in a Nova Scotian salt marsh: its association with angiosperms and the influence of some edaphic factors. Aquat Bot 4:227–244

    Article  CAS  Google Scholar 

  • Paul EA, Clark FE (1996) Soil microbiology and biochemistry. Academic, New York

    Google Scholar 

  • Piceno YM, Noble PA, Lovell CR (1999) Spatial and temporal assessment of diazotroph assemblage composition in vegetated salt marsh sediments using denaturing gradient gel electrophoresis analysis. Microb Ecol 38:157–167

    Article  CAS  PubMed  Google Scholar 

  • Piceno YM, Lovell CR (2000a) Stability in natural bacterial communties: I. Nutrient addition effects on rhizosphere diazotroph assemblage composition. Microb Ecol 39:32–40

    Article  CAS  Google Scholar 

  • Piceno YM, Lovell CR (2000b) Stability in natural bacterial communties: II. Plant resource allocation effects on rhizosphere diazotroph assemblage composition. Microb Ecol 39:41–48

    Article  CAS  Google Scholar 

  • Poly F, Monrozier LJ, Bally R (2001a) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103

    Article  CAS  Google Scholar 

  • Poly F, Ranjard L, Nazaret S, Gourbiere F, Monrozier LJ (2001b) Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Appl Environ Microbiol 67:2255–2262

    Article  CAS  Google Scholar 

  • Rasmussen T, Henry RJ (1990) Starch determination in horticultural plant material by enzymic-colorimetric procedure. J Sci Food Agric 52:159–170

    Article  CAS  Google Scholar 

  • Rooney-Varga JN, Devereux R, Evans RS, Hines ME (1997) Seasonal changes in relative abundance of uncultivated sulfate-reducing bacteria in a salt marsh sediment and the rhizosphere of Spartina alterniflora. Appl Environ Microbiol 63:3895–3901

    CAS  PubMed  Google Scholar 

  • Rozema J, Arp W, van Diggelen J, van Esbroek M, Broekman R, Punte H (1986) Occurrence and ecological significance of vesicular arbuscular mycorrhiza in the salt marsh environment. Acta Botan Neerlandia 35:457–467

    Google Scholar 

  • Sage RF, Pearcy RW (1987) The nitrogen use efficiency of C3 and C4 plants. II. Leaf nitrogen effects on the gas exchange characteristics of Chenopdium album (L.) and Amaranthus retroflexus (L.). Plant Physiol 84:954–963

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Schmidt IK, Ruess L, Bååth E, Michelsen A, Ekelund F, Jonasson S (2000) Long-term manipulation of microbes and microfauna of two subarctic heaths by addition of fungicide, bactericide, carbon and fertilizer. Soil Biol Biochem 32:707–720

    Article  CAS  Google Scholar 

  • Smart RM, Barko JW (1980) Nitrogen nutrition and salinity tolerance of Distichlis spicata and Spartina alterniflora. Ecology 61:630–638

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Smith MD, Hartnett DC, Wilson GWT (1999) Interacting influence of mycorrhizal symbiosis and competition on plant diversity in tallgrass prairie. Oecologia 121:574–582

    Article  Google Scholar 

  • Smith MD, Hartnett DC, Rice CW (2000) Effects of long-term fungicide applications on microbial properties in tallgrass prairie soil. Soil Biol Biochem 32:935–946

    Article  CAS  Google Scholar 

  • Stadden PL, Fitter AH, Robinson D (1999) Effects of mycorrhizal colonization and elevated atmospheric carbon dioxide on carbon fixation and below-ground carbon partitioning in Plantago lanceolata. J Exper Bot 50:853–860

    Article  Google Scholar 

  • Stumm W, Morgan JJ (1996) Aquatic chemistry. Wiley, New York

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sinauer, Sunderland

  • Teske A, Wawer C, Muyzer G, Ramsing NB (1996) Distribution of sulfate-reducing bacteria in a stratified fjord (Mariager Fjord, Denmark) as evaluated by most-probable-number counts and denaturing gradient gel electrophoresis of PCR-amplified ribosomal DNA fragments. Appl Environ Microbiol 62:1405–1415

    CAS  PubMed  Google Scholar 

  • van Duin W, Rozema J, Ernst WHO (1989) Seasonal and spatial variation in the occurrence of vesicular-arbuscular mycorrhizae in salt marsh plants. Agricult Ecosyst Environ 29:107–110

    Article  Google Scholar 

  • van Hoewyk D, Wigand C, Groffman PM (2001) Endomycorrhizal colonization of Dasiphora floribunda, a native species of calcareous wetlands in eastern New York state, USA. Wetlands 21:431–436

    Article  Google Scholar 

  • Von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry and of photosynthesis and gas exchange of leaves. Planta 153:367–387

    Article  Google Scholar 

  • Walker LR, Chapin FS (1987) Interactions among processes controlling successional change. Oikos 50:131–135

    Article  Google Scholar 

  • Wartiainen I, Eriksson T, Zheng W, Rasmussen U (2008) Variation in the active diazotrophic community in rice paddy-nifH PCR-DGGE analysis of rhizosphere and bulk soil. Appl Soil Ecol 39:65–75

    Article  Google Scholar 

  • Welsh A, Burke DJ, Hahn D (2007) Analysis of nitrogen-fixing members of the ε-subclass of Proteobacteria in salt marsh sediments. Appl Environ Microbiol 73:7747–7752

    Article  CAS  PubMed  Google Scholar 

  • White DS, Howes BL (1994) Translocation, remineralization, and turnover of nitrogen in the roots and rhizomes of Spartina alterniflora. Am J Bot 81:1225–1234

    Article  CAS  Google Scholar 

  • Whiting G, Gandy EL, Yoch DC (1986) Tight coupling of root-associated nitrogen fixation and plant photosynthesis in the salt marsh grass Spartina alterniflora and carbon dioxide enhancement of nitrogenase activity. Appl Environ Microbiol 52:108–113

    CAS  PubMed  Google Scholar 

  • Widmer F, Shaffer BT, Porteous L, Seidler RJ (1999) Analysis of nifH gene pool complexity in soil and litter at a Douglas fir forest site in the Oregon Cascade mountain range. Appl Environ Microbiol 65:374–380

    CAS  PubMed  Google Scholar 

  • Wilson GWT, Hartnett DC, Smith MD, Kobbeman K (2001) Effects of mycorrhizae on growth and demography of tallgrass prairie forbs. Am J Bot 88:1452–1457

    Article  Google Scholar 

  • Wright DP, Scholes JD, Read DJ (1998) Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21:209–216

    Article  Google Scholar 

  • Zani S, Mellon MT, Collier JL, Zehr JP (2000) Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR. Appl Environ Microbiol 66:3119–3124

    Article  CAS  PubMed  Google Scholar 

  • Zar JH (1998) Biostatistical analysis. Prentice Hall, Engelwood Cliffs

    Google Scholar 

Download references

Acknowledgements

These studies were supported, in part, by the New Jersey Institute of Technology under Grant No 421230, a Tibor T. Polgar Fellowship of the Hudson River Foundation, and the National Science Foundation (GK-12 grant No. 0742306).

Author information

Authors and Affiliations

  1. Department of Biology, Texas State University, 601 University Drive, San Marcos, TX, 78666, USA

    Allana K. Welsh & Dittmar Hahn

  2. The Holden Arboretum, 9500 Sperry Road, Kirtland, OH, 44094, USA

    David J. Burke

  3. USDA-ARS Southwest Watershed Research Center, 2000 E. Allen Rd., Tucson, AZ, 85719, USA

    Erik P. Hamerlynck

Authors
  1. Allana K. Welsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David J. Burke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erik P. Hamerlynck
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dittmar Hahn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dittmar Hahn.

Additional information

Responsible Editor: Timothy Richard Cavagnaro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Welsh, A.K., Burke, D.J., Hamerlynck, E.P. et al. Seasonal analyses of arbuscular mycorrhizae, nitrogen-fixing bacteria and growth performance of the salt marsh grass Spartina patens . Plant Soil 330, 251–266 (2010). https://doi.org/10.1007/s11104-009-0197-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-0197-5

Keywords

Search

Navigation