Skip to main content

Advertisement

Log in

Differential effects of abiotic factors and host plant traits on diversity and community composition of root-colonizing arbuscular mycorrhizal fungi in a salt-stressed ecosystem

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

Abstract

Arbuscular mycorrhizal fungi (AMF) were investigated in roots of 18 host plant species in a salinized south coastal plain of Laizhou Bay, China. From 18 clone libraries of 18S rRNA genes, all of the 22 AMF phylotypes were identified into Glomus, of which 18 and 4 were classified in group A and B in the phylogenetic tree, respectively. The phylotypes related to morphologically defined Glomus species occurred generally in soil with higher salinity. AMF phylotype richness, Shannon index, and evenness were not significantly different between root samples from halophytes vs. non-halophytes, invades vs. natives, or annuals vs. perennials. However, AMF diversity estimates frequently differed along the saline gradient or among locations, but not among pH gradients. Moreover, UniFrac tests showed that both plant traits (salt tolerance, life style or origin) and abiotic factors (salinity, pH, or location) significantly affected the community composition of AMF colonizers. Redundancy and variation partitioning analyses revealed that soil salinity and pH, which respectively explained 6.9 and 4.2 % of the variation, were the most influential abiotic variables in shaping the AMF community structure. The presented data indicate that salt tolerance, life style, and origin traits of host species may not significantly affect the AMF diversity in roots, but do influence the community composition in this salinized ecosystem. The findings also highlight the importance of soil salinity and pH in driving the distribution of AMF in plant and soil systems.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alguacil MM, Torrecillas E, Roldán A, Díaz G, Torres MP (2012) Perennial plant species from semiarid gypsum soils support higher AMF diversity in roots than the annual Bromus rubens. Soil Biol Biochem 49:132–138

    Article  CAS  Google Scholar 

  • Aliasgharzadeh N, Saleh Rastin N, Towfighi H, Alizadeh A (2001) Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz Plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza 11:119–122

    Article  CAS  Google Scholar 

  • Anderson IC, Cairney JWG (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol 6:769–779

    Article  CAS  PubMed  Google Scholar 

  • Appoloni S, Lekberg Y, Tercek MT, Zabinski CA, Redecker D (2008) Molecular community analysis of arbuscular mycorrhizal fungi in roots of geothermal soils in Yellowstone National Park (USA). Microb Ecol 56:649–659

    Article  PubMed  Google Scholar 

  • Bothe H (2012) Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis 58:7–16

    Article  Google Scholar 

  • Camprubí A, Calvet C, Cabot P, Pitet M, Estaún V (2010) Arbuscular mycorrhizal fungi associated with psammophilic vegetation in Mediterranean coastal sand dunes. J Agric Res 8:S96–S102

    Google Scholar 

  • Carvalho LM, Correia PH, Martins-Loução A (2001) Arbuscular mycorrhizal fungal propagules in a salt marsh. Mycorrhiza 14:165–170

    Article  Google Scholar 

  • Chen HH, Zhang YX, Wang XM, Ren ZY, Li L (1997) Salt-water intrusion in the lower reaches of the Weihe River, Shandong Province, China. Hydrogeol J 5:82–88

    Article  Google Scholar 

  • Cornejo P, Azcon-Aguilar C, Barea JM, Ferrol N (2004) Temporal temperature gradient gel electrophoresis (TTGE) as a tool for the characterization of arbuscular mycorrhizal fungi. FEMS Microbiol Lett 241:265–270

    Article  CAS  PubMed  Google Scholar 

  • Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    Article  CAS  PubMed  Google Scholar 

  • Gardner WH (1986) Water content. In: Klute, A. (ed). Methods of soil analysis. Part I. Physical and mineralogical methods. American Society of Agronomy, Madison

  • Greipsson S, DiTommaso A (2006) Invasive non-native plants alter the occurrence of arbuscular mycorrhizal fungi (AMF) and benefit from this association. Ecol Restor 24:236–241

    Article  Google Scholar 

  • Grzybowska B (2004) Arbuscular mycorrhiza of herbs colonizing a salt affected area near Kraków (Poland). Acta Soc Bot Polon 73:247–253

    Article  Google Scholar 

  • Han D, Kohfahl C, Song X, Xiao G, Yang J (2011) Geochemical and isotopic evidence for palaeo-seawater intrusion into the south coast aquifer of Laizhou Bay, China. Appl Geochem 26:863–883

    Article  CAS  Google Scholar 

  • Hassan SD, Boon E, St-Arnaud M, Hijri M (2011) Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Mol Ecol 16:3469–83

    Article  Google Scholar 

  • Heinemeyer A, Fitter AH (2004) Impact of temperature on the arbuscular mycorrhizal (AM) symbiosis: growth responses of the host plant and its AM fungal partner. J Exp Bot 55:525–534

    Article  CAS  PubMed  Google Scholar 

  • Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480

    Article  CAS  PubMed  Google Scholar 

  • Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938

    Article  CAS  PubMed  Google Scholar 

  • Hijri I, Sykorova Z, Oehl F, Ineichen K, Mader P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289

    Article  CAS  PubMed  Google Scholar 

  • Hildebrandt U, Janetta K, Ouziad F, Renne B, Nawrath K, Bothe H (2001) Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza 10:175–183

    Article  CAS  Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  CAS  PubMed  Google Scholar 

  • Johnson-Green P, Kenkel NC, Booth T (2001) Soil salinity and arbuscular mycorrhizal colonization of Puccinellia nuttalliana. Mycol Res 105:1094–1110

    Article  Google Scholar 

  • Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2003) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515

    Article  Google Scholar 

  • Jordan NR, Aldrich-Wolfe L, Huerd SC, Larson DL, Muehlbauer G (2012) Soil–occupancy effects of invasive and native grassland plant species on composition and diversity of mycorrhizal associations. Invasive Plant Sci Manag 5:494–505

    Article  Google Scholar 

  • Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. In: Posada D (ed) Methods in molecular biology. Springer, New York, pp 39–64

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kowalchuk GA, Gerards S, Woldendorp JW (1997) Detection and characterization of fungal infections of Ammophila arenaria (marram grass) roots by denaturing gradient gel electrophoresis of specifically amplified 18S rDNA. Appl Environ Microbiol 63:3858–3865

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kowalchuk GA, de Souza FA, van Veen JA (2002) Community analysis of arbuscular mycorrhizal fungi associated with Ammophila arenaria in Dutch coastal sand dunes. Mol Ecol 11:571–581

    Article  CAS  PubMed  Google Scholar 

  • Landwehr M, Hilderbrandt U, Wilde P, Nawrath K, Tóth T, Biró B, Bothe H (2002) The arbuscular mycorrhizal fungus Glomus geosporum in European saline, sodic and gypsum soils. Mycorrhiza 12:199–211

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  PubMed  Google Scholar 

  • Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433

    Google Scholar 

  • Li LF, Li T, Zhang Y, Zhao ZW (2010) Molecular diversity of arbuscular mycorrhizal fungi and their distribution patterns related to host-plants and habitats in a hot and arid ecosystem, southwest China. FEMS Microbiol Ecol 71:418–427

    Article  CAS  PubMed  Google Scholar 

  • Liang ZB, Drijber RA, Lee DJ, Dwiekat IM, Harris SD, Wedin DA (2008) A DGGE-cloning method to characterize arbuscular mycorrhizal community structure in soil. Soil Biol Biochem 40:956–966

    Article  CAS  Google Scholar 

  • Lin X, Feng Y, Zhang H, Chen R, Wang J, Zhang J, Chu H (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in north China revealed by 454 pyrosequencing. Environ Sci Technol 46:5764–5771

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, He J, Shi G, An L, Öpik M, Feng H (2011) Diverse communities of arbuscular mycorrhizal fungi inhabit sites with very high altitude in Tibet Plateau. FEMS Microbiol Ecol 355–365

  • Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinforma 7:371

    Article  Google Scholar 

  • Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci USA 104:11436–11440

    Article  CAS  PubMed  Google Scholar 

  • Lugo MA, Negritto MA, Jofré M, Anton A, Galetto L (2012) Colonization of native Andean grasses by arbuscular mycorrhizal fungi in Puna: a matter of altitude, host photosynthetic pathway and host life cycles. FEMS Microbiol Ecol 81:455–466

    Article  CAS  PubMed  Google Scholar 

  • Moora M, Berger S, Davison J, Öpik M, Bommarco R, Bruelheide H et al (2011) Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeogr 38:1305–1317

    Article  Google Scholar 

  • Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790

    Article  Google Scholar 

  • Öpik M, Moora M, Zobel M, Saks U, Wheatley R, Wright F, Daniell T (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytol 179:867–876

    Article  PubMed  Google Scholar 

  • Öpik M, Vanatoa A, Vanatoa E, MooraM DJ, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. Vienna, Austria: R 21 Foundation for statistical computing

  • Renker C, Blanke V, Buscot F (2005) Diversity of arbuscular mycorrhizal fungi in grassland spontaneously developed on area polluted by a fertilizer plant. Environ Pollut 135:255–266

    Article  CAS  PubMed  Google Scholar 

  • Richards LA (1954) Diagnosis and Improvement of Saline and Alkali Soil, U.S. Salinity Lab. Staff, USDA HandBook 60. Washington D.C.

  • Rosendahl S, Stukenbrock E (2004) Community structure of arbuscular mycorrhizal fungi in undisturbed vegetation revealed by analyses of LSU rDNA sequences. Mol Ecol 13:3179–3186

    Article  CAS  PubMed  Google Scholar 

  • Saint-Etienne L, Paul S, Imbert D, Dulormne M, Muller F, Toribio A, Plenchette C, Ba AM (2006) Arbuscular mycorrhizal soil infectivity in a stand of the wetland tree Pterocarpus officinalis along a salinity gradient. Forest Ecol Manag 232:86–89

    Article  Google Scholar 

  • Santos JC, Finlay RD, Tehler A (2006) Molecular analysis of arbuscular mycorrhizal fungi colonising a semi-natural grassland along a fertilisation gradient. New Phytol 172:159–168

    Article  CAS  PubMed  Google Scholar 

  • Schwarzenbach K, Enkerli J, Widmer F (2007) Objective criteria to assess representativity of soil fungal community profiles. J Microbiol Meth 68:358–366

    Article  CAS  Google Scholar 

  • Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sonjak S, Beguiristain T, Leyval C, Regvar M (2009a) Temporal temperature gradient gel electrophoresis (TTGE) analysis of arbuscular mycorrhizal fungi associated with selected plants from saline and metal polluted environments. Plant Soil 314:25–34

    Article  CAS  Google Scholar 

  • Sonjak S, Udovic M, Wraber T, Likar M, Regvar M (2009b) Diversity of halophytes and identification of arbuscular mycorrhizal fungi colonising their roots in an abandoned and sustained part of Secovlje salterns. Soil Biol Biochem 41:1847–1856

    Article  CAS  Google Scholar 

  • Stukenbrock EH, Rosendahl S (2005) Distribution of dominant arbuscular mycorrhizal fungi among five plant species in undisturbed vegetation of a coastal grassland. Mycorrhiza 15:497–503

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • ter Braak, CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical ordination, version 4.5. Microcomputer Power, Ithaca, New York

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequencing weighting, position sequence gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Torrecillas E, Alguacil MM, Roldán A (2012) Differences in the AMF diversity in soil and roots between two annual and perennial gramineous plants co-occurring in a Mediterranean, semiarid degraded area. Plant Soil 354:97–106

    Article  CAS  Google Scholar 

  • Tressner HD, Hayes JA (1971) Sodium chloride tolerance of terrestrial fungi. Appl Microbiol 22:210–213

    Google Scholar 

  • van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Vallino M, Massa N, Lumini E, Bianciotto V, Berta G, Bonfante P (2006) Assessment of arbuscular mycorrhizal fungal diversity in roots of Solidago gigantea growing in a polluted soil in Northern Italy. Environ Microbiol 8:971–983

    Article  PubMed  Google Scholar 

  • Wang FY, Liu RJ, Lin XG, Zhou JM (2004) Arbuscular mycorrhizal status of wild plants in saline-alkaline soils of the Yellow River Delta. Mycorrhiza 14:133–137

    Article  PubMed  Google Scholar 

  • Wang YT, Huang YL, Qiu Q, Xin GR, Yang ZY, Shi SH (2011) Flooding greatly affects the diversity of arbuscular mycorrhizal fungi communities in the roots of wetland plants. PLoS One 6:e24512

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wilde P, Manal A, Stodden M, Sieverding E, Hilderbrandt U, Bothe H (2009) Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 11:1548–1561

    Article  PubMed  Google Scholar 

  • Wirsel SGR (2004) Homogeneous stands of a wetland grass harbour diverse consortia of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 48:129–138

    Article  CAS  PubMed  Google Scholar 

  • Yamato M, Ikeda S, Iwase K (2008) Community of arbuscular mycorrhizal fungi in coastal vegetation on Okinawa Island and effect of the isolated fungi on growth of sorghum under salt-treated conditions. Mycorrhiza 18:241–249

    Article  PubMed  Google Scholar 

  • Yamato M, Yagame T, Yoshimura Y, Iwase K (2012) Effect of environmental gradient in coastal vegetation on communities of arbuscular mycorrhizal fungi associated with Ixeris repens (Asteraceae). Mycorrhiza 22:628–630

    Article  Google Scholar 

  • Zhang XL, Gu DQ, Feng AP, Xia DX (2006) Comparative research on characters and evolvement of vegetation of coastal wetlands of Yellow River Delta and southern Laizhou Bay. Bull Soil Water Conserv 26:127–140

    Google Scholar 

  • Zhang Z, Liu E, Zhang Y, Xin L (2008a) Environmental evolution in the salt-water intrusion area south of Laizhou Bay since late Pleistocene. J Geogr Sci 18:37–45

    Article  CAS  Google Scholar 

  • Zhang XL, Gu DQ, Chen DJ, Sui YZ (2008b) Flora characteristics of vascular plants of coastal wetlands of southern Laizhou Bay and its protection. Ecol Environ 17:86–92 (in Chinese with English Abstract)

    Google Scholar 

  • Zhang X, Ye S, Yin P, Yuan H (2009) Flora characteristics of vascular plants of coastal wetlands in Yellow River Delta. Ecol Environ Sci 18:600–607 (In Chinese with English Abstract)

    Google Scholar 

  • Zhao D, Zhao Z (2007) Biodiversity of arbuscular mycorrhizal fungi in the hot-dry valley of the Jinsha River, southwest China. Appl Soil Ecol 37:118–128

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Main Direction Program of Knowledge Innovation of CAS (grant no. KSCX2-EW-G-12B), the One Hundred Talent Program of CAS, the Natural Science Foundation for Distinguished Young Scholars of Shandong (no. JQ201210), and the Yantai Double Hundred Talent Plan awarded to JG. Thanks are due to Dr. Bin Ma and Dr. Xiaoli Zhang for helps in statistical analysis. The constructive comments of anonymous reviewers are greatly appreciated.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jun Gong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Taxonomic compositions of Glomeromycota and other eukaryotes in small subunit rDNA gene clone libraries generated from PCR with primers AML1/AML2 and DNA extracted from 18 plant species (A1-E3). Groupings are based on BLAST search against GenBank. A. A summary of the sequences newly obtained. B. Comparison of the 18 libraries. Note that the relative proportion of AMF was not significantly correlated with soil salt content (r = −0.246, P = 0.326). (JPEG 684 kb)

High-resolution image

(TIFF 1.96 mb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guo, X., Gong, J. Differential effects of abiotic factors and host plant traits on diversity and community composition of root-colonizing arbuscular mycorrhizal fungi in a salt-stressed ecosystem. Mycorrhiza 24, 79–94 (2014). https://doi.org/10.1007/s00572-013-0516-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-013-0516-9

Keywords

Navigation