Skip to main content

Advertisement

Log in

Intraspecific plant interaction affects arbuscular mycorrhizal fungal species richness

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

Abstract

Aims

It is well established that mycorrhizal symbiosis can affect plant-plant interactions. On the other hand, how intraspecific plant interactions influence communities of arbuscular mycorrhizal fungi (AMF) is still very poorly understood.

Methods

We applied 454 pyrosequencing to determine the responses of AMF communities to intraspecific shoot and root interactions using Medicago sativa L. as host plant.

Results

We found that intraspecific plant interaction caused significant variation in the structure of the AMF community assessed from roots but not from soil. Intraspecific root system interaction resulted in significantly elevated AMF species richness, greater total mycorrhizal and arbuscular colonization, and a larger root:shoot ratio compared to plants experiencing intraspecific shoot interaction or no interaction. Intraspecific shoot interaction resulted in significantly depressed AMF species richness.

Conclusions

Our results support two hypotheses. The first is that increased AMF species richness in plants experiencing intraspecific root interaction originates from competitive release provided by high root density. The second is that shoot interaction leads to reduced allocation to root systems, increasing the stringency with which host plants selectively reward the most cooperative fungi. Because intraspecific interactions among host plants can influence the structure of their AMF community, interactions among species in complex plant communities may influence AMF community structure in addition to a plant diversity effect.

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
Fig. 6

Similar content being viewed by others

References

  • Aldrich-Wolfe L (2007) Distinct mycorrhizal communities on new and established hosts in a transitional tropical plant community. Ecology 88:559–566

    Article  PubMed  Google Scholar 

  • Allsopp N, Stock WF (1992) Density dependent interactions between VA mycorrhizal fungi and even-aged seedlings of two perennial Fabaceae species. Oecologia 91:281–287

    Article  CAS  PubMed  Google Scholar 

  • Antoninka A, Reich PB, Johnson NC (2011) Seven years of carbon dioxide enrichment, nitrogen fertilization and plant diversity influence arbuscular mycorrhizal fungi in a grassland ecosystem. New Phytol 192:200–214

    Article  PubMed  Google Scholar 

  • Azcón R, Rubio R, Barea JM (1991) Selective interactions between different species of mycorrhizal fungi and rhizobium-meliloti strains, and their effects on growth, N2-fixation (15N) and nutrition of Medicago sativa L. New Phytol 117:399–404

    Article  PubMed  Google Scholar 

  • Barto EK, Antunes PM, Stinson K, Koch AM, Klironomos JN, Cipollini D (2011) Differences in arbuscular mycorrhizal fungal communities associated with sugar maple seedlings in and outside of invaded garlic mustard forest patches. Biol Invasions 13:2755–2762

    Article  Google Scholar 

  • Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J Ecol 84:71–82

    Article  Google Scholar 

  • Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Lett 12:13–21

    Article  PubMed  Google Scholar 

  • Bik HM, Porazinska DL, Creer S, Caporaso JG, Knight R, Thomas WK (2012) Sequencing our way towards understanding global eukaryotic biodiversity. Trends Ecol Evol 27:233–243

    Article  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davison J, Öpik M, Zobel M, Vasar M, Metsis M, Moora M (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS One 7:e41938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eissenstat DM, Newman EI (1990) Seedling establishment near large plants: effects of vesicular-arbuscular mycorrhizas on the intensity of plant competition. Funct Ecol 4:95–99

    Article  Google Scholar 

  • Hammer Ø, Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344

    Article  Google Scholar 

  • Hart MM, Forsythe J, Oshowski B, Bücking H, Jansa J, Kiers ET (2013) Hiding in a crowd - does diversity facilitate persistence of a low-quality fungal partner in the mycorrhizal symbiosis? Symbiosis 59:47–56

    Article  Google Scholar 

  • Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of cooccurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384

    Article  Google Scholar 

  • Hiiesalu I, Pärtel M, Davison J, Gerhold P, Metsis M, Moora M, Öpik M, Vasar M, Zobel M, Wilson SD (2014) Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol 203:233–244

    Article  CAS  PubMed  Google Scholar 

  • Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23(5–6):481–488

    Article  CAS  Google Scholar 

  • Jansa J, Mozafar A, Frossard E (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant Soil 276:163–176

    Article  CAS  Google Scholar 

  • Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789

    Article  CAS  PubMed  Google Scholar 

  • Jiang S, Liu Y, Luo J, Qin M, Johnson NC, Öpik M, Vasar M, Chai YZ, Zhou XL, Mao L, Du G, An LZ, Feng HY (2018) Dynamics of arbuscular mycorrhizal fungal community structure and functioning along a nitrogen enrichment gradient in an alpine meadow ecosystem. New Phytol 220:1222–1235

    Article  PubMed  Google Scholar 

  • Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757

    Article  PubMed  Google Scholar 

  • Johnson KH, Vogt KA, Clark HJ, Schmitz OJ, Vogt DJ (1996) Biodiversity and the productivity and stability of ecosystems. Trends Ecol Evol 11:372–377

    Article  CAS  PubMed  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  CAS  PubMed  Google Scholar 

  • Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303

    Article  CAS  Google Scholar 

  • Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415

    Article  CAS  PubMed  Google Scholar 

  • Koch AM, Antunes PM, Klironomos JN (2012) Diversity effects on productivity are stronger within than between trophic groups in the arbuscular mycorrhizal symbiosis. PLoS One 7:e36950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koide RT, Dickie IA (2002) Effects of mycorrhizal fungi on plants populations. Plant Soil 244:307–317

    Article  CAS  Google Scholar 

  • Lambers H, Chapin FS, Pons TL (2008) Interactions among plants. In: plant physiological ecology. Springer, New York, pp 505-531

  • Lekberg Y, Hammer E, Olsson P (2010) Plants as resource islands and storage units–adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol Ecol 74:336–345

    Article  CAS  PubMed  Google Scholar 

  • Li YY, Wang XJ, Dou CY, Lin SS, Luo QY, Cui HJ, Sun L, Jin L (2013) Effects of four host plants and different cultivation densities on the propagation of arbuscular mycorrhizal fungi. Acta Pratacul Sin 22:128–135

    Google Scholar 

  • Martínez-García LB, Pugnaire FI (2011) Arbuscular mycorrhizal fungi host preference and site effects in two plant species in a semiarid environment. Appl Soil Ecol 48:313–317

    Article  Google Scholar 

  • Martínez-García LB, Richardson SJ, Tylianakis JM, Peltzer DA, Dickie IA (2015) Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytol 205:1565–1576

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O‘Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: Community Ecology Package. R Package Version 2. pp. 0–10. http://CRAN.R-project.org/package=vegan

  • Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, 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 

  • Sasvári Z, Posta K (2010) Effect of different plant densities on the diversity of arbuscular mycorrhizal fungi community in a long-term maize monocrop system. Span J Agric Res 8:S123–S130

    Article  Google Scholar 

  • Sato K, Suyama Y, Saito M, Sugawara K (2005) A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassl Sci 51:179–181

    Article  CAS  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005) Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomus species in the presence of root flavonoids. J Plant Physiol 162:625–633

    Article  CAS  PubMed  Google Scholar 

  • Shaw AK, Halpern AL, Beeson K, Tran B, Venter JC, Martiny JB (2008) It’s all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 10:2200–2210

  • Shumway DL, Koide RT (1995) Size and reproductive inequality in mycorrhizal and nonmycorrhizal populations of Abutilon theophrasti. J Ecol 83:613–620

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis 3rd edition. Academic Press, San Diego

    Google Scholar 

  • Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18:607–621

    Article  CAS  PubMed  Google Scholar 

  • 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 biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  Google Scholar 

  • Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Coexisting grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095

    Article  CAS  PubMed  Google Scholar 

  • Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 1:15159

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Liu SJ, Song SR, Guo HL, Tang JJ, Yong JWH, Ma YD, Chen X (2018) Arbuscular mycorrhizal fungi influence decomposition and the associated soil microbial community under different soil phosphorus availability. Soil Biol Biochem 120:181–190

    Article  CAS  Google Scholar 

  • Yang HS, Zang YY, Yuan YG, Tang JJ, Chen X (2012) Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol Biol 12:50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang HS, Koide RT, Zhang Q (2016) Short-term waterlogging increases arbuscular mycorrhizal fungal species richness and shifts community composition. Plant Soil 404:373–384

    Article  CAS  Google Scholar 

  • Yang HS, Zhang Q, Koide RT, Hoeksema JD, Tang JJ, Bian XM, Hu SJ, Chen X (2017) Taxonomic resolution is a determinant of biodiversity effects in arbuscular mycorrhizal fungal communities. J Ecol 105:219–228

    Article  CAS  Google Scholar 

  • Yao Q, Hu YY, Liao JC, Zhu HH (2007) Influence of host planting density on sporulation of arbuscular mycorrhizal fungi. Journal of South China Agricultural University 28:14–17

    Google Scholar 

  • Yoda K, Kira T, Ogawa H, Hozumi K (1963) Self-thinning in overcrowded pure stands under cultivated and natural conditions. J Biol, Osaka City University 14:107–129

    Google Scholar 

  • Zhang Q, Zhang L, Weiner J, Tang J, Chen X (2011) Arbuscular mycorrhizal fungi alter plant allometry and biomass-density relationships. Ann Bot-London 107:407–413

    Article  Google Scholar 

  • Zheng C, Ji B, Zhang J, Zhang FS, Bever JD (2015) Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist. New Phytol 205:361–368

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Central Public-interest Scientific Institution Basal Research Fund (CAFYBB2019QB001) and the Natural Science Foundation of China (No. 31870099).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Haishui Yang.

Additional information

Responsible Editor: Yongguan Zhu.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Q., Koide, R.T., Liu, J. et al. Intraspecific plant interaction affects arbuscular mycorrhizal fungal species richness. Plant Soil 470, 141–152 (2022). https://doi.org/10.1007/s11104-021-04962-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-04962-5

Keywords

Navigation