Skip to main content
SpringerLink
Log in

Cultivation of arbuscular mycorrhizal Broussonetia papyrifera seedlings by planting the mycorrhizal nurse plant downwards

  • Short Note
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Plant mycorrhization can be achieved by transplanting new seedlings with mycorrhizal nurse plants; however, this method inevitably induces plant interactions. Transplanting nurse plants downwards may prevent light competition among new seedlings and nurse plants in the same pot. We hypothesized that seedling mycorrhization via mycorrhizal provision from plants planted downwards would be a feasible and efficient strategy. We used seedlings cultivated for 6 months after inoculation with arbuscular mycorrhizal fungi (AMF) as nurse plants, and seedlings cultivated for 1 month without AMF as recipient plants, transplanting one nurse plant and three recipient plants together in one pot. We compared two approaches for cultivating mycorrhizal Broussonetia papyrifera seedlings: planting mycorrhizal nurse plants upwards (M-NU) and downwards (M-ND). We also planted non-mycorrhizal nurse plants upwards (NM-NU) and downwards (NM-ND) as controls. We analyzed growth parameters and the mycorrhizal colonization status of recipient plants at 45, 60, and 75 days after planting (DAP). As expected, the plant growth, gas exchange, and root morphological parameters of recipient plants with mycorrhizal nurse plants were higher than those of recipient plants with non-mycorrhizal nurse plants at 60 and 75 DAP. Furthermore, the AMF colonization status and physiological growth status of M-ND recipient plants were improved compared with M-NU recipient plants. Our results demonstrate that inducing seedling mycorrhization by planting mycorrhizal nurse plants downwards is a feasible strategy for achieving AMF symbiosis while mitigating negative interactions among plants.

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

References

  • Balandier P, Collet C, Miller JH, Reynolds PE, Zedaker SM (2006) Designing forest vegetation management strategies based on the mechanisms and dynamics of crop tree competition by neighbouring vegetation. Forestry 79(1):3–27

    Article  Google Scholar 

  • Barto EK, Weidenhamer JD, Cipollini D, Rillig MC (2012) Fungal superhighways: do common mycorrhizal networks enhance below ground communication? Trends Plant Sci 17:633–637

    Article  CAS  PubMed  Google Scholar 

  • Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068

    Article  PubMed  PubMed Central  Google Scholar 

  • Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559

    Article  PubMed  PubMed Central  Google Scholar 

  • Beyer F, Hertel D, Jung K, Fender AC, Leuschner C (2013) Competition effects on fine root survival of Fagus sylvatica and Fraxinus excelsior. For Ecol Manage 302:14–22

    Article  Google Scholar 

  • Bhantana P, Rana MS, Sun XC, Moussa MG, Saleem MH, Syaifudin M, Hu CX (2021) Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation. Symbiosis 84(1):19–37

    Article  CAS  Google Scholar 

  • Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28(1):545–570

    Article  Google Scholar 

  • Chen J, Zhang HQ, Zhang XL, Tang M (2017a) Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Front Plant Sci 8:1739

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen P, Hu Y, Tang F, Zhao M, Peng X, Shen S (2020) Cooperation between Broussonetia papyrifera and its symbiotic fungal community to improve local adaptation of the host. Appl Environ Microbiol 86(18):e00464-e520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Zhao H, Zou C, Li Y, Chen Y, Wang Z, Ahammed GJ (2017b) Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front Microbiol 8:2516

    Article  PubMed  PubMed Central  Google Scholar 

  • Derelle D, Declerck S, Genet P, Dajoz I, van Aarle IM (2012) Association of highly and weakly mycorrhizal seedlings can promote the extra-and intraradical development of a common mycorrhizal network. FEMS Microbiol Ecol 79(1):251–259

    Article  CAS  PubMed  Google Scholar 

  • de Vries J, Evers JB, Kuyper TW, van Ruijven J, Mommer L (2021) Mycorrhizal associations change root functionality: a 3D modeling study on competitive interactions between plants for light and nutrients. New Phytol 231(3):1171–1182

    Article  PubMed  PubMed Central  Google Scholar 

  • El Omari B, El Ghachtouli N (2021) Arbuscular mycorrhizal fungi-weeds interaction in cropping and unmanaged ecosystems: a review. Symbiosis 83:279–292

    Article  Google Scholar 

  • Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, Bücking H (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203(2):646–656

    Article  CAS  PubMed  Google Scholar 

  • Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting. Trans Brit Mycol Soc 46(2):235–244

    Article  Google Scholar 

  • He Y, Cornelissen JH, Wang P, Dong M, Ou J (2019) Nitrogen transfer from one plant to another depends on plant biomass production between conspecific and heterospecific species via a common arbuscular mycorrhizal network. Environ Sci Pollut Res 26(9):8828–8837

    Article  CAS  Google Scholar 

  • Helander M, Saloniemi I, Omacini M, Druille M, Salminen JP, Saikkonen K (2018) Glyphosate decreases mycorrhizal colonization and affects plant-soil feedback. Sci Total Environ 642:285–291

    Article  CAS  PubMed  Google Scholar 

  • Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162(1):9–24

    Article  Google Scholar 

  • Hu W, Pan L, Chen H, Tang M (2020) VBA-AMF: A VBA program based on the magnified intersections method for quantitative recording of root colonization by arbuscular mycorrhizal fungi. Indian J Microbiol 60(3):374–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu W, Zhang H, Chen H, Tang M (2017) Arbuscular mycorrhizas influence Lycium barbarum tolerance of water stress in a hot environment. Mycorrhiza 27(5):451–463

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Zhang H, Song Y, Yang Y, Chen H, Tang M (2017) Subcellular compartmentalization and chemical forms of lead participate in lead tolerance of Robinia pseudoacacia L. with Funneliformis mosseae. Front Plant Sci 8:517

  • Igiehon NO, Babalola OO (2017) Biofertilizers and sustainable agriculture: exploring arbuscular mycorrhizal fungi. Appl Microbiol Biotechnol 101(12):4871–4881

    Article  CAS  PubMed  Google Scholar 

  • Jabborova D, Annapurna K, Paul S, Kumar S, Saad HA, Desouky S, Elkelish A (2021) Beneficial features of biochar and arbuscular mycorrhiza for improving spinach plant growth, root morphological traits, physiological properties, and soil enzymatic activities. J Fungi 7(7):571

    Article  CAS  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120(3):371–380

  • Jakobsen I, Hammer EC (2015) Nutrient dynamics in arbuscular mycorrhizal networks. Nutrient Dynamics in Arbuscular Mycorrhizal Networks. In: Horton TR (ed) Mycorrhizal Networks. Springer, Dordrecht, pp 91–131

    Chapter  Google Scholar 

  • Janos DP (1980) Mycorrhizae influence tropical succession. Biotropica 12:56–64

    Article  Google Scholar 

  • Janos DP, Scott J, Aristizabal C, Bowman DM (2013) Arbuscular-mycorrhizal networks inhibit Eucalyptus tetrodonta seedlings in rain forest soil microcosms. PLoS One 8(2):e57716

  • Ji L, Tan W, Chen X (2019) Arbuscular mycorrhizal mycelial networks and glomalin-related soil protein increase soil aggregation in calcaric regosol under well-watered and drought stress conditions. Soil Tillage Res 185:1–8

    Article  Google Scholar 

  • Kaur S, Kaur R, Chauhan BS (2018) Understanding crop-weed-fertilizer-water interactions and their implications for weed management in agricultural systems. Crop Prot 103:65–72

    Article  Google Scholar 

  • Kelly WL, Bryden MM (1983) A modified differential stain for cartilage and bone in whole mount preparations of mammalian fetuses and small vertebrates. Stain Technol 58(3):131–134

    Article  CAS  PubMed  Google Scholar 

  • Khade SW, Adholeya A (2007) Feasible bioremediation through arbuscular mycorrhizal fungi imparting heavy metal tolerance: a retrospective. Bioremediat J 11(1):33–43

    Article  CAS  Google Scholar 

  • Kitaya Y, Kiyota M, Imanaka T, Aiga I (1992) Growth of vegetables suspended upside down. Acta Hort 303:79–84

    Article  Google Scholar 

  • Kytöviita MM, Vestberg M, Tuomi J (2003) A test of mutual aid in common mycorrhizal networks: established vegetation negates benefit in seedlings. Ecology 84(4):898–906

    Article  Google Scholar 

  • Leonard RT, Vanderwoude WJ (1976) Isolation of plasma membranes from corn roots by sucrose density gradient centrifugation: an anomalous effect of ficoll. Plant Physiol 57(1):105–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin G, Mccormack ML, Guo D (2015) Arbuscular mycorrhizal fungal effects on plant competition and community structure. J Ecol 103:1224–1232

    Article  CAS  Google Scholar 

  • Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109(1):7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Ma Y, Wei Z, Wu J, Sun C, Yang J, Huang JH (2021) Effects of arbuscular mycorrhizal fungi symbiosis on microbial diversity and enzyme activities in the rhizosphere soil of Artemisia annua. Soil Sci Soc Am J 85:703–716

    Article  CAS  Google Scholar 

  • Merrild MP, Ambus P, Rosendahl S, Jakobsen I (2013) Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. New Phytol 200(1):229–240

    Article  CAS  PubMed  Google Scholar 

  • Olowolaju ED, Adelusi AA (2017) Photosynthetic pigments accumulation and some growth indices of cowpea, maize and tomato in response to interspecific and intraspecific competition stress. Sci Cold Arid Reg 9(2):1–6

    Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55(1):158–161

    Article  Google Scholar 

  • Pietikäinen A, Kytöviita MM (2007) Defoliation changes mycorrhizal benefit and competitive interactions between seedlings and adult plants. J Ecol 95(4):639–647

    Article  Google Scholar 

  • Rodriguez-Heredia M, Djian-Caporalino C, Ponchet M, Lapeyre L, Canaguier R, Fazari A, Marteau N, Offroy-Chave M (2020) Protective effects of mycorrhizal association in tomato and pepper against Meloidogyne incognita infection, and mycorrhizal networks for early mycorrhization of low mycotrophic plants. Phytopathol Mediterr 59(2):377–384

    Google Scholar 

  • Schroth G (1995) Tree root characteristics as criteria for species selection and systems design in agroforestry. Agrofor Syst 30:125–143

    Article  Google Scholar 

  • Schubert A, Lovisolo C, Peterlunger E (1999) Shoot orientation affects vessel size, shoot hydraulic conductivity and shoot growth rate in Vitis vinifera L. Plant Cell Environ 22(2):197–204

    Article  CAS  PubMed  Google Scholar 

  • Singh NV, Singh SK, Singh AK, Meshram DT, Suroshe SS, Mishra DC (2012) Arbuscular mycorrhizal fungi (AMF) induced hardening of micropropagated pomegranate (Punica granatum L.) plantlets. Sci Hortic 136:122–127

    Article  Google Scholar 

  • Song Y, Wang M, Zeng R, Groten K, Baldwin IT (2019) Priming and filtering of antiherbivore defences among Nicotiana attenuata plants connected by mycorrhizal networks. Plant Cell Environ 42(11):2945–2961

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Johny L, Adholeya A (2021) Review of patents for agricultural use of arbuscular mycorrhizal fungi. Mycorrhiza 31:1–10

    Article  Google Scholar 

  • Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001

    Article  Google Scholar 

  • Walder F, van Der Heijden MG (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 1(11):1–7

    Article  Google Scholar 

  • Wang X, Zhang R, Wang J, Di L, Sikdar A (2021) The effects of leaf extracts of four tree species on Amygdalus pedunculata seedlings growth. Front Plant Sci 11:587579

  • Weiner J (1990) Asymmetric competition in plant populations. Trends Ecol Evol 5(11):360–364

    Article  CAS  PubMed  Google Scholar 

  • Weremijewicz J, Sternberg LSLOR, Janos DP (2016) Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol 212(2):461–471

    Article  CAS  PubMed  Google Scholar 

  • Wipf D, Krajinski F, van Tuinen D, Recorbet G, Courty PE (2019) Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. New Phytol 223(3):1127–1142

    Article  CAS  PubMed  Google Scholar 

  • Wyatt GA, Kiers ET, Gardner A, West SA (2014) A biological market analysis of the plant-mycorrhizal symbiosis. Evolution 68(9):2603–2618

    Article  PubMed  Google Scholar 

  • Yang H, Zhang Q, Dai Y, Liu Q, Tang J, Bian X, Chen X (2015) Effects of arbuscular mycorrhizal fungi on plant growth depend on root system: a meta-analysis. Plant Soil 389(1):361–374

    Article  CAS  Google Scholar 

  • Zhang W, Zhao Y, Xu Z, Huang H, Zhou J, Yang G (2020) Morphological and physiological changes of Broussonetia papyrifera seedlings in cadmium contaminated soil. Plants 9(12):1698

    Article  CAS  PubMed Central  Google Scholar 

  • Zhu XQ, Wang CY, Chen H, Tang M (2014) Effects of arbuscular mycorrhizal fungi on photosynthesis, carbon content, and calorific value of black locust seedlings. Photosynthetica 52(2):247–252

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Prof. David Janos, the Editor-in-Chief of Mycorrhiza, and two anonymous reviewers for their instructive advice and useful suggestions on both language and academic aspects.

Funding

This study was financially supported by the National Natural Science Foundation of China (32001289, 32071639) and the Laboratory of Lingnan Modern Agriculture Project (NZ2021025). National Natural Science Foundation of China, 32001289, Wentao Hu, 32071639, Ming Tang, Laboratory of Lingnan Modern Agriculture Project, NZ2021025, Ming Tang.

Author information

Authors and Affiliations

  1. State Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, 510642, China

    Zhihao Wang, Jingwei Liang, Yuxuan Kuang, Xue Li, Hui Chen, Ming Tang & Wentao Hu

Authors
  1. Zhihao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jingwei Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuxuan Kuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xue Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ming Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wentao Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, MT, WH, and ZW. Data collection and analysis, ZW, JL, YK, and XL. Project administration, MT. Supervision, WH. Writing—original draft, ZW. Writing—review and editing, MT, WH, and HC.

Corresponding authors

Correspondence to Ming Tang or Wentao Hu.

Additional information

Publisher's Note

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

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1402 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Z., Liang, J., Kuang, Y. et al. Cultivation of arbuscular mycorrhizal Broussonetia papyrifera seedlings by planting the mycorrhizal nurse plant downwards. Mycorrhiza 32, 203–212 (2022). https://doi.org/10.1007/s00572-022-01070-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-022-01070-9

Keywords

Search

Navigation