Skip to main content
SpringerLink
Log in

Responses of mycorrhizal colonization to nitrogen and phosphorus addition in fourteen woody and herbaceous species: the roles of hypodermal passage cells and penetration points

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

Abstract

Background and aims

The rate of mycorrhizal colonization in plant roots generally decreases with increased soil nutrient availability but the underlying mechanism is still poorly understood. Our aims were to explore the responses of root mycorrhizal colonization, passage cells, and penetration points under nitrogen (N) and phosphorus (P) addition and their potential linkages in woody and herbaceous plants.

Methods

N and P were added to the pots of 14 temperate species (eight woody and six herbaceous) in the greenhouse, and the distribution of mycorrhizal colonization, passage cells and penetration points for each species were observed by staining and microscopy of first-order roots.

Results

The average density and proportion of mycorrhizal colonization, passage cells and penetration points of 14 species were significantly decreased under N and P addition. The N addition had a stronger effect on the plants than the P addition. More importantly, the mycorrhizal colonization density and proportion showed significant positive correlations with passage cell density and proportion, and with penetration point density and proportion of woody and herbaceous plants under control and nutrient treatments.

Conclusions

The density and proportion of mycorrhizal colonization were closely related with passage cells and penetration points in both woody and herbaceous species in either control or nutrient treatments. Our results are of great significance for understanding the relationship between soil fungi and plant roots under changes of soil nutrient availabilities.

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
Fig. 5

Similar content being viewed by others

References

  • Andersen TG, Naseer S, Ursache R et al (2018) Diffusible repression of cytokinin signalling produces endodermal symmetry and passage cells. Nature 555:529–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson RC, Ebbers BC, Liberta AE (2010) Soil moisture influences colonization of prairie cordgrass (Spartina pectinata Lind.) by vesicular–arbuscular mycorrhizal fungi. New Phytol 102:523–527

    Article  Google Scholar 

  • Antoninka A, Johnson RNC (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 

  • Bardgett RD, Mommer L, Vries FTD (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699

    Article  PubMed  Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Article  PubMed  Google Scholar 

  • Chen W, Koide RT, Adams TS et al (2016) Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. PNAS 113:8741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Booker FL, Tu C, Burkey KO, Zhou LS, Shew HD, Rufty TW, Hu SJ (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087

    Article  CAS  PubMed  Google Scholar 

  • Eissenstat DM, Kucharski JM (2015) Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytol 208:114–124

    Article  PubMed  Google Scholar 

  • Ejiri M, Shiono K (2020) Groups of multi–cellular passage cells in the root exodermis of Echinochloa crus–galli varieties lack not only suberin lamellae but also lignin deposits. Plant Signal Behav 15:1719749

    Article  PubMed  PubMed Central  Google Scholar 

  • Enstone DE, Peterson CA, Ma F. (2003) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351

    Google Scholar 

  • Esnault AL, Masuhara G, Mcgee PA (1994) Involvement of exodermal passage cells in mycorrhizal infection of some orchids. Mycol Res 98:672–676

    Article  Google Scholar 

  • Garcia MO, Ovasapyan T, Greas M et al (2008) Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest. Plant Soil 303:301–310

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Guo DL, Xia MX, Wei X, Chang WJ, Liu Y, Wang ZQ (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty–three Chinese temperate tree species. New Phytol 180:673–683

    Article  PubMed  Google Scholar 

  • Gutjahr C, Sawers R, Marti G et al (2013) Transcriptome diversity among rice root types during asymbiosis and interaction with arbuscular mycorrhizal fungi. PNAS 112:6754–6759

    Article  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 

  • Hartung W, Leport L, Ratcliffe RG, Sauter A, Turner NC (2002) Abscisic acid concentration, root pH and anatomy do not explain growth differences of chickpea (Cicer arietinum L.) and lupin (Lupinus angustifolius L.) on acid and alkaline soils. Plant Soil 240:191–199

    Article  CAS  Google Scholar 

  • Heijden MG, 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 

  • Heinemeyer A, Ridgway KP, Edwards EJ, Benham DG, Fitter AH (2010) Impact of soil warming and shading on colonization and community composition of arbuscular mycorrhizal fungi in roots of a native grassland community. Glob Change Biol 10:52–64

    Article  Google Scholar 

  • Hishi TK, Tateno RK, Takeda HS (2006) Anatomical characteristics of individual roots within the fine–root architecture of Chamaecyparis obtusa (Sieb. & Zucc.) in organic and mineral soil layers. Ecol Res 21:754–758

    Article  Google Scholar 

  • Jayne B (2012) Influence of soil microorganisms on plant growth and fitness. University of Denver

    Google Scholar 

  • Jia SX, ZhaoYL DGQ, Sun Y, Yang XY, Wang ZQ (2010) Relationship among fine–root morphology, anatomy, tissue nitrogen concentration and respiration in different branch root orders in larix gmelinii and fraxinus mandshurica. Chin Bul Bot 45:174–181

    CAS  Google Scholar 

  • Kadowaki K, Yamamoto S, Sato H, Akifumi ST, Amane H, Hirokazu T (2018) Mycorrhizal fungi mediate the direction and strength of plant–soil feedbacks differently between arbuscular mycorrhizal and ectomycorrhizal communities. Commun Biol 1:196

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiba T, Kudo T, Kojima M et al (2011) Hormonal control of nitrogen acquisition: Roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62:1399–1409

    Article  CAS  PubMed  Google Scholar 

  • Koide R, Kabir Z (2000) Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol 148:511–517

    Article  CAS  PubMed  Google Scholar 

  • Koide RT, Mooney HA (1987) Spatial variation in inoculum potential of vesicular arbuscular mycorrhizal fungi caused by formation of gopher mounds. New Phytol 107:173–182

    Article  Google Scholar 

  • Kong DL, Ma CE, Zhang Q, Li L, Chen XY, Zeng H, Guo DL (2014) Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytol 203:863–872

    Article  PubMed  Google Scholar 

  • Kumar P, Hallgren SW, Enstone DE, Peterson CA (2007) Root anatomy of Pinus taeda L: Seasonal and environmental effects on development in seedlings. Tree 21:693–706

    Article  Google Scholar 

  • Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: Origins of secondary metabolites. Chem Biol 19:792–798

    Article  CAS  PubMed  Google Scholar 

  • Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus–deficient soils. The Proceedings of The national Academy of Sciences 104:11192–11196

    Article  CAS  Google Scholar 

  • Liu BT, Li HB, Zhu B, Koide RT, Eissenstat DM, Guo DL (2015) Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytol 208:125–136

    Article  PubMed  Google Scholar 

  • Ma F, Peterson CA (2001) Development of cell wall modifications in the endodermis and exodermis of Allium cepa roots. Can J Bot 79:621–634

    Google Scholar 

  • Mao QG, Zhou XK et al (2017) Effects of long-term nitrogen and phosphorus additions on soil acidification in an N-rich tropical forest. Geoderma 285:57–63

    Article  CAS  Google Scholar 

  • Mcarthur DAJ, Knowles NR (1992) Resistance responses of potato to vesicular–arbuscular mycorrhizal fungi under varying abiotic phosphorus levels. Plant Physiol 100:341–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mckenzie EB, Peterson CA (1995a) Root browning in Pinus banksiana Lamn. and Eucalyptus pilularis Sm. 1. Anatomy and permeability of the white and tannin zones. Botanica Acta 108:127–137

    Article  CAS  Google Scholar 

  • Mckenzie EB, Peterson CA (1995b) Root browning in Pinus banksiana Lamn. and Eucalyptus pilularis Sm. 2. Anatomy and permeability of the cork zone. Botanica Acta 108:138–143

    Article  CAS  Google Scholar 

  • Michael JB, Gomola CE, Horton TR (2011) The effect of forest soil and community composition on ectomycorrhizal colonization and seedling growth. Plant Soil 341:321–331

    Article  Google Scholar 

  • Nagahashi G, Abney GD (1996) Phosphorus amendment inhibits hyphal branching of the VAM fungus Gigaspora margarita directly and indirectly through its effect on root exudation. Mycorrhiza 6:403–408

    Article  CAS  Google Scholar 

  • Namyslov JR, Bauriedlová Z, Janoušková J, Soukup A, Tylová E (2020) Exodermis and endodermis respond to nutrient deficiency in nutrient–specific and localized manner. Plants 9:201

    Article  CAS  PubMed Central  Google Scholar 

  • Noguchi K, Nagakura J, Sakata T, Kaneko S, Takahashi M (2013) Fine–root dynamics in sugi (Cryptomeria japonica) under manipulated soil nitrogen conditions. Plant Soil 364:159–169

    Article  CAS  Google Scholar 

  • Pan S, Wang Y, Qiu Y et al (2020) Nitrogen-induced acidification, not N-nutrient, dominates suppressive N effects on arbuscular mycorrhizal fungi. Glob Change Biol 26:1–37

    Article  Google Scholar 

  • Peterson CA, Enstone DE (1996) Functions of passage cells in the endodermis and exodermis of roots. Physiol Plant 97:592–598

    Article  CAS  Google Scholar 

  • Podolich O, Ardanov P, Zaets I, Pirttila AM, Kozyrovska N (2015) Reviving of the endophytic bacterial community as a putative mechanism of plant resistance. Plant Soil 388:367–377

    Article  CAS  Google Scholar 

  • Pregitzer KS, Deforest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine north American trees. Ecol Monogr 72:293–309

    Article  Google Scholar 

  • Read DJ, Perez-Moreno J (2010) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492

    Article  Google Scholar 

  • Reynolds HL, Hartley AE, Vogelsang KM, Bever JD, Schultz PA (2005) Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old–field perennials under low nitrogen supply in glasshouse culture. New Phytol 167:869–880

    Article  CAS  PubMed  Google Scholar 

  • Sharda JN, Koide RT (2008) Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi? New Phytol 180:696–701

    Article  CAS  PubMed  Google Scholar 

  • Sharda JN, Koide RT (2010) Exploring the role of root anatomy in p–mediated control of colonization by arbuscular mycorrhizal fungi. Botany 88:165–173

    Article  CAS  Google Scholar 

  • Shi T, Zhao D, Li D et al (2012) Brassica napusroot mutants insensitive to exogenous cytokinin show phosphorus efficiency. Plant Soil 358:61–74

    Article  CAS  Google Scholar 

  • Shishkoff N (1987) Distribution of the dimorphic hypodermis of roots in angiosperm families. Ann Bot 60:1–15

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press

    Google Scholar 

  • Smith SE, Smith FA (2010) Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250

    Article  Google Scholar 

  • Soukup A, Tylová E (2014) Essential methods of plant sample preparation for light microscopy. Plant Cell Morphogenesis. Springer

    Google Scholar 

  • Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136:3864–3876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao Q, Jupa R, Liu Y et al (2019) Abscisic acid-mediated modifications of radial apoplastic transport pathway play a key role in cadmium uptake in hyperaccumulator Sedum alfredii. Plant Cell Environ 42:1425–1440

    Article  CAS  PubMed  Google Scholar 

  • Tawaraya K, Hashimoto K, Wagatsuma T (1998) Effect of root exudate fractions from P–deficient and P–sufficient onion plants on root colonisation by the arbuscular mycorrhizal fungus Gigaspora margarita. Mycorrhiza 8:67–70

    Article  CAS  Google Scholar 

  • Tiunov AV, Scheu S (2005) Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia 142:636–642

    Article  PubMed  Google Scholar 

  • Treseder KK, Allen MF (2002) Direct nitrogen and phosphorus imitation of arbuscular mycorrhizal fungi: A model and field test. New Phytol 155:507–515

    Article  PubMed  Google Scholar 

  • Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Let 8:214–217

    Article  Google Scholar 

  • Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11:301–307

    Article  CAS  PubMed  Google Scholar 

  • Vos C, Claerhout S, Mkandawire R et al (2012) Arbuscular mycorrhizal fungi reduce root–knot nematode penetration through altered root exudation of their host. Plant Soil 354:335–345

    Article  CAS  Google Scholar 

  • Wang HF, Wang ZQ, Dong XY (2019) Anatomical structures of fine roots of 91 vascular plant species from four groups in a temperate forest in Northeast China. PLoS ONE 5:e0215126

    Article  Google Scholar 

  • Waterman RJ, Bidartondo MI (2008) Deception above, deception below: linking pollination and mycorrhizal biology of orchids. J Exp Bot 59:1085–1096

    Article  CAS  PubMed  Google Scholar 

  • Weiss M, Schmidt J, Neumann D, Wray V, Christ R, Strack D (1999) Phenyl-propanoids in mycorrhizas of the Pinaceae. Planta 208:491–502

    Article  CAS  Google Scholar 

  • Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235:1197–1207

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Key Research and Development Program of China (2017YFD0601204), the Fundamental Research Funds for the Central Universities (2572019CP16), and the Heilongjiang Touyan Innovation Team Program (Technology Development Team for Highly efficient Silviculture of Forest Resources). The authors thank AiMi Academic Services (www.aimieditor.com) for English language editing and review services.

Author information

Authors and Affiliations

  1. Key Laboratory of Sustainable Forest Ecosystem Management-Ministry of Education, School of Forestry, Northeast Forestry University, Harbin, 150040, China

    Liying Xu, Siyuan Wang, Yue Liu, Li Ji, Fangyuan Shen & Lixue Yang

  2. College of Life Science and Technology, Mudanjiang Normal College, Mudanjiang, 157011, China

    Liying Xu

  3. Jilin Academy of Forestry, Changchun, 130033, China

    Yue Liu & Li Ji

Authors
  1. Liying Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Siyuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yue Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Li Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fangyuan Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lixue Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lixue Yang.

Additional information

Responsible Editor: Stavros D. Veresoglou.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2013 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, L., Wang, S., Liu, Y. et al. Responses of mycorrhizal colonization to nitrogen and phosphorus addition in fourteen woody and herbaceous species: the roles of hypodermal passage cells and penetration points. Plant Soil 469, 273–285 (2021). https://doi.org/10.1007/s11104-021-05107-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-05107-4

Keywords

Search

Navigation