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Which root traits determine nitrogen uptake by alpine plant species on the Tibetan Plateau?

Abstract

Background and aims

Nitrogen (N) is one of the most important limiting factors influencing plant growth and reproduction in alpine and tundra ecosystems. However, in situ observations of the effects of root traits on N absorption by alpine plant species are still lacking.

Methods

We investigated the rates of N uptake and the effect of root characteristics in ten common herbaceous alpine plant species using a 15N isotope tracer technique and the root systems of plants growing in a semi-arid steppe environment on the Tibetan Plateau. Our objective was to determine the root traits (root biomass, volume, surface area, average diameter, length, specific root length and specific root area) that make the largest contribution to the total uptake of N (15N–NO3 , 15N–NH4 + or 15N–glycine) by alpine plant species.

Results

Monocotyledonous species had higher absorption rates for 15N–NH4 +, 15N–NO3 , 15N–glycine and total 15N than dicotyledonous species (P < 0.05). The root biomass, volume, surface area and average diameter were negatively correlated with the absorption capacity for 15N–NH4 +, 15N–NO3 and total 15N across the ten alpine plant species. However, the specific root length and the specific root area had significantly positive effects on the uptake of N.

Conclusions

In contrast with traditional views on the uptake of N, the N uptake rate was not improved by a larger root volume or root surface area for these alpine plant species in a high-altitude ecosystem. Root morphological traits had greater impacts on N absorption than traits related to the root system size in alpine herbaceous plants.

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References

  • Andersen KM, Turner BL (2013) Preferences or plasticity in nitrogen acquisition by understorey palms in a tropical montane forest. J Ecol 101:819–825

    CAS  Article  Google Scholar 

  • Andresen LC, Jonasson S, Ström L, Michelsen A (2008) Uptake of pulse injected nitrogen by soil microbes and mycorrhizal and non-mycorrhizal plants in a species-diverse subarctic heath ecosystem. Plant Soil 313:283–295

    CAS  Article  Google Scholar 

  • Ashton IW, Miller AE, Bowman WD, Suding KN (2008) Nitrogen preferences and plant-soil feedbacks as influenced by neighbors in the alpine tundra. Oecologia 156:625–636

    CAS  Article  PubMed  Google Scholar 

  • Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252

    Article  PubMed  Google Scholar 

  • Bowman AEMWD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250:283–292

    Article  Google Scholar 

  • Bowman WD, Conant RT (1993) Constraints of nutrient availability on primary production in two alpine tundra communities. Ecology 74:2085–2097

    Article  Google Scholar 

  • Bowsher AW, Miller BJ, Donovan LA (2016) Evolutionary divergences in root system morphology, allocation, and nitrogen uptake in species from high- versus low-fertility soils. Funct Plant Biol 43:129–140

    Article  Google Scholar 

  • Buljovcic Z, Engels C (2001) Nitrate uptake ability by maize roots during and after drought stress. Plant Soil 229:125–135

    CAS  Article  Google Scholar 

  • Cleavitt NLCL, Fahey TJFJ, Groffman PMGM, Hardy JPHP, Henry KSHS, Driscoll CTDT (2008) Effects of soil freezing on fine roots in a northern hardwood forest. Can J For Res 38:82–91

    Article  Google Scholar 

  • Craine JM (2005) Reconciling plant strategy theories of Grime and Tilman. J Ecol 93:1041–1052

    Article  Google Scholar 

  • Craine JM, Tilman D, Wedin D, Reich P, Tjoelker M, Knops J (2002) Functional traits, productivity and effects on nitrogen cycling of 33 grassland species. Funct Ecol 16:563–574

    Article  Google Scholar 

  • Cruz C, Lips SH, Martins-Loução MA (1995) Uptake regions of inorganic nitrogen in roots of carob seedlings. Physiol Plant 95:167–175

    CAS  Article  Google Scholar 

  • Gao JQ, Mo Y, Xu XL, Zhang XW, Yu FH (2014) Spatiotemporal variations affect uptake of inorganic and organic nitrogen by dominant plant species in an alpine wetland. Plant Soil 381:271–278

    CAS  Article  Google Scholar 

  • Grellmann D (2002) Plant responses to fertilization and exclusion of grazers on an arctic tundra heath. Oikos 98:190–204

    Article  Google Scholar 

  • Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999

    Article  PubMed  Google Scholar 

  • Harrison KA, Bol R, Bardgett RD (2008) Do plant species with different growth strategies vary in their ability to compete with soil microbes for chemical forms of nitrogen? Soil Biol Biochem 40:228–237

    CAS  Article  Google Scholar 

  • Hawkins BJ (2014) Nitrogen uptake over entire root systems of tree seedlings. Tree Physiol 34:334–342

    CAS  Article  PubMed  Google Scholar 

  • Holdaway RJ, Coomes DA (2011) Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. J Ecol 99:954–963

    Article  Google Scholar 

  • Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants—an important N uptake pathway? Soil Biol Biochem 37:413–423

    CAS  Article  Google Scholar 

  • Jumpponen A, Högberg P, Huss-Danell K, Mulder CPH (2002) Interspecific and spatial differences in nitrogen uptake in monocultures and two-species mixtures in north European grasslands. Funct Ecol 16:454–461

    Article  Google Scholar 

  • Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244–1255

    Article  PubMed  Google Scholar 

  • Kielland K (1994) Amino acid absorption by arctic plants: Implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383

    Article  Google Scholar 

  • Körner C (1999) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin

    Book  Google Scholar 

  • Kreyling J, Peršoh D, Werner S, Benzenberg M, Wöllecke J (2012) Short-term impacts of soil freeze-thaw cycles on roots and root-associated fungi of Holcus lanatus and Calluna vulgaris. Plant Soil 353:19–31

    CAS  Article  Google Scholar 

  • Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669

    CAS  Article  PubMed  Google Scholar 

  • Lambers H, Chapin FS, Pons TL (1998) Plant Physiological Ecology. Springer, New York

    Book  Google Scholar 

  • Li M, Qin C, Welti R, Wang X (2006) Double knockouts of phospholipases DZ1 and DZ2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140:761–770

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Li X et al (2011) Root biomass distribution in alpine ecosystems of the northern Tibetan Plateau. Environ Earth Sci 64:1911–1919

    Article  Google Scholar 

  • Liao M, Palta JA, Fillery IRP (2006) Root characteristics of vigorous wheat improve early nitrogen uptake. Aust J Agric Res 57:1097–1107

    Article  Google Scholar 

  • Liu J, Chen F, Olokhnuud C, Adm G, Tong Y, Zhang F, Mi G (2009) Root size and nitrogen-uptake activity in two maize (Zea mays) inbred lines differing in nitrogen-use efficiency. J Plant Nutr Soil Sci 172:230–236

    CAS  Article  Google Scholar 

  • Lõhmus K et al. (2006) Black alder as a promising deciduous species for the reclaiming of oil shale mining areas. Brownfields III. Prevention, assessment, rehabilitation and development of Brownfield sites. Southampton: WIT Press

  • Lu X, Yan Y, Fan J, Wang X (2012) Gross Nitrification and Denitrification in Alpine Grassland Ecosystems on the Tibetan Plateau. Arct Antarct Alp Res 44:188–196

    Article  Google Scholar 

  • Luo J et al (2013) Net fluxes of ammonium and nitrate in association with H + fluxes in fine roots of Populus popularis. Planta 237:919–931

    CAS  Article  PubMed  Google Scholar 

  • Luo HH, Tao XP, Hu YY, Zhang YL, Zhang WF (2015) Response of cotton root growth and yield to root restriction under various water and nitrogen regimes. J Plant Nutr Soil Sci 178:384–392

    CAS  Article  Google Scholar 

  • Maire V, Gross N, Pontes LDS, Picon-Cochard C, Soussana JF (2009) Trade-off between root nitrogen acquisition and shoot nitrogen utilization across 13 co-occurring pasture grass species. Funct Ecol 23:668–679

    Article  Google Scholar 

  • Mccormack ML et al (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505

    Article  PubMed  Google Scholar 

  • McKane RB et al (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    CAS  Article  PubMed  Google Scholar 

  • Ostonen I et al (2006) Morphological adaptations of fine roots in Scots pine (Pinus sylvestris L.), silver birch (Betula pendula Roth.) and black alder (Alnus glutinosa (L.) Gaertn.) stands in recultivated areas of oil shale mining and semicoke hills. Oil Shale 23:187–202

    Google Scholar 

  • Ostonen I et al (2007) Specific root length as an indicator of environmental change Plant. Biosystems 141:426–442

    Google Scholar 

  • Raab TK, Lipson DA, Monson RK (1996) Non-mycorrhizal uptake of amino acids by roots of the alpine sedge Kobresia myosurides: Implications for the alpine nitrogen cycle. Oecologia 108:488–494

    Article  PubMed  Google Scholar 

  • Ran Y, Erez A (1992) Root volume influence on dry matter production and partitioning as related to nitrogen and water uptake rates by peach trees. J Plant Nutr 15:713–726

    CAS  Article  Google Scholar 

  • Ran Y, Habib R, Bar B (1994) Root volume effects on nitrogen uptake and partitioning in peach trees. Agron J 86:530–534

    Article  Google Scholar 

  • Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: Plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291

    Article  Google Scholar 

  • Ricroch A, Chopra S, Fleischer S (2014) Plant biotechnology: experience and future prospects. Springer, Berlin

    Book  Google Scholar 

  • Roumet C, Lafont F, Sari M, Warembourg F, Garnier E (2008) Root traits and taxonomic affiliation of nine herbaceous species grown in glasshouse conditions. Plant Soil 312:69–83

    CAS  Article  Google Scholar 

  • Ryser P (2006) The mysterious root length. Plant Soil 286:1–6

    CAS  Article  Google Scholar 

  • Schamp B, Chau J, Aarssen L (2008) Dispersion of traits related to competitive ability in an old-field plant community. J Ecol 96:204–212

    Google Scholar 

  • Schenk MK (1996) Regulation of nitrogen uptake on the whole plant level. Plant Soil 181:131–137

    CAS  Article  Google Scholar 

  • Schoeny A, Deviennebarret F, Jeuffroy MH, Lucas P (2003) Effect of take-all root infections on nitrate uptake in winter wheat. Plant Pathol 52:52–59

    Article  Google Scholar 

  • Senwo ZN, Tabatabai MA (1998) Amino acid composition of soil organic matter. Biol Fertil Soils 26:235–242

    CAS  Article  Google Scholar 

  • Templer PH (2012) Changes in winter climate: soil frost, root injury, and fungal communities. Plant Soil 353:15–17

    CAS  Article  Google Scholar 

  • Tran TT, Kano-Nakata M, Suralta RR, Menge D, Mitsuya S, Inukai Y, Yamauchi A (2015) Root plasticity and its functional roles were triggered by water deficit but not by the resulting changes in the forms of soil N in rice. Plant Soil 386:65–76

    CAS  Article  Google Scholar 

  • Vogt KA, Persson H (1991) Measuring growth and development of roots. Techniques and approaches in forest tree ecophysiology. CRC Press, Boca Raton

    Google Scholar 

  • Wang K-b, Li J-p, Shangguan Z-p (2012a) Biomass Components and Environmental Controls in Ningxia Grasslands. J Integr Agric 11:2079–2087

    Article  Google Scholar 

  • Wang W, Ma Y, Xu J, Wang H, Zhu J, Zhou H (2012b) The uptake diversity of soil nitrogen nutrients by main plant species in Kobresia humilis alpine meadow on the Qinghai-Tibet Plateau. Science China. Earth Sci 55:1688–1695

    CAS  Google Scholar 

  • Weigelt A, Bol R, Bardgett RD (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635

    Article  PubMed  Google Scholar 

  • Withington JM, Reich PB, Oleksyn J, Eissenstat DM (2006) Comparisons of structure and life span in roots and leaves among temperate trees. Ecol Monogr 76:381–397

    Article  Google Scholar 

  • Wu J, Pagès L, Wu Q, Yang B, Guo Y (2014) Three-dimensional architecture of axile roots of field-grown maize. Plant Soil 387:1–15

    Google Scholar 

  • Wurzburger N, Wright SJ (2015) Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96:2137

    Article  PubMed  Google Scholar 

  • Xu X, Ouyang H, Cao G, Richter A, Wanek W, Kuzyakov Y (2010) Dominant plant species shift their nitrogen uptake patterns in response to nutrient enrichment caused by a fungal fairy in an alpine meadow. Plant Soil 341:495–504

    Article  Google Scholar 

  • Zhu Q, Zhuang Q (2013) Modeling the effects of organic nitrogen uptake by plants on the carbon cycling of boreal forest and tundra ecosystems. Biogeosciences 10:7943–7955

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the State Key Research Development Program of China (2016YFC0502002), the National Natural Science Foundation of China (41701343), the 135 Key Cultivation Program of the Institute of Mountain Hazard and Environment (2017–2020) and the Chinese Academy of Sciences Light of West China program (2017–2019).

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Correspondence to Xiaodan Wang.

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Hong, J., Ma, X., Yan, Y. et al. Which root traits determine nitrogen uptake by alpine plant species on the Tibetan Plateau?. Plant Soil 424, 63–72 (2018). https://doi.org/10.1007/s11104-017-3434-3

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  • DOI: https://doi.org/10.1007/s11104-017-3434-3

Keywords

  • Ammonium nitrogen
  • Nitrate nitrogen
  • Glycine
  • Root morphology
  • Nitrogen absorption