Skip to main content

Nitrogen ion form and spatio-temporal variation in root distribution mediate nitrogen effects on lifespan of ectomycorrhizal roots

Abstract

Background and Aims

Absorptive roots active in soil resource uptake are often intimately associated with mycorrhizal fungi, yet it remains unclear how nitrogen (N) loading affects lifespan of absorptive roots associating with ectomycorrhizal (ECM) fungi.

Methods

Through a three-year minirhizotron experiment, we investigated the responses of ECM lifespan to different rates of N addition and examined the roles of N ion form, rooting depth, seasonal root cohort, and ECM morphotype in mediating the N effects on ECM lifespan in a slash pine (Pinus elliottii) forest in subtropical China.

Results

High rates of NH4Cl significantly decreased foliar P concentrations and increased foliar N:P ratios, and mean ECM lifespan was negatively correlated to foliar P concentration. N additions generally increased the lifespan of most ectomycorrhizas, but the specific differences were context dependent. N rates and forms exerted significant positive effects on ECM lifespan with stronger effects occurring at high N rates and under ammonium N addition. N additions extended lifespan of ectomycorrhizas in shallower soil and born in spring and autumn, but shortened lifespan of ectomycorrhizas in deeper soil and born in summer and winter. N additions reduced lifespan of dichotomous ectomycorrhizas, but increased lifespan of coralloid ectomycorrhizas.

Conclusions

The increased ECM lifespan in response to N additions may primarily be driven by the persistent and aggravated P limitation to plants. Our findings highlight the importance of environmental contexts in controlling ECM lifespan and the need to consider potential differences among mycorrhizal morphotypes when studying N—lifespan relationships of absorptive roots in the context of N deposition.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. Bioscience 39:378–386

    Article  Google Scholar 

  2. Adams TS, Eissenstat DM (2015) On the controls of root lifespan: assessing the role of soluble phenolics. Plant Soil 392:301–308

    CAS  Article  Google Scholar 

  3. Adams TS, McCormack ML, Eissenstat DM (2013) Foraging strategies in trees of different root morphology: the role of root lifespan. Tree Physiol 33:940–948

    CAS  Article  PubMed  Google Scholar 

  4. Agerer R (1991) Characteristics of ectomycorrhiza. In: Norris JR, Read DJ, Varma AK (eds) Methods in microbiology, vol vol 23. Academic Press, New York, pp. 25–73

    Google Scholar 

  5. Baddeley JA, Watson CA (2005) Influences of root diameter, tree age, soil depth and season on fine root survivorship in Prunus avium. Plant Soil 276:15–22

    CAS  Article  Google Scholar 

  6. Bai WM, Wang ZW, Chen QS, Zhang WH, Li LH (2008) Spatial and temporal effects of nitrogen addition on root life span of Leymus chinensis in a typical steppe of Inner Mongolia. Funct Ecol 22:583–591

    Article  Google Scholar 

  7. Baldi E, Toselli M, Eissenstat DM, Marangoni B (2010) Organic fertilization leads to increased peach root production and lifespan. Tree Physiol 30:1373–1382

    CAS  Article  PubMed  Google Scholar 

  8. Bauer GA, Bazzaz FA, Minocha R, Long S, Magill A, Aber J, Berntson GM (2004) Effects of chronic N additions on tissue chemistry, photosynthetic capacity, and carbon sequestration potential of a red pine (Pinus resinosa Ait.) stand in the NE United States. Forest Ecol Manag 196:173–186

    Article  Google Scholar 

  9. Braun S, Thomas VFD, Quiring R, Fluckiger W (2010) Does nitrogen deposition increase forest production? The role of phosphorus. Environ Pollut 158:2043–2052

    CAS  Article  PubMed  Google Scholar 

  10. Bünemann EK, Oberson A, Frossard E (2011) Phosphorus in action: biological processes in soil phosphorus cycling. Springer, Berlin

    Book  Google Scholar 

  11. Burton AJ, Pregitzer KS, Hendrick RL (2000) Relationships between fine root dynamics and nitrogen availability in Michigan northern hardwood forests. Oecologia 125:389–399

    Article  Google Scholar 

  12. Burton AJ, Pregitzer KS, Ruess RW, Hendrik RL, Allen MF (2002) Root respiration in north American forests: effects of nitrogen concentration and temperature across biomes. Oecologia 131:559–568

    Article  Google Scholar 

  13. Burton AJ, Jarvey JC, Jarvi MP, Zak DR, Pregitzer KS (2012) Chronic N deposition alters root respiration-tissue N relationship in northern hardwood forests. Glob Chang Biol 18:258–266

    Article  Google Scholar 

  14. Cox DR (1972) Regression models and life-tables. J Roy Stat Soc B 34:187–220

    Google Scholar 

  15. Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. P Natl Acad Sci USA 98:13454–13459

    CAS  Article  Google Scholar 

  16. Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60

    Article  Google Scholar 

  17. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LJ (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550

    Article  Google Scholar 

  18. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Fernandez CW, McCormack ML, Hill JM, Pritchard SG, Koide RT (2013) On the persistence of Cenococcum geophilum ectomycorrhizas and its implications for forest carbon and nutrient cycles. Soil Biol Biochem 65:141–143

    CAS  Article  Google Scholar 

  20. Finlay RD, Ek H, Odham G, Söderström B (1989) Uptake, translocation and assimilation of nitrogen from 15N-labelled ammonium and nitrate sources by intact ectomycorrhizal systems of Fagus sylvatica infected with Paxillus involutus. New Phytol 113:47–55

    CAS  Article  Google Scholar 

  21. Gao WL, Kou L, Zhang JB, Müller C, Wang HM, Yang H, Li SG (2016) Enhanced deposition of nitrate alters microbial cycling of N in a subtropical forest soil. Biol Fert Soils in press

  22. Grassein F, Lemauviel-Lavenant S, Lavorel S, Bahn M, Bardgett RD, Desclos-Theveniau M, Laine P (2015) Relationships between functional traits and inorganic nitrogen acquisition among eight contrasting European grass species. Ann Bot 115:107–115

    Article  PubMed  Google Scholar 

  23. Guo DL, Mitchell RJ, Withington JM, Fan PP, Hendricks JJ (2008a) Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. J Ecol 96:737–745

    CAS  Article  Google Scholar 

  24. Guo DL, Xia MX, Wei X, Chang WJ, Liu Y, Wang ZQ (2008b) 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 

  25. Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  Google Scholar 

  26. Hansson K, Helmisaari HS, Sah SP, Lange H (2013) Fine root production and turnover of tree and understorey vegetation in scots pine, silver birch and Norway spruce stands in SW Sweden. Forest Ecol Manag 309:58–65

    Article  Google Scholar 

  27. Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285

    CAS  Article  Google Scholar 

  28. Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Nitrogen capture by plants grown in N-rich organic patches of contrasting size and strength. J Exp Bot 50:1243–1252

    CAS  Article  Google Scholar 

  29. IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  30. Kaplan EL, Meier P (1958) Nonparametric-estimation from incomplete observations. J Am Stat Assoc 53:457–481

    Article  Google Scholar 

  31. Kauserud H, Heegaard E, Büntgen U, Halvorsen R, Egli S, Senn-Irlet B, Krisai-Greilhuber I, Dämon W, Sparks T, Nordén J (2012) Warming-induced shift in European mushroom fruiting phenology. Proc Natl Acad Sci USA 109:14488–14493

  32. Koide RT, Shumway DL, Xu B, Sharda JN (2007) On temporal partitioning of a community of ectomycorrhizal fungi. New Phytol 174:420–429

  33. Kou L, Chen WW, Gao WL, Yang H, Wang HM, Li SG (2015a) Effects of mixture of branch order-based roots and nitrogen addition on root decay in a subtropical pine plantation. Biol Fertil Soils 51:947–957

    CAS  Article  Google Scholar 

  34. Kou L, Guo DL, Yang H, Gao WL, Li SG (2015b) Growth, morphological traits and mycorrhizal colonization of fine roots respond differently to nitrogen addition in a slash pine plantation in subtropical China. Plant Soil 391:207–218

    CAS  Article  Google Scholar 

  35. Kubisch P, Hertel D, Leuschner C (2015) Do ectomycorrhizal and arbuscular mycorrhizal temperate tree species systematically differ in root order-related fine root morphology and biomass? Front Plant Sci 6:1–12

  36. Liu BT, Li HB, Zhu BA, 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 

  37. López B, Sabaté S, Gracia CA (2001) Fine-root longevity of Quercus ilex. New Phytol 151:437–441

    Article  Google Scholar 

  38. Majdi H, Andersson P (2005) Fine root production and turnover in a Norway spruce stand in northern Sweden: effects of nitrogen and water manipulation. Ecosystems 8:191–199

    CAS  Article  Google Scholar 

  39. Majdi H, Nylund JE (1996) Does liquid fertilization affect fine root dynamics and lifespan of mycorrhizal short roots? Plant Soil 185:305–309

    CAS  Article  Google Scholar 

  40. Matson PA, McDowell WH, Townsend AR, Vitousek PM (1999) The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46:67–83

    CAS  Google Scholar 

  41. McCormack ML, Guo DL (2014) Impacts of environmental factors on fine root lifespan. Front Plant Sci 5:1–11

  42. McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195:823–831

    Article  Google Scholar 

  43. McCormack ML, Adams TS, Smithwick EA, Eissenstat DM (2014) Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95:2224–2235

    Article  PubMed  Google Scholar 

  44. McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo DL, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518

    Article  PubMed  Google Scholar 

  45. Megda MXV, Mariano E, Leite JM, Megda MM, Trivelin PCO (2014) Chloride ion as nitrification inhibitor and its biocidal potential in soils. Soil Biol Biochem 72:84–87

    Article  Google Scholar 

  46. Nadelhoffer KJ (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147:131–139

    CAS  Article  Google Scholar 

  47. Nordin A, Hogberg P, Nasholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–132

    Article  Google Scholar 

  48. Pregitzer KS, Hendrick RL, Fogel R (1993) The demography of fine roots in response to patches of water and nitrogen. New Phytol 125:575–580

    Article  Google Scholar 

  49. 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 

  50. Pritchard SG, Taylor BN, Cooper ER, Beidler KV, Strand AE, Mccormack ML, Zhang SY (2014) Long-term dynamics of mycorrhizal root tips in a loblolly pine forest grown with free-air CO2 enrichment and soil N fertilization for 6 years. Glob Chang Biol 20:1313–1326

    Article  PubMed  Google Scholar 

  51. Recous S, Machet JM, Mary B (1992) The partitioning of fertilizer-N between soil and crop: comparison of ammonium and nitrate applications. Plant Soil 144:101–111

    CAS  Article  Google Scholar 

  52. Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado JL (2008) Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecol Lett 11:793–801

    Article  PubMed  Google Scholar 

  53. Rygiewicz PT, Johnson MG, Ganio LM, Tingey DT, Storm MJ (1997) Lifetime and temporal occurrence of ectomycorrhizae on ponderosa pine (Pinus ponderosa Laws) seedlings grown under varied atmospheric CO2 and nitrogen levels. Plant Soil 189:275–287

    CAS  Article  Google Scholar 

  54. See CR, Yanai RD, Fisk MC, Vadeboncoeur MA, Quintero BA, Fahey TJ (2015) Soil nitrogen affects phosphorus recycling: foliar resorption and plant-soil feedbacks in a northern hardwood forest. Ecology 96:2488–2498

    Article  PubMed  Google Scholar 

  55. Smithwick EAH, Eissenstat DM, Lovett GM, Bowden RD, Rustad LE, Driscoll CT (2013) Root stress and nitrogen deposition: consequences and research priorities. New Phytol 197:712–719

    CAS  Article  PubMed  Google Scholar 

  56. Soudzilovskaia NA, Douma JC, Akhmetzhanova AA, Bodegom PM, Cornwell WK, Moens EJ, Treseder KK, Tibbett M, Wang YP, Cornelissen JH (2015) Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob Ecol Biogeogr 24:371–382

    Article  Google Scholar 

  57. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355

    Article  Google Scholar 

  58. Wang YD, Wang ZL, Wang HM, Guo CC, Bao WK (2012) Rainfall pulse primarily drives litterfall respiration and its contribution to soil respiration in a young exotic pine plantation in subtropical China. Can J For Res 42:657–666

    Article  Google Scholar 

  59. Wang M, Murphy MT, Moore TR (2014) Nutrient resorption of two evergreen shrubs in response to long-term fertilization in a bog. Oecologia 174:365–377

    Article  PubMed  Google Scholar 

  60. Wang JJ, Tharayil N, Chow AT, Suseela V, Zeng H (2015) Phenolic profile within the fine-root branching orders of an evergreen species highlights a disconnect in root tissue quality predicted by elemental- and molecular-level carbon composition. New Phytol 206:1261–1273

    CAS  Article  PubMed  Google Scholar 

  61. Wells CE, Glenn DM, Eissenstat DM (2002) Changes in the risk of fine-root mortality with age: a case study in peach, Prunus persica (Rosaceae. Am J Bot 89:79–87

    Article  PubMed  Google Scholar 

  62. Wen XF, Wang HM, Wang JL, GR Y, Sun XM (2010) Ecosystem carbon exchanges of a subtropical evergreen coniferous plantation subjected to seasonal drought, 2003-2007. Biogeosciences 7:357–369

    CAS  Article  Google Scholar 

  63. 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 

  64. Xia MX, Guo DL, Pregitzer KS (2010) Ephemeral root modules in Fraxinus mandshurica. New Phytol 188:1065–1074

    Article  PubMed  Google Scholar 

  65. Xiong YM, Fan PP, SL F, Zeng H, Guo DL (2013) Slow decomposition and limited nitrogen release by lower order roots in eight Chinese temperate and subtropical trees. Plant Soil 363:19–31

    CAS  Article  Google Scholar 

  66. Zhu JX, He NP, Wang QF, Yuan GF, Wen D, GR Y, Jia YL (2015) The composition, spatial patterns, and influencing factors of atmospheric wet nitrogen deposition in Chinese terrestrial ecosystems. Sci Total Environ 511:777–785

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research is financially supported by the grants from the National Natural Science Foundation of China (No. 31130009), the National Key Research and Development Plan (No. 2016YFD06000202), and the Key Frontier Science Program of Chinese Academy of Sciences (QYJ-DQ098). The authors acknowledge the contributions of the anonymous reviewers.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Shenggong Li.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Responsible Editor: Thom W. Kuyper.

Electronic supplementary material

ESM 1

(DOCX 2208 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kou, L., McCormack, M.L., Chen, W. et al. Nitrogen ion form and spatio-temporal variation in root distribution mediate nitrogen effects on lifespan of ectomycorrhizal roots. Plant Soil 411, 261–273 (2017). https://doi.org/10.1007/s11104-016-3018-7

Download citation

Keywords

  • Absorptive roots
  • Ectomycorrhizas
  • Median lifespan
  • Morphotype
  • Nitrogen deposition