Nutrient allocation and photochemical responses of Populus × canadensis ‘Neva’ to nitrogen fertilization and exogenous Rhizophagus irregularis inoculation

  • Fei Wu
  • Haoqiang Zhang
  • Fengru Fang
  • Ming TangEmail author
Original Article


Arbuscular mycorrhizal fungi (AMF) can promote plant growth performance, but their effectiveness varies depending on soil nitrogen (N) availability. To clarify the effectiveness of exogenous AMF along an N-fertilization gradient (0, 2, 10, 20, and 30 mM), the impacts of exogenous Rhizophagus irregularis and N on the growth, photochemical activity, and nutritional status of Populus × canadensis ‘Neva’ in natural soil were evaluated in a pot experiment. The results showed that the 10 mM N level was the optimal fertilization regime with the highest promotion effect on plant growth and the maximum quantum yield of photosystem II (PSII) (Fv/Fm). Excess N (20 and 30 mM) fertilization reduced the actual quantum yield of PSII (ФPSII) and the Fv/Fm of the plants. Regardless of the N availability, inoculated plants exhibited greater Fv/Fm values than did non-inoculated plants. The biomass of inoculated plants was significantly higher compared with the control under low N levels (0 and 2 mM). Under high N levels, inoculated plants showed significant increases in ФPSII. Moreover, the nutrient imbalance of plants inoculated with exogenous R. irregularis was eased by increasing P, Fe, Mn and Cu uptake in roots and higher P, Ca, Mg, Fe, Mn and Zn concentrations in leaves. Moreover, the Fv/Fm and ФPSII exhibited positive correlations with P, Ca, Mg and Zn concentrations in leaves. In conclusion, inoculation with exogenous R. irregularis can benefit plant fitness by improving the photochemical capacity and nutrient composition of poplar under different N levels.


Nitrogen fertilization Arbuscular mycorrhiza Poplar Chlorophyll fluorescence Nutrient allocation 



This study was supported by the National Natural Science Foundation of China (41671268 and 31270639), and the Shaanxi Science and Technology Innovation Project Plan (2016KTCL02-07).

Compliance with ethical standards

Conflict of interest

The author(s) declare no conflict of interest.

Supplementary material

11738_2018_2728_MOESM1_ESM.xlsx (12 kb)
Supplementary material 1 (XLSX 12 KB)
11738_2018_2728_MOESM2_ESM.pdf (619 kb)
Supplementary material 2 (PDF 619 KB)


  1. Azcón R, Ambrosano E, Charest C (2003) Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci 165:1137–1145. CrossRefGoogle Scholar
  2. Bago B, Cano C, Azcón-Aguilar C, Samson J, Coughlan AP, Piche Y (2004) Differential morphogenesis of the extraradical mycelium of an arbuscular mycorrhizal fungus grown monoxenically on spatially heterogeneous culture media. Mycologia 96:452–462. CrossRefPubMedGoogle Scholar
  3. Barunawati N, Giehl RFH, Bauer B, von Wirén N (2013) The influence of inorganic nitrogen fertilizer forms on micronutrient retranslocation and accumulation in grains of winter wheat. Front Plant Sci 4:320. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bati CB, Santilli E, Lombardo L (2015) Effect of arbuscular mycorrhizal fungi on growth and on micronutrient and macronutrient uptake and allocation in olive plantlets growing under high total Mn levels. Mycorrhiza 25:97–108. CrossRefGoogle Scholar
  5. Brooker R, Kikvidze Z, Pugnaire FI, Callaway RM, Choler P, Lortie CJ et al (2005) The importance of importance. Oikos 109:63–70. CrossRefGoogle Scholar
  6. Cabral C, Ravnskov S, Tringovska I, Wollenweber B (2016) Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress. Plant Soil 408:385–399. CrossRefGoogle Scholar
  7. Carvalho LM, Cacador I, Martins-Loucao MA (2006) Arbuscular mycorrhizal fungi enhance root cadmium and copper accumulation in the roots of the salt marsh plant Aster tripolium L. Plant Soil 285:161–169. CrossRefGoogle Scholar
  8. Cely MVT, de Oliveira AG, de Freitas VF, de Luca MB, Barazetti AR, dos Santos IMO et al (2016) Inoculant of arbuscular mycorrhizal fungi (Rhizophagus clarus) increase yield of soybean and cotton under field conditions. Front Microbiol 7:720. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Corrêa A, Cruz C, Ferrol N (2015) Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown. Mycorrhiza 25:499–515. CrossRefPubMedGoogle Scholar
  10. Cooke JEK, Martin TA, Davis JM (2005) Short-term physiological and developmental responses to nitrogen availability in hybrid poplar. New Phytol 167:41–52. CrossRefPubMedGoogle Scholar
  11. Fonseca HMAC, Berbara RLL, Daft MJ (2001) Shoot δ15N and δ13C values of non-host Brassica rapa change when exposed to ± Glomus etunicatum inoculum and three levels of phosphorus and nitrogen. Mycorrhiza 11:151–158. CrossRefPubMedGoogle Scholar
  12. Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327. CrossRefGoogle Scholar
  13. He JL, Li H, Ma CF, Zhang YL, Polle A, Rennenberg H et al (2015) Overexpression of bacterial gamma-glutamylcysteine synthetase mediates changes in cadmium influx, allocation and detoxification in poplar. New Phytol 205:240–254. CrossRefPubMedGoogle Scholar
  14. Hoopen FT, Cuin TA, Pedas P, Hegelund JN, Shabala S, Schjoerring JK et al (2010) Competition between uptake of ammonium and potassium in barley and arabidopsis roots: molecular mechanisms and physiological consequences. J Exp Bot 61:2303–2315. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hu JL, Lin XG, Wang JH, Dai J, Cui XC, Chen RR et al (2009) Arbuscular mycorrhizal fungus enhances crop yield and P-uptake of maize (Zea mays L.): a field case study on a sandy loam soil as affected by long-term P-deficiency fertilization. Soil Biol Biochem 41:2460–2465. CrossRefGoogle Scholar
  16. Johansen A, Jakobsen I, Jensen ES (1994) Hyphal N transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at 3 nitrogen levels. Plant Soil 160:1–9. CrossRefGoogle Scholar
  17. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647. CrossRefPubMedGoogle Scholar
  18. Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M et al (2014) Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol Bioch 81:16–25. CrossRefGoogle Scholar
  19. Labidi S, Ben Jeddi F, Tisserant B, Yousfi M, Sanaa M, Dalpe Y et al (2015) Field application of mycorrhizal bio-inoculants affects the mineral uptake of a forage legume (Hedysarum coronarium L.) on a highly calcareous soil. Mycorrhiza 25:297–309. CrossRefPubMedGoogle Scholar
  20. Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology. Springer, New YorkCrossRefGoogle Scholar
  21. Li CY, Korpelainen H (2015) Transcriptomic regulatory network underlying morphological and physiological acclimation to nitrogen starvation and excess in poplar roots and leaves. Tree Physiol 35:1279–1282. CrossRefPubMedGoogle Scholar
  22. Li Z, Wu N, Liu T, Chen H, Tang M (2015) Effect of arbuscular mycorrhizal inoculation on water status and photosynthesis of Populus cathayana males and females under water stress. Physiol Plant 155:192–204. CrossRefPubMedGoogle Scholar
  23. Liu T, Wang CY, Chen H, Fang FR, Zhu XQ, Tang M (2014) Effects of arbuscular mycorrhizal colonization on the biomass and bioenergy production of Populus × canadensis ‘Neva’ in sterilized and unsterilized soil. Acta Physiol Plant 36:871–880. CrossRefGoogle Scholar
  24. Marulanda A, Azcón R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533. CrossRefGoogle Scholar
  25. Mauromicale G, Ierna A, Marchese M (2006) Chlorophyll fluorescence and chlorophyll content in field-grown potato as affected by nitrogen supply, genotype, and plant age. Photosynthetica 44:76–82. CrossRefGoogle Scholar
  26. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. CrossRefPubMedGoogle Scholar
  27. McGonigle T, Miller M, Evans D, Fairchild G, Swan J (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501CrossRefGoogle Scholar
  28. Mechri B, Cheheb H, Boussadia O, Attia F, Ben Mariem F, Braham M et al (2011) Effects of agronomic application of olive mill wastewater in a field of olive trees on carbohydrate profiles, chlorophyll a fluorescence and mineral nutrient content. Environ Exp Bot 71:184–191. CrossRefGoogle Scholar
  29. Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364. CrossRefGoogle Scholar
  30. Nakaji T, Fukami M, Dokiya Y, Izuta T (2001) Effects of high nitrogen load on growth, photosynthesis and nutrient status of Cryptomeria japonica and Pinus densiflora seedlings. Trees 15:453–461. CrossRefGoogle Scholar
  31. Osmond C (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Photoinhibition of photosynthesis from molecular mechanisms to the field. Bios. Scientific Publishers, Oxford, pp 1–24Google Scholar
  32. Pegoraro RF, Oliveira D, Moreira GBL, Kondo MK, Maia VM, Vieira NMB (2013) Absorption, accumulation and export of macronutrients by common bean irrgated, and influenced by nitrogen fertilization. J Agr Sci 5:34–48. CrossRefGoogle Scholar
  33. Pellegrino E, Turrini A, Gamper HA, Cafà G, Bonari E, Young JPW et al (2012) Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytol 194:810–822. CrossRefPubMedGoogle Scholar
  34. Philippot L, Raaijmakers JM, Lemanceau P, van der Puttern WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. CrossRefPubMedGoogle Scholar
  35. Phillips J, Hayman D (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–N118CrossRefGoogle Scholar
  36. Rockström J, Steffen W, Noone K, Persson A, Chapin FS, Lambin EF et al (2009) A safe operating space for humanity. Nature 461:472–475. CrossRefPubMedGoogle Scholar
  37. Sheng M, Tang M, Chen H, Yang BW, Zhang FF, Huang YH (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296. CrossRefPubMedGoogle Scholar
  38. Smethurst CF, Garnett T, Shabala S (2005) Nutritional and chlorophyll fluorescence responses of lucerne (Medicago sativa) to waterlogging and subsequent recovery. Plant Soil 270:31–45. CrossRefGoogle Scholar
  39. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New YorkGoogle Scholar
  40. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. CrossRefPubMedGoogle Scholar
  41. Sýkorová Z, Börstler B, Zvolenská S, Fehrer J, Gryndler M, Vosátka M, Redecker D (2012) Long-term tracing of Rhizophagus irregularis isolate BEG140 inoculated on Phalaris arundinacea in a coal mine spoil bank, using mitochondrial large subunit rDNA markers. Mycorrhiza 22:69–80. CrossRefPubMedGoogle Scholar
  42. Szczerba MW, Britto DT, Ali SA, Balkos KD, Kronzucker HJ (2008) NH4 +-stimulated and-inhibited components of K+ transport in rice (Oryza sativa L.). J Exp Bot 59:3415–3423. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. CrossRefGoogle Scholar
  44. Treseder KK (2013) The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil 371:1–13. CrossRefGoogle Scholar
  45. Treseder KK, Allen MF (2002) Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and feld test. New Phytol 155:507–515. CrossRefGoogle Scholar
  46. van den Driessche R (1999) First-year growth response of four Populus trichocarpa × Populus deltoides clones to fertilizer placement and level. Can J Forest Res 29:554–562. CrossRefGoogle Scholar
  47. Wu F, Zhang H, Fang F, Liu H, Tang M (2017a) Arbuscular mycorrhizal fungi alter nitrogen allocation in the leaves of Populus × canadensis ‘Neva’. Plant Soil 421:477–491. CrossRefGoogle Scholar
  48. Wu F, Zhang H, Fang F, Wu N, Zhang Y, Tang M (2017b) Effects of nitrogen and exogenous Rhizophagus irregularis on the nutrient status, photosynthesis and leaf anatomy of Populus × canadensis ‘Neva’. J Plant Growth Regul 36:824–835. CrossRefGoogle Scholar
  49. Zhang X, Misra A, Nargund S, Coleman GD, Sriram G (2018) Concurrent isotope-assisted metabolic flux analysis and transcriptome profiling reveal responses of poplar cells to altered nitrogen and carbon supply. Plant J 93:472–488. CrossRefPubMedGoogle Scholar
  50. Zhou XJ, Liang Y, Chen H, Shen SH, Ding YX (2006) Effects of rhizobia inoculation and nitrogen fertilization on photosynthetic physiology of soybean. Photosynthetica 44:530–535. CrossRefGoogle Scholar
  51. Zhu XC, Song FB, Liu SQ, Liu TD (2011) Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 346:189–199. CrossRefGoogle Scholar
  52. 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 52:247–252. CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  • Fei Wu
    • 1
    • 2
  • Haoqiang Zhang
    • 2
  • Fengru Fang
    • 2
  • Ming Tang
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess PlateauNorthwest A&F UniversityXianyangChina
  2. 2.College of ForestryNorthwest A&F UniversityXianyangChina

Personalised recommendations