, Volume 30, Issue 2, pp 405–413 | Cite as

Aluminum effect on starch, soluble sugar, and phytohormone in roots of Quercus serrata Thunb. seedlings

  • Ubuki Moriyama
  • Rie TomiokaEmail author
  • Mikiko Kojima
  • Hitoshi Sakakibara
  • Chisato Takenaka
Original Article


Key message

Glucose was a key substance as an energy source in the root growth promotion by Al, and ABA may relate to metabolism involved with its process.


Generally, excess aluminum (Al) ions in soil solution are toxic to many cultivated plant species, but beneficial effects of Al for plant growth have been reported. Previously, we reported stimulation of root growth and nitrate reductase (NR) activity by Al. In this study, we focused on sugars, such as sucrose, glucose, and fructose, as energy sources and also signaling substances to regulate root growth. To understand the mechanism of root growth stimulation by Al, we investigated the change in concentration of sugars and phytohormones, and the activity of NR in roots using Quercus serrata seedlings. Ten-week-old Q. serrata seedlings were hydroponically cultured with nutrient solution containing 2.5 mM Al (pH 4.0) or 3.25 mM calcium (Ca) (pH 4.0) for 3 and 15 days. The growth of first lateral root and NR activity was stimulated for 3 and 15 days of Al treatment. The concentration of starch and sucrose decreased, while the concentration of glucose increased in the Al-treated roots. The concentration of abscisic acid (ABA) in Al-treated roots increased gradually throughout the experiment. From the present study, the mechanism of root growth promotion by Al involves a complex signaling network. We suggest that glucose is a key substance as an energy source and a signaling substance to promote root growth induced by Al and ABA may relate to nitrogen (N) and carbon (C) metabolism involved with the signaling network to promote root growth induced by Al.


Sucrose Glucose Abscisic acid Aluminum Quercus serrata 



We thank Dr Kunio Yamada (Chubu University), Dr Katsuhiro Shiratake and Kayoko Miyashita (Nagoya University), and Dr Takafumi Tezuka for valuable advice and support to analysis of carbohydrates.


  1. Abdalla MM (2008) Physiological aspects of aluminium toxicity on some metabolic and hormonal contents of Hordum Vulgare seedlings. Aust J Basic Appl Sci 2(3):549–560Google Scholar
  2. Abou-Hadid AF, Abd-Elmoniem EM, EL-Shinawy MZ, Abou-Elsoud M (1996) Electrical conductivity effect on growth and mineral composition of lettuce plants in hydroponic system. Acta Hort 434:59–66CrossRefGoogle Scholar
  3. Aslam M, Oaks A (1975) Effect of glucose on the induction of nitrated reductase in corn roots. Plant Physiol 56:634–639CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bhatia S, Singh R (2000) Calcium-mediated conversion of sucrose to starch in relation to the activities of amylases and sucrose-metabolizing enzymes in sorghum grains raised through liquid culture. Indian J Biochem Bio 37(2):135–139Google Scholar
  5. Bhatia S, Singh R (2002) Phytohormone-mediated transformation of sugars to starch in relation to the activities of amylases, sucrose-metabolising enzymes in sorghum grain. Plant Growth Regul 36(2):97–104CrossRefGoogle Scholar
  6. Bortel A, Kaiser WM (1997) Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status. Planta 201:496–501CrossRefGoogle Scholar
  7. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743. doi: 10.1105/tpc.006494 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321PubMedPubMedCentralGoogle Scholar
  9. Foy CD, Fleming AL (1982) Aluminum tolerance of two wheat genotypes related to nitrate reductase activities. J Plant Nutr 5:1313–1333CrossRefGoogle Scholar
  10. Gazzarrini S, McCourt P (2001) Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr Opin Plant Biol 4:387–391CrossRefPubMedGoogle Scholar
  11. Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102. doi: 10.1016/j.pbi.2004.11.003 CrossRefPubMedGoogle Scholar
  12. Goupil P, Loncle D, Druart N, Bellettre A, Rambour S (1998) Influence of ABA on nitrate reductase activity and carbohydrate metabolism in chicory roots (Cichorium intybus L.). J Exp Bot 49:1885–1886CrossRefGoogle Scholar
  13. Graham CJ (2002) Nonstructural carbohydrate and prunasin composition of peach seedlings fertilized with different nitrogen sources and aluminum. Sci Hortic Amsterdam 94:21–32CrossRefGoogle Scholar
  14. Hageman RH, Reed AJ (1980) Nitrate reductase from higher plants. Method Enzymol 69:270–280CrossRefGoogle Scholar
  15. Huang J, Bechelard EP (1993) Effects of aluminum on growth and cation uptake in seedlings of Eucalyptus mannifera and Pinus radiata. Plant Soil 149:121–127CrossRefGoogle Scholar
  16. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246. doi: 10.1016/j.pbi.2004.03.014 CrossRefPubMedGoogle Scholar
  17. Kojima M, Kamada NT, Komatsu H, Takei K, Kuroha T, Mizutani M, Ashikari M, Ueguchi TM, Matsuoka M, Suzuki K, Sakakibara H (2009) Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant Cell Physiol 50(7):1201–1214. doi: 10.1093/pcp/pcp057 CrossRefPubMedPubMedCentralGoogle Scholar
  18. León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8(3):110–116. doi: 10.1016/S1360-1385(03)00011-6 CrossRefPubMedGoogle Scholar
  19. Lindon FC, Ramalho JC, Barreiro MG (1998) Aluminium toxicity modulates nitrate to ammonia reduction. Photosynthetica 35:213–222CrossRefGoogle Scholar
  20. Liu B, Sukalovic VH (1998) Effect of aluminum on growth and nitrate reductase activities of maize seelings. Acta Phytophysiol Sin 24:347–353Google Scholar
  21. Mi G, Chen F, Zhang F (2008) Multiple signaling pathways control nitrogen-mediated root elongation in maize. Plant Signal Behav 3:1030–1032CrossRefPubMedPubMedCentralGoogle Scholar
  22. Mihailovic N, Vucinic Z, Sukalovic HT (2015) Ammonium enables aluminum-induced stimulation of nitrogen assimilation in roots of Al-tolerant maize genotoypes. J Plant Nutr 38:371–383CrossRefGoogle Scholar
  23. Mishra BS, Singh M, Aggrawal P, Laxmi A (2009) Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS One 4(2):e4502. doi: 10.1371/journal.pone.0004502 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Miwa I, Okuda J, Maeda K, Okuda G (1972) Mutarotase effect on colorimetric determination of blood glucose with β-d-glucose oxidase. Clin Chim Acta 37:538–540CrossRefPubMedGoogle Scholar
  25. Miyazawa Y, Sakai A, Miyagishima S, Takano H, Kawano S, Kuroiwa T (1999) Auxin and cytokinin have opposite effects on amyloplast development and the expression of starch synthesis genes in cultured bright yellow-2 tobacco cells. Plant Physiol 121:461–469CrossRefPubMedPubMedCentralGoogle Scholar
  26. Moubayidin L, Mambro RD, Sabatini S (2009) Cytokin-in-Auxin Cross Talk. Trend. Plant Sci 14:557–562. doi: 10.1016/j.tplants.2009.06.010 CrossRefGoogle Scholar
  27. Nishina K, Takenaka C, Ishizuka S (2009) Relationship between N2O and NO emission potentials and soil properties in Japanese forest soils. Soil Sci Plant Nutr 55:203–214CrossRefGoogle Scholar
  28. Oda A, Yamamoto F (2002) Effects of aluminum on growth and biomass allocation of hydroponically cultured Quercus acutissima, Cinnamomum comphora and Eucalyptus viminalis seedlings. J Tree Health 6:99–103Google Scholar
  29. Oh HJ, Park JE, Park YG, Jeong BR (2014) Growth and quality of plug seedlings of three indigenous medicinal plants as affected by ionic strength of the nutrient solution. Hort Environ Biotechnol 55(2):63–69CrossRefGoogle Scholar
  30. Okazaki M, Matui K (1993) Environmental soil science. Aasakura Pub Co Ltd, TokyoGoogle Scholar
  31. Påhlsson AB (1990) Influence of aluminium on biomass, nutrients, soluble carbohydrates and phenols in beech (Fagus sylvatica). Physiol Plantarum 78:79–84CrossRefGoogle Scholar
  32. Pegtel DM (1987) Effect of ionic Al in culture solutions on the growth of Arnica montana L. and Deschampsia flexuosa (L.) Trin. Plant Soil 102:85–92CrossRefGoogle Scholar
  33. Radin JW (1974) Distribution and development of nitrate reductase activity in germinating cotton seedlings. Plant Physiol 53:458–463CrossRefPubMedPubMedCentralGoogle Scholar
  34. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell S185–S205. doi:  10.1105/tpc.010455
  35. Rotisch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trend Plant Sci 9(12):606–613. doi: 10.1016/j.tplants.2004.10.009 CrossRefGoogle Scholar
  36. Ruffel S, Gojon A, Lejay L (2014) Signal interactions in the regulation of root nitrate uptake. J Exp Bot 65(19):5509–5517. doi: 10.1093/jxb/eru321 CrossRefPubMedGoogle Scholar
  37. Sahulka J (1972) The effect of exogenous IAA and kinetin on nitrate reductase, nitrite reductase and glutamate dehydrogenase activities in excised pea roots. Biol Plantarum 14:330–336CrossRefGoogle Scholar
  38. Smeekens S (2000) Sugar-induced signal transduction. Annu Rev Plant Phys 51:49–81CrossRefGoogle Scholar
  39. Tomioka R, Takenaka C (2007) Enhancement of root respiration and photosynthesis in Quercus serrata Thunb. seedlings by long-term aluminum treatment. Environ Sci 14(3):141–148PubMedGoogle Scholar
  40. Tomioka R, Oda A, Takenaka C (2005) Root growth enhancement by rhizospheric aluminum treatment in Quercus serrata Thunb. seedlings. J Forest Res 10:319–324. doi: 10.1007/s10310-005-0152-0 CrossRefGoogle Scholar
  41. Tomioka R, Uchida A, Takenaka C, Tezuka T (2007) Effect of aluminum on nitrate reductase and photosynthetic activities in Quercus serrata Seedlings. Environ Sci 14(3):157–165PubMedGoogle Scholar
  42. Tomioka R, Takenaka C, Maeshima M, Tezuka T, Kojima M, Sakakibara H (2012) Stimulation of root growth induced by aluminum in Quercus serrata Thunb is related to activity of nitrate reductase and maintenance of IAA concentration in roots. Am J Plant Sci 3:1619–1624. doi: 10.4236/ajps.2012.311196 CrossRefGoogle Scholar
  43. Trouverie J, Chateau-Joubert S, Thévenot C, Jacquemot MP, Prioul JL (2004) Regulation of vacuolar invertase by abscisic acid or glucose in leaves and roots from maize plantlets. Planta 219:894–905CrossRefPubMedGoogle Scholar
  44. Tsuji M, Kuboi T, Konishi S (1994) Stimulatory effects of aluminum on the growth of cultured roots of tea. Soil Sci Plant Nutr 40:471–476CrossRefGoogle Scholar
  45. Watanabe T, Osaki M, Tadano T (1998) Effects of nitrogen source and aluminum on growth of tropical tree seedlings adapted to low pH soil. Soil Sci Plant Nutr 44:655–666CrossRefGoogle Scholar
  46. Yamamoto K (2000) Estimation of the canopy-cap size using two photographs taken at different heights. Ecol Res 15(2):203–208. doi: 10.1046/j.1440-1703.2000.00341.x CrossRefGoogle Scholar
  47. Yuan TT, Xu HH, Zhang KX, Guo TT, Lu YT (2014) Glucose inhibits root meristem growth via ABA INSENSITIVE 5, which represses PIN1 accumulation and auxin activity in Arabidopsis. Plant Cell Environ 37:1338–1350CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Ubuki Moriyama
    • 1
  • Rie Tomioka
    • 1
    Email author
  • Mikiko Kojima
    • 2
  • Hitoshi Sakakibara
    • 1
    • 2
  • Chisato Takenaka
    • 1
  1. 1.Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan
  2. 2.RIKEN Center for Sustainable Resource ScienceYokohamaJapan

Personalised recommendations