The role of root exudates in the aluminum tolerance of Norway spruce

Fig. 1: Hydroponic treatments of 3-month (left) and 3-year (right) old Norway spruce plants.

Fig. 2: Treatments of Norway spruce seedlings in perlite; pots are placed in sunbags. Picture: Alexander Heim.

Fig. 3: Fluorescence spectra of phenolic compounds exuded by roots of Norway spruce (top) and Al complexes formed by these compounds (bottom).

Fig. 4: Accumulation of aluminium at the surface and in the apoplast of a spruce root.

Acidification of forest soils can lead to high concentrations of phytotoxic aluminium in the soil solution. In this project the hypothesis is tested that the aluminium tolerance of Norway spruce is increased by root exudation of organic acid anions that form stable complexes with the metal.

Collaboration

In this project, the WSL research unit “Soil Sciences” collaborated with the ETH research group “Plant Nutrition” (Emmanuel Frossard); the work was performed mainly by the former Ph.D. student Alexander Heim (current address: “Department of Geography”, University of Zürich.

Problem

Soil acidification below pH 4.5. can lead to elevated concentrations of phytotoxic aluminium species in soil solution. They can directly affect the growth and vitality of roots and indirectly lead to nutrient deficiencies by aluminium competing with major nutrient cations for uptake. The acceleration of the acidification caused by the input of acidity or acidifying compounds with atmospheric deposition has raised the concern that acid-sensitive tree species are not replaced quickly enough by more acid-tolerant ones and this can lead to forest damages.

Objectives

For crops like wheat and barley it could be shown that acid-tolerant cultivars owe their resistance to the root exudation of organic acid anions like citrate or malate that can form stable complexes with aluminum. These complexes cannot be taken up by the plant roots, and thus phytotoxic effects can be avoided.
Based on these observations, we wanted to test the hypothesis that acid-tolerant tree species like Norway spruce exude organic acid anions to exclude aluminium from uptake.

Results from hydroponic treatments of 3-month and 3-year old Norway spruce plants

(Heim, 2001; Heim et al. 1999, 2001):

• Aluminium accumulated at the surface and in the apoplast of the roots both in exchangeable and non-exchangeable form
• The exchangeable and precipitated aluminium was possibly bound to phenolic substances and / or phosphate
• Norway spruce exhibited a constitutive root exudation of organic acid anions (mainly oxalate), phenolic substances, carbohydrates, amino acids and phosphate
• Complexation of aluminium by exuded phenolic substances could be detected in the nutrient solution by fluorescence spectroscopy; however, the exuded amounts were not enough to detoxify a substantial portion of the aluminium present.

In conclusion, root exudation of soluble organic ligands is not a major aluminium tolerance mechanism in Norway spruce. Tolerance could rather be attributed to immobilization of aluminium in the root apoplast, where strong binding sites are available or precipitation may occur.

Results from treatments of mycorrhizal and non-mycorrhizal Norway spruce seedlings in perlite 

(Heim, 2001; Heim et al. 2003):

• The perlite buffered the pH at values > 5 and no soluble aluminium was detected in the system
• Plant biomass was significantly reduced when high concentrations of aluminium were added without fungal inoculation, and aluminium uptake was significantly higher than in the control
• Fungal inoculation compensated the growth reduction but did not reduce aluminium uptake

In conclusion, spruce seedlings seem to be able to mobilize and take up aluminium from the soil solid phase.

Publications

• Heim, A.; Brunner, I.; Frossard, E.; Luster, J. 2003. Aluminum Effects on Picea abies at Low Solution Concentrations. - Soil Sci. Soc. Am. J. 67: 895-898.
• Heim, A.; Brunner, I.; Frey, B.; Frossard, E.; Luster, J. 2001. Root exudation, organic acids, and element distribution in roots of Norway spruce seedlings treated with aluminium in hydroponics. - J. Plant Nutr. Soil Sci. 164: 519-526.
• Heim, A. 2001. Chelating organic substances in roots and root exudates and their potential role in aluminium resistance of Norway spruce (Picea abies [L.] Karst.). ETH Zurich, Diss. ETH Nr. 13807.
• Heim, A.; Luster, J.; Brunner, I.; Frey, B.; Frossard, E. 1999. Effects of aluminium treatment on Norway spruce roots: Aluminium binding forms, element distribution, and release of organic substances. - Plant Soil 216: 103-116.