The inhibition of ammonium uptake in excised birch (Betula pendula) roots by batatasin‐III

Abstract

In northern Sweden, plants growing in association with the clonal dwarf shrub Empetrum hermaphroditum usually exhibit limited growth and are N-depleted. Previous studies suggest that this negative effect by E. hermaphroditum may be explained, at least in part, by the release of phenolic compounds, particularly the dihydrostilbene, batatasin-III from foliage to soil. In the present work, we investigated whether batatasin-III has the potential to interfere with NH4+ uptake in birch (Betula pendula) roots. Excised birch roots were exposed to batatasin-III during brief periods in 15NH4+ solutions, and then analyzed for labeled N. Batatasin-III inhibited N-NH4+ uptake by 28, 89 and 95% compared with the control, when roots were treated with 0.1, 1.0 and 2.8 mM of batatasin-III, respectively. The effect of 1.0-mM batatasin-III was greater at pH 4.2 than at pH 6.8. In addition, the inhibition of N-NH4+ uptake by batatasin-III was not reversed after rinsing the roots in water and transferring them to a batatasin-III free solution. Furthermore, birch seedlings immersed in a 1.0-mM batatasin-III solution for 2 h, and then replanted in pots with soil, had decreased growth, such that 10 weeks after treatment, the dry mass of both shoots and roots was reduced by 74 and 73%, respectively, compared with control seedlings. This suggests that a brief exposure to batatasin-III may have a long-term inhibitory effect on whole plant growth. Using plasma membrane vesicles isolated from easily extractable spinach (Spinacia oleracea) leaves, it was found that batatasin-III strongly inhibited proton pumping in isolated plasma membrane vesicles, while it only slightly inhibited ATP hydrolytic activity. The uncoupling of proton pumping from ATP hydrolytic activity suggests that batatasin-III disturbs membrane integrity. This hypothesis was further supported by a greater efflux of ions from birch roots immersed in a batatasin-III solution than from roots in a control solution.

Ecosystem disturbance reduces the allelopathic effects of Empetrum hermaphroditum humus on tundra plants

“…Furthermore, N bound in phenolic–protein complexes may be released by elevated pH, given that the phenolics of Empetrum are less stable in high pH solutions (Harper & Balke 1981; Nilsson et al 2002). Also, the inhibitory effect of batatasin‐III on ammonium uptake is greater at pH 4.2 than at pH 6.8 (Wallstedt et al 2001). Finally, elevated pH causes enhanced microbial activity, greater N mineralization rates and elevated mineral N availability in Empetrum ‐dominated sites (Nilsson et al 2002).…”

“…Empetrum interferes with several important ecosystem processes. Plant metabolites produced by Empetrum can affect soil processes and have phytotoxic effects Nilsson et al 1998;Wallstedt et al 2001;Castells et al 2005). Empetrum has been shown to inhibit nutrient uptake by the trees Pinus sylvestris (Nilsson et al 1993) and Betula pendula (Wallstedt et al 2001), and has a negative impact on soil biota such as nematodes (Ruess et al 1998), and soil microbial activity, causing decreased decomposition rates (Wardle & Lavelle 1997;Wardle et al , 2003b.…”

“…Plant metabolites produced by Empetrum can affect soil processes and have phytotoxic effects Nilsson et al 1998;Wallstedt et al 2001;Castells et al 2005). Empetrum has been shown to inhibit nutrient uptake by the trees Pinus sylvestris (Nilsson et al 1993) and Betula pendula (Wallstedt et al 2001), and has a negative impact on soil biota such as nematodes (Ruess et al 1998), and soil microbial activity, causing decreased decomposition rates (Wardle & Lavelle 1997;Wardle et al , 2003b. These allelopathic effects by Empetrum, in turn, affect plant succession and stand productivity in boreal forests Nilsson 1994;Wardle et al 1998b), and have implications for commercial forestry (Nilsson & Wardle 2005).…”

Litter mixture effects on tropical tree seedling growth – a greenhouse experiment

“…For example, in boreal ecosystems, litter and litter extracts of the dwarf shrub Empetrum hermaphroditum have been demonstrated to inhibit seed germination and reduce growth of boreal tree species . These negative litter effects were attributed to the soluble phenolic compound, batatasin-III (Odén et al 1992), which was observed to decrease plant N uptake (Nilsson et al 1993;Wallstedt et al 2001). Similarly, the negative effect of Kalmia angustifolia on Picea mariana regeneration in Canada has been associated with an alteration in N cycling patterns by Kalmia litter tannins.…”

Adsorption of allelopathic compounds by wood-derived charcoal: the role of wood porosity

“…In the boreal forests of northern Sweden, E. hermaphroditum releases phenolic compounds, and in particularly the dihydrostilbene Batatasin-III, from green leaves and litter (Nilsson et al, 1998;Ode´n et al, 1992;Wardle et al, 1998b;Zackrisson and Nilsson, 1992) which inhibits seed germination and seedling emergence, disturbs the plasmalemma integrity of target roots' cells (Wallstedt et al, 2001) and negatively affects mycorrhizal symbiosis of coniferous trees (Nilsson et al, 1993). Further, Batatasin-III impairs soil microbial activity and slows down decomposition which both contribute to an increased accumulation of soil organic material with time since last fire disturbance (DeLuca et al, 2002;Zackrisson et al, 1996).…”