The tripartite symbiosis between legumes, rhizobia and indigenous mycorrhizal fungi is more efficient in undisturbed soil

Abstract

We investigated how the rate of colonization by indigenous arbuscular mycorrhizal fungi (AMF) affects the interaction between AMF, Sinorrhizobium meliloti and Medicago truncatula Gaertn. To generate a differential inoculum potential of indigenous AMF, five cycles of wheat, each of 1 month, were grown in sieved or undisturbed soil before M. truncatula was sown. The early colonization of M. truncatula roots by indigenous AMF was faster in undisturbed soil compared with sieved soil, but by pod-fill the frequency of hyphae, arbuscules and vesicles was similar in both treatments. At this latter stage, M. truncatula grown in undisturbed soil had accumulated a greater biomass in aboveground tissues, had a greater P concentration and derived more N from the atmosphere than plants grown in disturbed soil, although soil compaction resulted in plants having a smaller root system than those from disturbed soil. The difference in plant P content could not be explained by modifications in hydrolytic soil enzymes related to the P cycle as the activity of acid phosphatase was greater in sieved than in undisturbed soil, and the activity of alkaline phosphatase was unaffected by the treatment. Thus, the results observed were a consequence of the different rates of AMF colonization caused by soil disturbance. Together with earlier results for soybean, this study confirms that soil disturbance modifies the interaction between indigenous AMF, rhizobia and legumes leading to a reduced efficacy of the bacterial symbiont.

Introduction

Many legumes form symbioses with both rhizobia and arbuscular mycorrhizal fungi (AMF). Dual inoculation with both microorganisms results in a tripartite mutualistic symbiosis and generally increases plant growth to a greater extent than inoculation with only one (for a review see Chalk et al., 2006). There is now evidence that both enhanced acquisition of P by the host and effects on molecular signalling between the three symbionts may explain the synergism of AMF and rhizobia. Flavonoids are thought to be key signal compounds associated with the establishment of the tripartite symbiosis and Antunes et al., 2006a, Antunes et al., 2006b reported that the presence of both symbionts changed the accumulation of flavonoids in soybean roots. Overall, the root content of daidzein was reduced when Glomus clarum was present, whereas genistein and coumestrol only decreased when soybean plants (Glycine max (L.) Merr.) were inoculated with both G. clarum and Bradyrhizobium japonicum.

Goss and de Varennes (2002) studied the interaction of soybean, B. japonicum and indigenous AMF. They generated a differential inoculum potential for AMF by growing maize (Zea mays L.) in sieved or undisturbed soil before soybeans were sown. The soybean plants grown in undisturbed soil developed faster and accumulated a greater biomass than plants from disturbed soil. Moreover, there was a positive interaction between the two microbial symbionts in undisturbed soil that resulted in more abundant colonization of soybean roots by both microbes. By pod-fill, the frequency of hyphal, arbuscular and vesicular colonization was greater in undisturbed than in sieved soil. At this stage, nodule weight and the percentage of N derived from the atmosphere was also greater in undisturbed than disturbed soil.

The effect of the extent of AMF colonization on the efficacy of the tripartite symbiosis has only been shown for one crop (soybean), one soil (a gleyed Melanic Brunisol from the Elora Research Station near Guelph—43°39′N, 80°25′W) and one bacterial symbiont (B. japonicum) (Goss and de Varennes, 2002).

The hypothesis we tested was that this is a common phenomenon, and should therefore be observed using a very different combination of soil, plant and microbial symbionts, especially the bacteria.