Actinorhizal symbioses and their N₂ fixation

Abstract

summary More than 200 angiosperms, distributed in 25 genera, develop root nodule symbioses (actinorhizas) with soil bacteria of the actinomycetous genus Frankia. Although most soils studied contain infective Frankia, cultured strains are available only after isolation from root nodules. Frankia infects roots via root hairs in some hosts or via intercellular penetration in others. The nodule originates in the pericycle. The number of nodules in Alnus is determined by the plant in an autoregulated process that, in turn, is modulated by nutrients such as nitrogen and phosphate. Except in the genera Allocausarina and Casuarina, Frankia in nodules develops so‐called vesicles where nitrogenase is localized. Sporulation of Frankia occurs in some symbioses. As a group, actinorhizal plants show a large range of anatomical and biochemical adaptations in order to balance the oxygen tension near nitrogenase. In symbioses with well aerated nodule tissue like Alnus, the vesicles have a multilayered envelope composed mainly of lipids, bacterio‐hopanetetrol and their derivatives. This envelope is assumed to retard the diffusion of oxygen into the nitrogenase‐containing vesicle. In symbioses like Casuarina, the infected plant cells themselves, rather than Frankia, appear to retard oxygen diffusion, and high concentrations of haemoglobin indicate an infected region with a low oxygen tension. At least in Alnus spp., ammonia resulting from N2 fixation is assimilated by glutamine synthetase in the plant. The carbon compound(s) used by Frankia in nodules is not yet known. Nitrogenase activity decreases in response to a number of environmental factors but recovers upon return to normal conditions. This dynamism in nitrogenase activity is often explained by loss and recovery of active nitrogenase and has been traced to loss and recovery of the nitrogenase proteins themselves. Recovery is partly due to growth of Frankia and to development of new vesicles in the Alnus nodules. In the field, varying conditions continuously affect the plants and the measured rate of N2 fixation is a result not only of the conditions prevailing at the moment but also of the conditions experienced over preceding days. N2 fixed by actinorhizal plants is substantial and actinorhizal plants have great potential in soil reclamation and in various types of forestry. Several species are also useful in horticulture.

Evolutionary tradeoffs can select against nitrogen fixation and thereby maintain nitrogen limitation

“…Newly evolved symbioses would likely have less efficient N fixation (owing to the smaller amount of evolutionary time to work out the symbiotic arrangement), so we would expect steeper tradeoff curves for evolutionary invasions than ecological invasions. Furthermore, although we focus on invasions of old-growth systems, our model is consistent with the well documented pattern of the dominance of N fixers in primary succession (3)(4)(5)(6)25): when the soil available N pool, A, is small, nonfixers (F ϭ 0) die out but N fixers (F Ͼ 0) can grow (see Eq. 1 when A is small).…”

“…The first of these questions addresses a well documented successional pattern: In temperate and boreal ecosystems, N fixers dominate early primary succession but are replaced during the course of succession by nonfixers, even when N may still limit NPP (3)(4)(5)(6). Some recent modeling studies have investigated this question (7)(8)(9)(10), as outlined below.…”

“…11) and (ii) there are traits inherent to N fixation that lead to selection against N fixers when they appear in old-growth systems. Given that N-fixing bacteria are ubiquitous in natural ecosystems (1), phylogenetically diverse (12), and that they form symbioses with hundreds of plant species from nine plant families (6), many of which are temperate and boreal trees, phylogenetic constraints might not explain the absence of oldgrowth N fixers. In this article, we therefore explore the second hypothesis, using a simple evolutionary model to investigate factors that can select against N fixers in an old-growth N-limited environment.…”

Biofertilizer, a way towards organic agriculture: A review

“…Frankia is the genus of N2-fixing actinomycetes (Benson and Silvester, 1993;Huss-Danell, 1997). These are also called actinorhizal plants and they are also used in land reclamation, for timber and fuel wood production, in mixed plantations, for windbreaks, (Schwencke and Carù, 2001).…”

Nitrogen Fixation in Seabuckthorn (Hippophae rhamnoides L.) Root Nodules and Effect of Nitrate on Nitrogenase Activity

“…The oxygen diffusion barrier and leghaemoglobin are probably related to the nitrate inhibition of nitrogenase activity in legume root nodules Kato et al, 2003;Vessey and Waterer, 1992). On the other hand, in actinorhizal root nodules, the envelope surrounding Frankia vesicles in infected cells is assumed to retard the diffusion of oxygen into the nitrogenase-containing vesicle (Huss-Danell, 1997). Symbiotic haemoglobin was not observed in seabuckthorn root nodules based on the color of the infected region of the root nodules; the pink color of leghaemoglobin was observed in the infected region of legume root nodules.…”