5.1 Trehalose in the Rhizobia-Legume Symbiosis
It is the domain of some prokaryotes to reduce atmospheric nitrogen to ammonia that afterward can be assimilated into biological material. A large group of nitrogen fixing soil bacteria is able to establish symbiotic associations with plants to obtain the energy necessary for nitrogen fixation from compounds that they receive from their host plants. The symbiosis between legumes and rhizobia occurs within specialized organs called nodules situated mainly on the root. The architecture of these nodules provides the specific physiological and anatomical requisites for the activity of nitrogenase (the key enzyme of this symbiosis) and the nutrient exchange between the symbiotic partners.
In 1980 was first described the appearance of trehalose as a major carbohydrate in soybean root nodules at the onset of nitrogen fixation (Streeter 1980). Trace amounts of trehalose were also detected in other plant organs, but the bulk of tre-halose was specific to the symbiotic organs (Streeter 1980). At this time trehalose was thought to be uncommon in plants, so it was speculated that the trehalose measured in other parts of the plant was nodule-derived. In later studies, treha-lose appeared to be a common carbohydrate in almost all nodules tested. Phillips et al. (1984) detected trehalose accumulation in nodules of white clover (Trifolium repens), Pueraria thun-bergiana, Albizia julibrissin, and even in the nodules of the nonlegume Alnus glutinosa and Elaeagnus angustifolia. Streeter (1985) discovered trehalose accumulation in the field grown nodules of peanut (Arachis hypogenus), alfalfa (Medicago sativa), common bird's-foot-trefoil (Lotus corniculatus), and again in white clover (Trifolium repens).
When trehalose was discovered as a carbohydrate in root nodules, it was predicted that it was synthesized by bacteroids since the presence of trehalose in uninfected higher plants was not known at that time. This prediction was supported by the findings that (a) trehalose was synthesized in bacteroids isolated from soybean nodules (Streeter 1985), (b) trehalose was not depleted in senescing soybean nodules but accumulated while the concentration of other compounds declined (Müller et al. 2001), and (c) trehalose concentration in bacteroids varied greatly depending on the rhizobial strain (Streeter 1985).
The fact that nodules of soybean infected by Bradyrhizobium japonicum and B. elkanii contains three independent pathways for trehalose biosynthesis such as TS, MOTS and TPS suggests the importance of trehalose in this microorganism in symbiosis and free-living (Streeter and Gómez 2006).
The impact of trehalose on nodule metabolism has been further examined by the addition of the trehalase inhibitor validamycin A, or the external supply of trehalose. The addition of validamycin A to Medicago truncatula (López et al. 2009) and Lotus japonicus (López et al. 2006) caused an increase in the amount of trehalose that improved the response to salinity in both legumes by increasing the biomass production under stress conditions, although nitrogen fixation was not affected in both cases. The addition of trehalose to the nutrient solution of soybean roots growing in sterile conditions caused a strong impact on sucrose metabolism by an increase of the sucrose synthase and to a lesser extent alkaline invertase (Müller et al. 1997). In addition, soybean nodules with naturally occurring high levels of trehalose, had significantly lower levels of sucrose than nodules with low levels of trehalose, and higher levels of the catalytic activities sucrose synthase and alkaline invertase (Müller et al. 1997). With all this information, it has been hypothesized that trehalose turns out to have the same effect as sucrose suggesting that trehalose might be secreted by plant-associated microorganisms as an instrument to influence assimilates allocation by inducing a sink in the surrounding cells or tissues.
5.1.2 Role of Trehalose in Nodules Under Abiotic Stress Conditions
Trehalose accumulation in nodules can further be altered by diverse abiotic factors such as salt stress, drought or nitrate. Therefore it has been tested whether trehalose is involved in stress protection in the rhizobia-legume symbiosis. The overexpression of TPS in the symbiotic bacteria Rhizobium etli has been used as strategy to increase drought tolerance in legumes. The host plant (Phaseolus vulgaris) inoculated with this transformed bacteria displayed higher resistance to drought stress. Besides, plants inoculated with the mutant strain showed higher nodule number and hence increased nitrogenase activity and higher biomass compared with plants inoculated with the wild-type R. etli (Suárez et al. 2008).
In soybean root nodules, an increase of the trehalose pools size upon water stress was reported, but this accumulation was dependent on the rhizo-bial strain that was used for infection (Müller et al. 1996). In addition, an increase of sucrose and pin-itol pools was measured in these experiments.
In common bean (Phaseolus vulgaris), the increase in nodule trehalose content during drought stress differed among rhizobial strains, exhibiting higher leaf relative water contents and more drought resistance those cultivars with higher nodule trehalose levels (Farias-Rodriguez et al. 1998).
In the model legumes Lotus japonicus and Medicago truncatula exposed to salt stress, an increase of trehalose concentration of about 40 and 100%, respectively, has been detected (López et al. 2008a). Similarly, in Medicago sativa plants infected with Rhizobium meliloti, maltose and trehalose concentrations were significantly enhanced upon 0.15 M sodium chloride stress, especially in roots and bacteroids (Fougère et al. 1991). All these data support a role for trehalose as osmoprotectant under stress conditions in the Rhizobium-legume symbiosis.
Around 90-95% of land plants maintain some type of colonization of their roots by soil borne filamentous fungi known as arbuscular mycor-rhiza (AM), due to the tree-like structures that fungi form into the plant cell. This symbiosis increases plant biomass and photosynthesis since the extraradical mycelium, spreading into the soil, is responsible of the mineral nutrient and water uptake that benefits its plant host. In return, the fungi direct the flow of a significant fraction of the host plant photoassimilate. Glycogen and trehalose have been described as the dominant storage carbohydrates in AM fungal hyphae and spores (Pfeffer et al. 1999).
In the mycorrhizal roots of two maize cultivars exposed to drought, the trehalose content increased fivefold (Schellenbaum et al. 1998). AM fungi seem to accumulate trehalose upon stress in the same way as other microorganisms (Müller et al. 1995b) , allowing them to survive freezing overwintering conditions (Addy et al. 1994) and periods of drought (Jasper et al. 1993). Hence, accumulation of trehalose could be an important determinant for sustained viability under stress and for successful colonization of plants after frost or drought at the beginning of the growing season.
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