legumes [4, 5]. Within root nodules, the rhizobia are developed into specialized
symbiotic forms, bacteroids, which fix N 2 into ammonia by using nitrogenase
enzyme complex and supply it to the host plant. This relationship provides nutrient
benefits for both partners, a plant cell supplying carbon sources to bacteria and
receiving, in response, NH 3 for growth [6–8]. Symbiosis of legumes with rhizobia
covers over 60% of plant needs in nitrogen [9] and accounts for 20% of the estimated
biological nitrogen fixed each year on Earth [10]. There are species of agronomic
importance among legumes – common bean (Phaseolus vulgaris), alfalfa (Medicago
sativa), soybean (Glycine max), pea (Pisum sativum), and lentil (Lens culinaris). The
establishment of successful legume-rhizobium symbiosis can increase plant biomass
and crop yield and contribute to nitrogen enrichment of the soil [7, 8].
To establish the effective symbiosis, two symbiotic partners require being compatible with each other. Compatibility depends on mutual recognition via chemical
signals releasing from both the host plant and nodule bacteria [8, 11, 12]. However,
bacteria frequently can invade incompatible plants. In these cases, bacteria are
not able to form nodules or form nodules that cannot fix molecular nitrogen [8, 9,
12, 13]. Chemotaxis of soil rhizobia to root exudates plays an important role in
competitive nodulation [3, 14–16]. Specialized metabolites (or secondary metabolites) produced by legume roots attract rhizobia that adhere to the wall of the root hair
cells [11, 13, 14, 16, 17]. Root exudates are complex mixtures of low-molecular
mass organic compounds with flavonoids being the most important in the initiation
of symbiosis with rhizobia as benefit partners [3, 18–20]. Plant flavonoids activate
bacterial transcriptional factors NodDs that trigger the expression of nodulation
genes (nod genes) [1, 17, 20, 21]. The products of nod genes are proteins involved
in synthesis and export of specific lipochitooligosaccharides called Nod factors.
Bacterial Nod factors serve as signaling molecules that initiate nodule formation
in root cortex [1, 8, 12, 18, 22, 23, 27]. Recent studies suggest a crucial role of
Nod factors in the regulation of host phytohormone balance as a prerequisite for
successful nodule formation [16, 24–27]. The interaction between bacterial surface
polysaccharides and plant lectin receptors is also involved in the recognition process
and successful colonization of root hairs [6, 20, 28–31].
Rhizobial infection intensifies oxidative processes in plants, leading to
increased production of reactive oxygen species (ROS) and reactive nitrogen
species (RNS) [10, 32–37]. There is increasing evidence that ROS/RNS and
antioxidant system play a key role in the formation and functioning of legumerhizobium symbiosis [10, 38–47]. Uncontrolled changes in levels of these reactive
species impair either the formation of root nodules or N 2 -fixing activity of bacteroids [10, 38, 40, 42, 48]. A number of studies reported that elevated levels of
heavy metals in soils can disturb redox balance either in legume plants rhizobia
affecting their growth and decreasing efficacy of legume-rhizobium symbiosis
[48–56]. Under cultivation of legumes on the soils with the high level of heavy
metals (Cd, Cr, Cu, Pb, etc.), the root nodules can be the major accumulators of
heavy metals from soil [57–59].In this context, rhizobia are actively studied as one
of the suitable tools for effective soil bioremediation with reducing toxic effects of
heavy metals to legumes [48, 51, 58–62]. At the same time, legume-rhizobium
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
293
symbiotic forms, bacteroids, which fix N 2 into ammonia by using nitrogenase
enzyme complex and supply it to the host plant. This relationship provides nutrient
benefits for both partners, a plant cell supplying carbon sources to bacteria and
receiving, in response, NH 3 for growth [6–8]. Symbiosis of legumes with rhizobia
covers over 60% of plant needs in nitrogen [9] and accounts for 20% of the estimated
biological nitrogen fixed each year on Earth [10]. There are species of agronomic
importance among legumes – common bean (Phaseolus vulgaris), alfalfa (Medicago
sativa), soybean (Glycine max), pea (Pisum sativum), and lentil (Lens culinaris). The
establishment of successful legume-rhizobium symbiosis can increase plant biomass
and crop yield and contribute to nitrogen enrichment of the soil [7, 8].
To establish the effective symbiosis, two symbiotic partners require being compatible with each other. Compatibility depends on mutual recognition via chemical
signals releasing from both the host plant and nodule bacteria [8, 11, 12]. However,
bacteria frequently can invade incompatible plants. In these cases, bacteria are
not able to form nodules or form nodules that cannot fix molecular nitrogen [8, 9,
12, 13]. Chemotaxis of soil rhizobia to root exudates plays an important role in
competitive nodulation [3, 14–16]. Specialized metabolites (or secondary metabolites) produced by legume roots attract rhizobia that adhere to the wall of the root hair
cells [11, 13, 14, 16, 17]. Root exudates are complex mixtures of low-molecular
mass organic compounds with flavonoids being the most important in the initiation
of symbiosis with rhizobia as benefit partners [3, 18–20]. Plant flavonoids activate
bacterial transcriptional factors NodDs that trigger the expression of nodulation
genes (nod genes) [1, 17, 20, 21]. The products of nod genes are proteins involved
in synthesis and export of specific lipochitooligosaccharides called Nod factors.
Bacterial Nod factors serve as signaling molecules that initiate nodule formation
in root cortex [1, 8, 12, 18, 22, 23, 27]. Recent studies suggest a crucial role of
Nod factors in the regulation of host phytohormone balance as a prerequisite for
successful nodule formation [16, 24–27]. The interaction between bacterial surface
polysaccharides and plant lectin receptors is also involved in the recognition process
and successful colonization of root hairs [6, 20, 28–31].
Rhizobial infection intensifies oxidative processes in plants, leading to
increased production of reactive oxygen species (ROS) and reactive nitrogen
species (RNS) [10, 32–37]. There is increasing evidence that ROS/RNS and
antioxidant system play a key role in the formation and functioning of legumerhizobium symbiosis [10, 38–47]. Uncontrolled changes in levels of these reactive
species impair either the formation of root nodules or N 2 -fixing activity of bacteroids [10, 38, 40, 42, 48]. A number of studies reported that elevated levels of
heavy metals in soils can disturb redox balance either in legume plants rhizobia
affecting their growth and decreasing efficacy of legume-rhizobium symbiosis
[48–56]. Under cultivation of legumes on the soils with the high level of heavy
metals (Cd, Cr, Cu, Pb, etc.), the root nodules can be the major accumulators of
heavy metals from soil [57–59].In this context, rhizobia are actively studied as one
of the suitable tools for effective soil bioremediation with reducing toxic effects of
heavy metals to legumes [48, 51, 58–62]. At the same time, legume-rhizobium
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
293