flowering, iron homeostasis, drought response, or resistance against pathogens [41,
116, 122].
Due to high reactivity, ROS/RNS possess strong damaging properties. To avoid
oxidative damages, plant cells have evolved a number of antioxidant mechanisms
that aid to maintain low steady-stable levels of ROS/RNS, which are sufficient
to performing their signaling functions [116, 117]. The production of ROS/RNS
is significantly increased when plants are exposed to adverse abiotic factors
or attack of pathogens [42, 89, 117]. Enhanced ROS production followed
by oxidative stress development is considered as a component of host-plant immunity to combat with pathogens, including microbial infection. In this context, the
inability of incompatible rhizobia to form productive nodules is explained by death
of bacteroids and inactivation of nitrogenase due to intense oxidative stress induced
by plant cells [46]. It seems that a small increase in ROS/RNS levels is required for
successful rhizobial infection and nodule formation. At low levels, ROS/RNS are
proposed to be involved in signal transduction cascades during nodule development
[44–46, 93]. However, large amounts of ROS and RNS generated during the
interaction between rhizobia and legumes can potentially cause development of
oxidative/nitrosative stress followed by nodulation defects; therefore, concentrations
of these reactive species must be tightly regulated by antioxidant enzymes and
metabolites from both the host and microsymbiont sides.
3.2
Role of ROS/NO
• in Early Steps of Symbiotic Interaction
There is much evidence that ROS and antioxidant defense play an important role in
the establishment of an effective legume-rhizobium symbiosis [32–35, 38, 40, 41,
123]. Similarly to respond to pathogen invasion, the infection of legumes with
rhizobia causes an intensification of oxidative processes in plant cells, promoted
by increased production of ROS and
• NO. However, apart from the response to
pathogenesis, production of ROS and NO
• may not be a plant defense response to the
rhizobia but rather a process that is needed for the development of a symbiosis [28,
44–46, 93].
Early differentiation during legume-rhizobium symbiosis involves the structural
modification of root hairs and formation of infection threads, which allows root
infection by the bacteria. In parallel, root cortex cells dedifferentiate to generate
nodule meristem. The molecular communication between plant and bacteria
involves the modification in ROS and RNS production by the plant partner. Changes
of ROS and RNS accumulation have been detected during the symbiotic interaction
from the first hours following the initial interaction up to the ceasing of the
interaction during nodule senescence [93].
As in the case of pathogen attack, the root cells respond to rhizobia infection with
increased production of O • À
2 and Н 2 О 2 . Production of H 2 O 2 during symbiosis was
detected in infection threads and root nodules of M. sativa and P. sativum [38]. It was
shown that changes in O • À
2
and Н 2 О 2 levels in P. sativum roots under symbiosis
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
305
116, 122].
Due to high reactivity, ROS/RNS possess strong damaging properties. To avoid
oxidative damages, plant cells have evolved a number of antioxidant mechanisms
that aid to maintain low steady-stable levels of ROS/RNS, which are sufficient
to performing their signaling functions [116, 117]. The production of ROS/RNS
is significantly increased when plants are exposed to adverse abiotic factors
or attack of pathogens [42, 89, 117]. Enhanced ROS production followed
by oxidative stress development is considered as a component of host-plant immunity to combat with pathogens, including microbial infection. In this context, the
inability of incompatible rhizobia to form productive nodules is explained by death
of bacteroids and inactivation of nitrogenase due to intense oxidative stress induced
by plant cells [46]. It seems that a small increase in ROS/RNS levels is required for
successful rhizobial infection and nodule formation. At low levels, ROS/RNS are
proposed to be involved in signal transduction cascades during nodule development
[44–46, 93]. However, large amounts of ROS and RNS generated during the
interaction between rhizobia and legumes can potentially cause development of
oxidative/nitrosative stress followed by nodulation defects; therefore, concentrations
of these reactive species must be tightly regulated by antioxidant enzymes and
metabolites from both the host and microsymbiont sides.
3.2
Role of ROS/NO
• in Early Steps of Symbiotic Interaction
There is much evidence that ROS and antioxidant defense play an important role in
the establishment of an effective legume-rhizobium symbiosis [32–35, 38, 40, 41,
123]. Similarly to respond to pathogen invasion, the infection of legumes with
rhizobia causes an intensification of oxidative processes in plant cells, promoted
by increased production of ROS and
• NO. However, apart from the response to
pathogenesis, production of ROS and NO
• may not be a plant defense response to the
rhizobia but rather a process that is needed for the development of a symbiosis [28,
44–46, 93].
Early differentiation during legume-rhizobium symbiosis involves the structural
modification of root hairs and formation of infection threads, which allows root
infection by the bacteria. In parallel, root cortex cells dedifferentiate to generate
nodule meristem. The molecular communication between plant and bacteria
involves the modification in ROS and RNS production by the plant partner. Changes
of ROS and RNS accumulation have been detected during the symbiotic interaction
from the first hours following the initial interaction up to the ceasing of the
interaction during nodule senescence [93].
As in the case of pathogen attack, the root cells respond to rhizobia infection with
increased production of O • À
2 and Н 2 О 2 . Production of H 2 O 2 during symbiosis was
detected in infection threads and root nodules of M. sativa and P. sativum [38]. It was
shown that changes in O • À
2
and Н 2 О 2 levels in P. sativum roots under symbiosis
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
305