the induction of nod genes in plants when the interaction between symbionts was
incompatible [37, 125].
Under bacterial infection, legume NADPH oxidases play a pivotal role in production of O • À
2
and Н 2 О 2 and, in turn, have a crucial role in different stages of
nodulation [47]. The inhibition of ROS production by the NAD(P)H oxidase
inhibitor diphenyleneiodonium [126] and the correlation between ROS accumulation and transcript accumulation of two NADPH oxidase genes in response to Nod
factors in M. truncatula roots [32] support for the involvement of NADPH oxidases
in ROS generation. The involvement of other potential enzymatic ROS sources
cannot be excluded. The source of Н 2 О 2 is a number of plant peroxidases and
other oxidases [127]. Production of ROS in legume-rhizobium symbiosis also occurs
during the reductive processes required for nitrogen fixation. Many compounds that
act as electron donors for nitrogenase (e.g. ferredoxin) can undergo auto-oxidation
with O • À
2
formation. ROS production may also be promoted by leghemoglobin,
which facilitates O 2 transport to the bacteroids at a low but constant flux, thus
preventing O 2 inactivation of nitrogenase [42]. In the presence of O 2 , leghemoglobin
can undergo auto-oxidation, and as a result, O • À
2
is generated with further
dismutation to Н 2 О 2 [42, 94]. The interaction of leghemoglobin with Н 2 О 2 leads
to the formation of a highly oxidized ferric-porphyrin cation radical, which further
can oxidize protein molecules with formation, for example, tyrosine radicals
[128]. Н 2 О 2 can be released from leghemoglobin and promote HO
• generation
via Fenton reaction [128].
Together with ROS, RNS are now considered as major components of oxidative
burst and redox regulation [41]. RNS, such as nitric oxide (
•
NO) and peroxynitrite
(ONOO
À ), can be formed in nodules and other plant organs. There are several
possible pathways of
• NO synthesis, which can be divided into oxidative
(NO synthase, polyamine-mediated, hydroxylamine-mediated) and reductive
(plasma membrane-bound nitrite NO reductase, mitochondrial electron transport
chain, xanthine oxidoreductase) pathways [46, 123]. To date, there is no evidence
for an involvement of the bacterial partner in NO production during symbiosis
establishment. As with ROS, uncontrolled formation of RNS is potentially dangerous and may cause cellular damage, but low concentrations of RNS, especially
of
•
NO, are critical in many plant processes, stress responses, and nodule formation
[39, 123]. Transcriptomic analysis at an early stage of the symbiosis showed
that
• NO is potentially involved in the repression of plant defense reactions, favoring
the establishment of the legume-rhizobium interaction [45]. Various genes involved
in the developmental program of the root hair during nodulation (kinases, receptorlike kinases, and transcription factors), in carbon metabolism (sucrose transport,
sucrose synthase, or malate dehydrogenase), as well as in proteasome-dependent
proteolysis were upregulated by
•
NO. Genes involved in the control of the cellular
redox state, such as glutathione (GSH) and H 2 O 2 metabolism, are also regulated
by
• NO [45]. Redox signaling mediated by RNS is realized via posttranslational
modification of antioxidant proteins or transcription factors. RNS can lead to
nitrosylation (addition of an NO group) or nitration (addition of an NO 2 group) of
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
307
incompatible [37, 125].
Under bacterial infection, legume NADPH oxidases play a pivotal role in production of O • À
2
and Н 2 О 2 and, in turn, have a crucial role in different stages of
nodulation [47]. The inhibition of ROS production by the NAD(P)H oxidase
inhibitor diphenyleneiodonium [126] and the correlation between ROS accumulation and transcript accumulation of two NADPH oxidase genes in response to Nod
factors in M. truncatula roots [32] support for the involvement of NADPH oxidases
in ROS generation. The involvement of other potential enzymatic ROS sources
cannot be excluded. The source of Н 2 О 2 is a number of plant peroxidases and
other oxidases [127]. Production of ROS in legume-rhizobium symbiosis also occurs
during the reductive processes required for nitrogen fixation. Many compounds that
act as electron donors for nitrogenase (e.g. ferredoxin) can undergo auto-oxidation
with O • À
2
formation. ROS production may also be promoted by leghemoglobin,
which facilitates O 2 transport to the bacteroids at a low but constant flux, thus
preventing O 2 inactivation of nitrogenase [42]. In the presence of O 2 , leghemoglobin
can undergo auto-oxidation, and as a result, O • À
2
is generated with further
dismutation to Н 2 О 2 [42, 94]. The interaction of leghemoglobin with Н 2 О 2 leads
to the formation of a highly oxidized ferric-porphyrin cation radical, which further
can oxidize protein molecules with formation, for example, tyrosine radicals
[128]. Н 2 О 2 can be released from leghemoglobin and promote HO
• generation
via Fenton reaction [128].
Together with ROS, RNS are now considered as major components of oxidative
burst and redox regulation [41]. RNS, such as nitric oxide (
•
NO) and peroxynitrite
(ONOO
À ), can be formed in nodules and other plant organs. There are several
possible pathways of
• NO synthesis, which can be divided into oxidative
(NO synthase, polyamine-mediated, hydroxylamine-mediated) and reductive
(plasma membrane-bound nitrite NO reductase, mitochondrial electron transport
chain, xanthine oxidoreductase) pathways [46, 123]. To date, there is no evidence
for an involvement of the bacterial partner in NO production during symbiosis
establishment. As with ROS, uncontrolled formation of RNS is potentially dangerous and may cause cellular damage, but low concentrations of RNS, especially
of
•
NO, are critical in many plant processes, stress responses, and nodule formation
[39, 123]. Transcriptomic analysis at an early stage of the symbiosis showed
that
• NO is potentially involved in the repression of plant defense reactions, favoring
the establishment of the legume-rhizobium interaction [45]. Various genes involved
in the developmental program of the root hair during nodulation (kinases, receptorlike kinases, and transcription factors), in carbon metabolism (sucrose transport,
sucrose synthase, or malate dehydrogenase), as well as in proteasome-dependent
proteolysis were upregulated by
•
NO. Genes involved in the control of the cellular
redox state, such as glutathione (GSH) and H 2 O 2 metabolism, are also regulated
by
• NO [45]. Redox signaling mediated by RNS is realized via posttranslational
modification of antioxidant proteins or transcription factors. RNS can lead to
nitrosylation (addition of an NO group) or nitration (addition of an NO 2 group) of
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
307