Several reactive oxygen and nitrogen species (ROS/RNS) are continuously produced in plants as by-products of aerobic metabolism or in response to stresses. Depending on the nature of the ROS and RNS, some of them are highly toxic and rapidly detoxified by various cellular enzymatic and non-enzymatic mechanisms. Whereas plants have many mechanisms with which to combat increased ROS/RNS levels produced during stress conditions, under other circumstances plants appear to generate ROS/RNS as signalling molecules to control various processes encompassing the whole lifespan of the plant such as normal growth and development stages. This review aims to summarize recent studies highlighting the involvement of ROS/RNS, as well as the low molecular weight thiols, glutathione and homoglutathione, during the symbiosis between rhizobia and leguminous plants. This compatible interaction initiated by a molecular dialogue between the plant and bacterial partners, leads to the formation of a novel root organ capable of fixing atmospheric nitrogen under nitrogen-limiting conditions. On the one hand, ROS/RNS detection during the symbiotic process highlights the similarity of the early response to infection by pathogenic and symbiotic bacteria, addressing the question as to which mechanism rhizobia use to counteract the plant defence response. Moreover, there is increasing evidence that ROS are needed to establish the symbiosis fully. On the other hand, GSH synthesis appears to be essential for proper development of the root nodules during the symbiotic interaction. Elucidating the mechanisms that control ROS/RNS signalling during symbiosis could therefore contribute in defining a powerful strategy to enhance the efficiency of the symbiotic interaction.
Rhizobia form a symbiotic relationship with plants of the legume family to produce nitrogen-fixing root nodules under nitrogen-limiting conditions. We have examined the importance of glutathione (GSH) during free-living growth and symbiosis of Sinorhizobium meliloti. An S. meliloti mutant strain (SmgshA) which is unable to synthesize GSH due to a gene disruption in gshA, encoding the enzyme for the first step in the biosynthesis of GSH, was unable to grow under nonstress conditions, precluding any nodulation. In contrast, an S. meliloti strain (SmgshB) with gshB, encoding the enzyme involved in the second step in GSH synthesis, deleted was able to grow, indicating that ␥-glutamylcysteine, the dipeptide intermediate, can partially substitute for GSH. However, the SmgshB strain showed a delayed-nodulation phenotype coupled to a 75% reduction in the nitrogen fixation capacity. This phenotype was linked to abnormal nodule development. Both the SmgshA and SmgshB mutant strains exhibited higher catalase activity than the wild-type S. meliloti strain, suggesting that both mutant strains are under oxidative stress. Taken together, these results show that GSH plays a critical role in the growth of S. meliloti and during its interaction with the plant partner.All aerobic organisms are exposed to reactive oxygen species (ROS), such as the superoxide anion, hydrogen peroxide (H 2 O 2 ), and the hydroxyl radical, during normal aerobic metabolism or after exposure to stress conditions. ROS can cause irreversible damage to cellular components if they are not rapidly detoxified by antioxidant defense systems (15). To protect themselves against oxidant damage, cells contain effective defense mechanisms, including scavenging enzymes, such as catalases, superoxide dismutases, and glutathione peroxidases, and antioxidants, such as the tripeptide glutathione ␥-glutamyl-L-cysteinylglycine (GSH).GSH is synthesized by a two-step process. In the first step, glutamate and cysteine are conjugated by ␥-glutamyl cysteine synthetase (␥ECS) to form ␥-glutamyl cysteine (␥EC). In a second step, glycine is added to ␥EC to form GSH in a reaction catalyzed by glutathione synthetase (GSHS). The redox-active sulfhydryl group of GSH protects cells from ROS by directly scavenging free radicals and acting as a cofactor for antioxidant enzymes such as glutathione peroxidases. GSH oxidized in this manner forms GSH disulfide, which is recycled back to its reduced form by glutathione reductase.Initial studies of the requirement for GSH and its role in protection against oxidative stress were performed on bacteria. E. coli mutants devoid of GSH were isolated by means of a transposon insertion in gshA, which encodes ␥ECS (13). From these studies, it was found that not only was GSH nonessential under normal growth conditions, but also, rather surprisingly, these mutants were unaffected in their resistance to compounds which cause oxidative damage. These results contrast with the situation found in mammalian cells, where GSH deficiency results in cellular dama...
To investigate the involvement of bacterial catalases of the symbiotic gram-negative bacterium Rhizobium meliloti in the development of Medicago-Rhizobium functional nodules, we cloned a putative kat gene by screening a cosmid library with a catalase-specific DNA probe amplified by PCR from the R. meliloti genome. Nucleotide sequence analysis of a 1.8-kb DNA fragment revealed an open reading frame, called katA, encoding a peptide of 562 amino acid residues with a calculated molecular mass of 62.9 kDa. The predicted amino acid sequence showed a high homology with the primary structure of monofunctional catalases from eucaryotes and procaryotes. The katA gene was localized on the chromosome, and the katA gene product was essentially found in the periplasmic space. A katA::Tn5 mutant was obtained and showed a drastic sensitivity to hydrogen peroxide, indicating an essential protective role of KatA. However, neither Nod nor Fix phenotypes were impaired in the mutant, suggesting that KatA is not essential for nodulation and establishment of nitrogen fixation. Exposure to a sublethal concentration of H 2 O 2 enhanced KatA activity (100-fold) and also increased survival to subsequent H 2 O 2 exposure at higher concentrations. No protection is observed in katA::Tn5, indicating that KatA is the major component of an adaptive response.Reactive oxygen species such as superoxide radical, hydrogen peroxide, and hydroxyl radical naturally arise during normal metabolism in aerobically growing cells as a result of the incomplete reduction of molecular oxygen. These species can damage lipids, proteins and DNA and are probably involved in some degenerative processes in living cells (23). In this framework, there is increasing evidence that oxygen-derived species play an important role in Rhizobium-legume symbiosis, at least during the senescence period. This symbiotic association leads to the formation of nodules where a high degree of interaction between the host cell and the microbial symbiont is found (35). The symbiosis is mainly characterized by its ability to fix atmospheric nitrogen, and the key enzyme of this process, the nitrogenase located in the microsymbiont, is rapidly and irreversibly inactivated by oxygen; the possible role of oxygen-derived species in this inactivation is still an open question (40). Nodules have a high potential to produce damaging oxygen-derived species such as hydrogen peroxide because of the strong reducing conditions required for nitrogen fixation and the action of several proteins, including ferredoxin, uricase, hydrogenase, and leghemoglobin (12). This hemoprotein, present in large amounts in legume nodules, is itself subject to an autoxidation process, generating superoxide anion and hydrogen peroxide (41). Furthermore, hydrogen peroxide has been shown to react with leghemoglobin to generate further damaging species (13), and significant amounts of hydroxyl radicals have been found in senescing nodules (3). This can be related to the high concentration of catalytic iron, which is able to c...
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