IrrE, a Global Regulator of Extreme Radiation Resistance in Deinococcus radiodurans, Enhances Salt Tolerance in Escherichia coli and Brassica napus

Pan, Jie; Wang, Jin; Zhou, Zhengfu; Yan, Yongliang; Zhang, Wei; Lu, Wei; Ping, Shuzhen; Dai, Qilin; Yuan, Menglong; Feng, Bo; Hou, Xiaoguang; Zhang, Ying; Ma, Ruiqiang; Liu, Tingting; Feng, Lu; Wang, Lei; Chen, Ming; Lin, Min

doi:10.1371/journal.pone.0004422

Cited by 90 publications

(115 citation statements)

References 54 publications

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“…d IR, ionizing radiation; ϩϩ, high level of postirradiation induction; ϩD or ϩϩD, induction after ionizing radiation and desiccation. (479,681). Another novel stress response transcriptional regulator, DrRRA, regulates the expression of numerous genes under normal and ionizing radiation conditions, such as DNA damage-related genes (e.g., recA, pprA, ligT, cinA, gyrB, and uvrB), dps1, genes homologous to plant desiccation resistance proteins, and genes for antioxidant proteins, chaperones, and proteases (645).…”

Section: Continued On Following Pagementioning

confidence: 99%

Oxidative Stress Resistance inDeinococcus radiodurans

Slade

Radman

2011

Microbiol Mol Biol Rev

648

639

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SUMMARY Deinococcus radiodurans is a robust bacterium best known for its capacity to repair massive DNA damage efficiently and accurately. It is extremely resistant to many DNA-damaging agents, including ionizing radiation and UV radiation (100 to 295 nm), desiccation, and mitomycin C, which induce oxidative damage not only to DNA but also to all cellular macromolecules via the production of reactive oxygen species. The extreme resilience of D. radiodurans to oxidative stress is imparted synergistically by an efficient protection of proteins against oxidative stress and an efficient DNA repair mechanism, enhanced by functional redundancies in both systems. D. radiodurans assets for the prevention of and recovery from oxidative stress are extensively reviewed here. Radiation- and desiccation-resistant bacteria such as D. radiodurans have substantially lower protein oxidation levels than do sensitive bacteria but have similar yields of DNA double-strand breaks. These findings challenge the concept of DNA as the primary target of radiation toxicity while advancing protein damage, and the protection of proteins against oxidative damage, as a new paradigm of radiation toxicity and survival. The protection of DNA repair and other proteins against oxidative damage is imparted by enzymatic and nonenzymatic antioxidant defense systems dominated by divalent manganese complexes. Given that oxidative stress caused by the accumulation of reactive oxygen species is associated with aging and cancer, a comprehensive outlook on D. radiodurans strategies of combating oxidative stress may open new avenues for antiaging and anticancer treatments. The study of the antioxidation protection in D. radiodurans is therefore of considerable potential interest for medicine and public health.

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Section: Continued On Following Pagementioning

confidence: 99%

Oxidative Stress Resistance inDeinococcus radiodurans

Slade

Radman

2011

Microbiol Mol Biol Rev

648

639

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“…Our previous study revealed that the protein expression profile of E. coli harboring the irrE gene was significantly different from that of the control strain when challenged by NaCl. In total, 124 proteins including the osmotically inducible, detoxification and growth-related proteins, were differentially expressed (Pan et al 2009). Brassica napus is one of the most important oilseed crops cultivated worldwide, and it is sensitive to salt stress throughout the growing season.…”

Section: Introductionmentioning

confidence: 99%

“…Brassica napus is one of the most important oilseed crops cultivated worldwide, and it is sensitive to salt stress throughout the growing season. Our previous study showed that transgenic B. napus plants expressing the irrE gene can tolerate 350 mM NaCl (Pan et al 2009), a concentration that usually inhibits the growth of almost all crop plants, and the gene expression analysis of the transgenic irrE B. napus showed the gene encoding the plasma membrane Na ? /H ?…”

Section: Introductionmentioning

confidence: 99%

Salt tolerance conferred by expression of a global regulator IrrE from Deinococcus radiodurans in oilseed rape

et al. 2016

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As salinity is a major threat to sustainable agriculture worldwide, cultivation of salt-tolerant crops becomes increasingly important. IrrE acts as a global regulator and a general switch for stress resistance in Deinococcus radiodurans. In this study, to determine whether the irrE gene can improve the salt tolerance of Brassica napus, we introduced the irrE gene into B. napus by the Agrobacterium tumefaciens-mediated transformation method. Fortytwo independent transgenic plants were regenerated. Polymerase chain reaction (PCR) analyses confirmed that the irrE gene had integrated into the plant genome. Northern as well as Western blot analyses revealed that the transgene was expressed at various levels in transgenic plants. Analysis for the T 1 progenies derived from four independent transformants showed that irrE had enhanced the salt tolerance of T 1 in the presence of 350 mM NaCl. Furthermore, under salt stress, transgenic plants accumulated more compatible solutes (proline) and a lower level of malondialdehyde (MDA), and they had higher activities of catalase (CAT), peroxidase (POD) and superoxide dismutase (SOD). However, agronomic traits were not affected by irrE gene overexpression in the transgenic B. napus plants. This study indicates that the irrE gene can improve the salt tolerance of B. napus and represents a promising candidate for the development of crops with enhanced salt tolerance by genetic engineering.

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“…It can withstand extremely high doses of ionizing radiation, long periods of desiccation, UV radiation, and oxidizing agents and has a more efficient DNA repair system than any known species in the bacterial kingdom (12). The overexpression of IrrE (also named PprI), a global regulator of D. radiodurans that is essential for extreme radioresistance (13), has been reported to confer radiotolerance on E. coli (14), enhance salt tolerance in E. coli and Brassica napus (15), and improve osmoticstress tolerance in ethanologenic strains of E. coli, thereby increasing ethanol production (16). This global regulator has also been artificially engineered to improve tolerance to alcohols, such as ethanol and butanol (17), and inhibitors, such as furfural, hydroxyl methyl furfural, and vanillin, which are routinely observed in lignocellulosic hydrolysates used in biorefineries (18).…”

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confidence: 99%

Engineering Synthetic Multistress Tolerance in Escherichia coli by Using a Deinococcal Response Regulator, DR1558

Appukuttan

Singh

Park

et al. 2016

Appl Environ Microbiol

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Cellular robustness is an important trait for industrial microbes, because the microbial strains are exposed to a multitude of different stresses during industrial processes, such as fermentation. Thus, engineering robustness in an organism in order to push the strains toward maximizing yield has become a significant topic of research. We introduced the deinococcal response regulator DR1558 into Escherichia coli (strain Ec-1558), thereby conferring tolerance to hydrogen peroxide (H 2 O 2 ). The reactive oxygen species (ROS) level in strain Ec-1558 was reduced due to the increased KatE catalase activity. Among four regulators of the oxidative-stress response, OxyR, RpoS, SoxS, and Fur, we found that the expression of rpoS increased in Ec-1558, and we confirmed this increase by Western blot analysis. Electrophoretic mobility shift assays showed that DR1558 bound to the rpoS promoter. Because the alternative sigma factor RpoS regulates various stress resistance-related genes, we performed stress survival analysis using an rpoS mutant strain. Ec-1558 was able to tolerate a low pH, a high temperature, and high NaCl concentrations in addition to H 2 O 2 , and the multistress tolerance phenotype disappeared in the absence of rpoS. Microarray analysis clearly showed that a variety of stress-responsive genes that are directly or indirectly controlled by RpoS were upregulated in strain Ec-1558. These findings, taken together, indicate that the multistress tolerance conferred by DR1558 is likely routed through RpoS. In the present study, we propose a novel strategy of employing an exogenous response regulator from polyextremophiles for strain improvement.

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IrrE, a Global Regulator of Extreme Radiation Resistance in Deinococcus radiodurans, Enhances Salt Tolerance in Escherichia coli and Brassica napus

Cited by 90 publications

References 54 publications

Oxidative Stress Resistance inDeinococcus radiodurans

Oxidative Stress Resistance inDeinococcus radiodurans

Salt tolerance conferred by expression of a global regulator IrrE from Deinococcus radiodurans in oilseed rape

Engineering Synthetic Multistress Tolerance in Escherichia coli by Using a Deinococcal Response Regulator, DR1558

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