Modulation of NADPH-oxidase gene expression in rolB- transformed calli of Arabidopsis thaliana and Rubia cordifolia

Veremeichik, Galina N.; Bulgakov, Victor P.; Shkryl, Yuri N.

doi:10.1016/j.plaphy.2016.05.014

Cited by 11 publications

(7 citation statements)

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“…The subject of this study was to define how the rol B gene affects D. muscipula physiology at the level of oxidative stress response, primary and secondary metabolism, in two clones, K and L. Tusevki et al [ 8 ] hypothesised that transformation of Hypericum perforatum L. plants with wild strains of R. rhizogenes modifies cell redox status and consequently leads to an oxidative stress response. Furthermore, it was demonstrated that the rol B oncogene can suppress ROS production and activate secondary metabolism in transformed cells, while the mechanism of such an event is still poorly understood [ 12 ]. In the present research, MDA content was estimated in transformed plants as the oxidative stress marker.…”

Section: Discussionmentioning

confidence: 99%

“…Nevertheless, the mechanism by which the rol B gene stimulates the protein antioxidant system remains unknown [ 8 ]. Veremeichik et al [ 12 ] showed that the rol B gene regulates the expression of NADPH oxidase in Arabidopsis thaliana and Rubia cordifolia transformed calli, while activity of this enzyme is one of the main sources of ROS production during plant-pathogen interactions. Moreover, it has been postulated that rol genes induce the reprogramming of transformed plant cells and provoke pleiotropic effects on primary and secondary metabolism, including enzymatic and non-enzymatic antioxidant systems [ 29 ].…”

Section: Discussionmentioning

confidence: 99%

“…Expression of the rol B oncogene can increase the level of secondary metabolites in plant tissue [ 10 , 11 ], suppress reactive oxygen species (ROS) production [ 4 ], and modulate the antioxidant defence system [ 8 ]. Moreover, Veremeichik et al [ 12 ] showed that rol B expression regulates the activity of NADPH oxidase, while Bulgakov et al [ 5 ] reported the tyrosine phosphatase activity of the rolB protein. Nevertheless, the complex physiological response of medical plants transformed with the rol B oncogene has never been studied.…”

Section: Introductionmentioning

confidence: 99%

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Response of physiological parameters in Dionaea muscipula J. Ellis teratomas transformed with rolB oncogene

et al. 2021

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Background Plant transformation with rol oncogenes derived from wild strains of Rhizobium rhizogenes is a popular biotechnology tool. Transformation effects depend on the type of rol gene, expression level, and the number of gene copies incorporated into the plant’s genomic DNA. Although rol oncogenes are known as inducers of plant secondary metabolism, little is known about the physiological response of plants subjected to transformation. Results In this study, the physiological consequences of rolB oncogene incorporation into the DNA of Dionaea muscipula J. Ellis was evaluated at the level of primary and secondary metabolism. Examination of the teratoma (transformed shoots) cultures of two different clones (K and L) showed two different strategies for dealing with the presence of the rolB gene. Clone K showed an increased ratio of free fatty acids to lipids, superoxide dismutase activity, synthesis of the oxidised form of glutathione, and total pool of glutathione and carotenoids, in comparison to non-transformed plants (control). Clone L was characterised by increased accumulation of malondialdehyde, proline, activity of superoxide dismutase and catalase, total pool of glutathione, ratio of reduced form of glutathione to oxidised form, and accumulation of selected phenolic acids. Moreover, clone L had an enhanced ratio of total triglycerides to lipids and accumulated saccharose, fructose, glucose, and tyrosine. Conclusions This study showed that plant transformation with the rolB oncogene derived from R. rhizogenes induces a pleiotropic effect in plant tissue after transformation. Examination of D. muscipula plant in the context of transformation with wild strains of R. rhizogenes can be a new source of knowledge about primary and secondary metabolites in transgenic organisms.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Response of physiological parameters in Dionaea muscipula J. Ellis teratomas transformed with rolB oncogene

et al. 2021

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“…Other growth inhibition effects, like early leaf necrosis in rolB transgenic plants were previously reported in N. tabacum and A. thaliana (Schmülling et al, 1988;Nilsson et al, 1993a;Dehio and Schell, 1994;Kodahl et al, 2016), but in this study, leaf necrosis was not observed in any of the overexpressing rolB lines of K. blossfeldiana. The absence of necrosis could be attributed to the ability to suppress reactive oxygen species (ROS) observed in light induced stress in rolB transformed R. cordifolia callus (Bulgakov et al, 2012), potentially due to rolB regulation of NADPH oxidase isoforms (Veremeichik et al, 2016). In addition, there is evidence that the fresh and dry weight of rolB lines is significantly lower than that of WT in A. thaliana (Kodahl et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Transgenic Kalanchoë blossfeldiana, Containing Individual rol Genes and Open Reading Frames Under 35S Promoter, Exhibit Compact Habit, Reduced Plant Growth, and Altered Ethylene Tolerance in Flowers

et al. 2021

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Reduced growth habit is a desirable trait for ornamental potted plants and can successfully be obtained through Rhizobium rhizogenes transformation in a stable and heritable manner. Additionally, it can also be obtained by transformation with Agrobacterium tumefaciens harboring specific genes from R. rhizogenes. The bacterial T-DNA harbors four root oncogenic loci (rol) genes and 14 less known open reading frames (ORFs). The four rol genes, i.e., rolA, rolB, rolC, and rolD, are conceived as the common denominator for the compact phenotype and the other less characterized ORFs seem auxiliary but present a potential breeding target for less aberrant and/or more tailored phenotypes. In this study, Kalanchoë blossfeldiana ‘Molly’ was transformed with individual rol genes and selected ORFs in 35S overexpressing cassettes to comprehensively characterize growth traits, gene copy and expression, and ethylene tolerance of the flowers. An association of reduced growth habit, e.g. height and diameter, was observed for rolB2 and ORF14-2 when a transgene single copy and high gene expression were detected. Chlorophyll content was reduced in overexpressing lines compared to wild type (WT), except for one ΔORF13a (a truncated ORF13a, where SPXX DNA-binding motif is absent). The flower number severely decreased in the overexpressing lines compared to WT. The anthesis timing showed that WT opened the first flower at 68.9 ± 0.9 days and the overexpressing lines showed similar or up to 24 days delay in flowering. In general, a single or low relative gene copy insertion was correlated to higher gene expression, ca. 3 to 5-fold, in rolB and ΔORF13a lines, while in ORF14 such relation was not directly linked. The increased gene expression observed in rolB2 and ΔORF13a-2 contributed to reducing plant growth and a more compact habit. Tolerance of detached flowers to 0.5 μl L−1 ethylene was markedly higher for ORF14 with 66% less flower closure at day 3 compared to WT. The subcellular localization of rolC and ΔORF13a was investigated by transient expression in Nicotiana benthamiana and confocal images showed that rolC and ΔORF13a are soluble and localize in the cytoplasm being able to enter the nucleus.

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“…It has been shown that important ROS generators, NADPH oxidase genes AtRbohD and AtRbohF and corresponding proteins, are upregulated in rolB-expressing cells [90], and the deletion of rolB from wild-type hairy roots decreases ROS level in rolB-deficient hairy roots [12]. This data could indicate that ROS levels in rolB-transformed plants should be increased.…”

Section: Ros Metabolism and Abiotic Stress Responsementioning

confidence: 99%

Proteomic Analysis of Proteins Related to Defense Responses in Arabidopsis Plants Transformed with the rolB Oncogene

Vereshchagina

Mironova

Bulgakov

et al. 2023

IJMS

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During Agrobacterium rhizogenes–plant interaction, the rolB gene is transferred into the plant genome and is stably inherited in the plant’s offspring. Among the numerous effects of rolB on plant metabolism, including the activation of secondary metabolism, its effect on plant defense systems has not been sufficiently studied. In this work, we performed a proteomic analysis of rolB-expressing Arabidopsis thaliana plants with particular focus on defense proteins. We found a total of 77 overexpressed proteins and 64 underexpressed proteins in rolB-transformed plants using two-dimensional gel electrophoresis and MALDI mass spectrometry. In the rolB-transformed plants, we found a reduced amount of scaffold proteins RACK1A, RACK1B, and RACK1C, which are known as receptors for activated C-kinase 1. The proteomic analysis showed that rolB could suppress the plant immune system by suppressing the RNA-binding proteins GRP7, CP29B, and CP31B, which action are similar to the action of type-III bacterial effectors. At the same time, rolB plants induce the massive biosynthesis of protective proteins VSP1 and VSP2, as well as pathogenesis-related protein PR-4, which are markers of the activated jasmonate pathway. The increased contents of glutathione-S-transferases F6, F2, F10, U19, and DHAR1 and the osmotin-like defense protein OSM34 were found. The defense-associated protein PCaP1, which is required for oligogalacturonide-induced priming and immunity, was upregulated. Moreover, rolB-transformed plants showed the activation of all components of the PYK10 defense complex that is involved in the metabolism of glucosinolates. We hypothesized that various defense systems activated by rolB protect the host plant from competing phytopathogens and created an effective ecological niche for A. rhizogenes. A RolB → RACK1A signaling module was proposed that might exert most of the rolB-mediated effects on plant physiology. Our proteomics data are available via ProteomeXchange with identifier PXD037959.

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Modulation of NADPH-oxidase gene expression in rolB- transformed calli of Arabidopsis thaliana and Rubia cordifolia

Cited by 11 publications

References 60 publications

Response of physiological parameters in Dionaea muscipula J. Ellis teratomas transformed with rolB oncogene

Response of physiological parameters in Dionaea muscipula J. Ellis teratomas transformed with rolB oncogene

Transgenic Kalanchoë blossfeldiana, Containing Individual rol Genes and Open Reading Frames Under 35S Promoter, Exhibit Compact Habit, Reduced Plant Growth, and Altered Ethylene Tolerance in Flowers

Proteomic Analysis of Proteins Related to Defense Responses in Arabidopsis Plants Transformed with the rolB Oncogene

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