Suppression of Reactive Oxygen Species and Enhanced Stress Tolerance in <i>Rubia cordifolia</i> Cells Expressing the <i>rolC</i> Oncogene

Bulgakov, Victor P.; Aminin, Dmitry L.; Shkryl, Yuri N.; Gorpenchenko, Tatiana Y.; Veremeichik, Galina N.; Dmitrenok, Pavel S.; Zhuravlev, Yuri N.

doi:10.1094/mpmi-21-12-1561

Cited by 52 publications

(33 citation statements)

References 56 publications

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“…The response of RolC plants was opposite in this case, showing decreased levels of fatty acids and hydroxyl fatty acids in CR samples compared to controls. Indeed, this result confirmed that the rol C gene expression prevents the production of ROS, as previously reported by Bulgakov et al [38] for Rubia cordifolia cells. GRCR plants showed no significant changes in lysolipid intensities or in fatty acid content.…”

Section: Chromium and Water Stressessupporting

confidence: 90%

Metabolomic analysis of wild and transgenic Nicotiana langsdorffii plants exposed to abiotic stresses: unraveling metabolic responses

et al. 2015

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Nicotiana langsdorffii plants, wild and transgenic for the Agrobacterium rhizogenes rol C gene and the rat glucocorticoid receptor (GR) gene, were exposed to different abiotic stresses (high temperature, water deficit, and high chromium concentrations). An untargeted metabolomic analysis was carried out in order to investigate the metabolic effects of the inserted genes in response to the applied stresses and to obtain a comprehensive profiling of metabolites induced during abiotic stresses. High-performance liquid chromatography separation (HPLC) coupled to high-resolution mass spectrometry (HRMS) enabled the identification of more than 200 metabolites, and statistical analysis highlighted the most relevant compounds for each plant treatment. The plants exposed to heat stress showed a unique set of induced secondary metabolites, some of which were known while others were not previously reported for this kind of stress; significant changes were observed especially in lipid composition. The role of trichome, as a protection against heat stress, is here suggested by the induction of both acylsugars and glykoalkaloids. Water deficit and Cr(VI) stresses resulted mainly in enhanced antioxidant (HCAs, polyamine) levels and in the damage of lipids, probably as a consequence of reactive oxygen species (ROS) production. Moreover, the ability of rol C expression to prevent oxidative burst was confirmed. The results highlighted a clear influence of GR modification on plant stress response, especially to water deficiency-a phenomenon whose applications should be further investigated. This study provides new insights into the field of system biology and demonstrates the importance of metabolomics in the study of plant functioning.

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Section: Chromium and Water Stressessupporting

confidence: 90%

Metabolomic analysis of wild and transgenic Nicotiana langsdorffii plants exposed to abiotic stresses: unraveling metabolic responses

et al. 2015

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“…The results indicated decreased intracellular ROS levels in rolC-expressing cells compared with control cells [11]. Moreover, the gene attenuated ROS accumulation after ROS-inducing treatments.…”

Section: Ros Homeostasis and Expression Of Antioxidant Genesmentioning

confidence: 89%

“…The first indication that the expression of individual rol genes in plant cells has an effect on the metabolism of reactive oxygen species (ROS) was published in 2008 [11]. This investigation was performed to determine whether the increased production of secondary metabolites in Rubia cordifolia cultured cells is associated with the oxidative burst.…”

Section: Ros Homeostasis and Expression Of Antioxidant Genesmentioning

confidence: 99%

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Recent Advances in the Understanding of Agrobacterium rhizogenes-Derived Genes and Their Effects on Stress Resistance and Plant Metabolism

Bulgakov

Shkryl

Veremeichik

et al. 2013

Advances in Biochemical Engineering/Biotechnology

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It is commonly accepted that the plant pathogens Agrobacterium rhizogenes and Agrobacterium tumefaciens, acting via their T-DNA oncogenes, disturb hormone metabolism or hormone perception pathways in plants, thereby attaining their aim of successful pathogenesis. In this work, we summarize recent data on the A. rhizogenes rolC and rolB oncogenes in comparison to the A. tumefaciens 6b oncogene with respect to their effects on the physiology of transformed cells. The newly discovered functions of the rol genes include the modulation of secondary metabolism, the modulation of levels of intracellular ROS and stress resistance of transformed cells, changed sucrose metabolism, and the inhibition of programmed cell death. We show that the rol genes do not have suppressive effects on plant innate immunity; rather, these genes activate plant defense reactions. The existence of not only the hormone-related mechanism of pathogenicity but also the defense-related mechanism of pathogenicity during plant-Agrobacterium interactions is suggested.

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“…4,5 Both genes, when expressed in plant cells, decreased intracellular ROS level. The rolB gene acts by inducing upregulation of antioxidant genes, thereby permanently supporting an active anti-oxidative status of transformed cells.…”

mentioning

confidence: 99%

Can plant oncogenes inhibit programmed cell death? The rolB oncogene reduces apoptosis-like symptoms in transformed plant cells

Gorpenchenko

Aminin

Vereshchagina

et al. 2012

Plant Signaling & Behavior

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The interplay between oncogene expression, ROS production and apoptosis has received a great deal of attention in animal cell biology. Few studies have focused on the role of plant oncogenes in these processes. Plant oncogenes are Agrobacterium T-DNA genes of the plast (RolB) family of eukaryotic regulators.1 During plant infection by the pathogen Agrobacterium rhizogenes, the rolA, rolB and rolC oncogenes are transferred from the bacteria into the plant genome, causing tumor formation and hairy root disease.2 The function of rolB is not restricted to root formation; the gene promotes de novo formation of floral and shoot meristems, induces parthenocarpy, causes a delay in pistil and anther development and modifies the balance between the proliferation of procambial cells and xylem differentiation. 3 The mechanism by which the RolB oncoprotein exerts such varied morphological changes remains unknown.Recently, involvement of the rolB and rolC plant oncogenes in ROS metabolism was revealed. 4,5 Both genes, when expressed in plant cells, decreased intracellular ROS level. The rolB gene acts by inducing upregulation of antioxidant genes, thereby permanently supporting an active anti-oxidative status of transformed cells.5 As ROS perturbations and apoptotic processes are tightly linked, we proposed involvement of the RolB protein in signaling networks regulating PCD in plants. The present investigation was aimed at testing this possibility.The rolB oncogene was previously identified as an important player in ROS metabolism in transformed plant cells. Numerous reports indicate a crucial role for animal oncogenes in apoptotic cell death. Whether plant oncogenes such as rolB can induce programmed cell death (PCD) in transformed plant cells is of particular importance. In this investigation, we used a single-cell assay based on confocal microscopy and fluorescent dyes capable of discriminating between apoptotic and necrotic cells. Our results indicate that the expression of rolB in plant cells was sufficient to decrease the proportion of apoptotic cells in steady-state conditions and diminish the rate of apoptotic cells during induced PCD. These data suggest that plant oncogenes, like animal oncogenes, may be involved in the processes mediating PCD. Can plant oncogenes inhibit programmed cell death?The rolB oncogene reduces apoptosis-like symptoms in transformed plant cells Necrosis, a rapid form of cell death, is characterized by cytoplasmic swelling, destruction of organelles and disruption of the plasma membrane. 6 Apoptosis is characterized by cell shrinkage, maintenance of organelle integrity and condensation and fragmentation of DNA.6 A distinct type of PCD called apoptosis was originally identified in single cells that were usually surrounded by healthy-looking neighbors. 6 In the present work, we used the terms "PCD" and "apoptosis" interchangeably. Early symptoms of apoptosis, such as nuclear chromatin condensation at the periphery of nucleus and around nucleoli, were studied. To distinguish between necrotic and...

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Suppression of Reactive Oxygen Species and Enhanced Stress Tolerance in Rubia cordifolia Cells Expressing the rolC Oncogene

Cited by 52 publications

References 56 publications

Metabolomic analysis of wild and transgenic Nicotiana langsdorffii plants exposed to abiotic stresses: unraveling metabolic responses

Metabolomic analysis of wild and transgenic Nicotiana langsdorffii plants exposed to abiotic stresses: unraveling metabolic responses

Recent Advances in the Understanding of Agrobacterium rhizogenes-Derived Genes and Their Effects on Stress Resistance and Plant Metabolism

Can plant oncogenes inhibit programmed cell death? The rolB oncogene reduces apoptosis-like symptoms in transformed plant cells

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