High levels of the cytokinin BAP suppress programmed cell death in hybrid tobacco cells (Nicotiana suaveolens*N. tabacum) expressing hybrid lethality

Kobori, Satoshi; Masuda, Yu; Horii, Manabu; Marubashi, Wataru

doi:10.5511/plantbiotechnology.24.375

Cited by 10 publications

(20 citation statements)

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“…In human and animals, cytokinins participate in the control of cell differentiation (Ishii et al 2002; Berge et al 2006). In cancer cells (Ishii et al 2002; Cabello et al 2009) as well as in plant cell-suspension cultures (Carimi et al 2003; Mlejnek et al 2003) and in planta systems (Carimi et al 2003), various natural cytokinins can induce cell death which is manifested by cytoplasm and cell shrinkage (Mlejnek et al 2003; Jan et al 2008), nuclei condensation (Carimi et al 2003; Gahan et al 2003; Mlejnek et al 2003) and fragmentation (Ishii et al 2002; Kobori et al 2007). Sometimes, chromatin breakdown into internucleosomal DNA fragments (Gahan et al 2003; Carimi et al 2003; Mlejnek et al 2003), release of cytochrome c (Carimi et al 2003), formation of DNA-containing, apoptotic-like bodies (Ishii et al 2002), presence of apoptosis-specific caspase/metacaspase enzymes (van Doorn and Woltering 2005; Mlejnek and Procházka 2002; Parish and Li 2010) as well as activation of 28 kDa endonuclease are observed (Gahan et al 2003).…”

Section: Discussionmentioning

confidence: 99%

“…Then, the fragments were washed two times with PHB and fixed with 1 % glutaraldehyde (Merck) at PHB for 15 min, cut along their long axes into very thin sections, washed three times with PHB, observed and photographed using fluorescence microscope (Byczkowska et al 2012). The changing colour of chromatin, from green to red, allowed to distinguish living, dying and dead cells after the measurement of resultant fluorescence intensity (RFI) of green AO, migrating into the nuclei via cell membrane which did not change its permeability or integrity, and red EB, permeating to dying or dead cells in which cell membrane permeability or integrity was changed (Ribble et al 2005; Kobori et al 2007). The RFI values increased with the changing colour from green to red (Byczkowska et al 2012).…”

Section: Methodsmentioning

confidence: 99%

“…However, 0.04 μM of BAP at 28 °C induced changes similar to apoptosis suppressing the percentage of dead cells and extending nuclear fragmentation. In the hybrid cells, at higher levels of BAP, positive terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling (TUNEL) signals and accumulation of formazan, indicating production of reactive oxygen species (ROS), were detected less frequently than at its lower levels (Kobori et al 2007). However, application of TUNEL method to study cell death would not be an unequivocal test because it shows DNA breaks which are not necessarily related to the studied processes (Kobori et al 2007).…”

Section: Introductionmentioning

confidence: 99%

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Kinetin induces cell death in root cortex cells of Vicia faba ssp. minor seedlings

2012

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The double fluorescence staining with acridine orange and ethidium bromide (AO/EB) revealed that treatment of Vicia faba ssp. minor seedlings with kinetin-induced programmed cell death (PCD) in root cortex cells. Kinetin-induced cell death reflected by the morphological changes of nuclei including their invagination, volume increase, chromatin condensation and degradation as well as formation of micronuclei showed by AO/EB and 4,6-diamidino-2-phenylindol staining was accompanied by changes including increase in conductivity of cell electrolytes secreted to culture media, decrease in the number of the G1- and G2-phase cells and appearance of fraction of hypoploid cells as the effect of DNA degradation without ladder formation. Decrease in the number of mitochondria and in the activity of cellular dehydrogenases, production of reactive oxygen species (ROS), appearance of small and then large lytic vacuoles and increase in the amount of cytosolic calcium ions were also observed. The PCD was also manifested by increased width and weight of apical fragments of roots as well as decreased length of cortex cells which led to shortening of the whole roots. The kinetin-induced PCD process was almost completely inhibited by adenine, an inhibitor of phosphoribosyl transferase, and mannitol, an inhibitor of ROS production. These cell-death hallmarks and pathway of this process suggested that the induction of kinetin-specific vacuolar type of death, expressed itself with similar intensity on both morphological and metabolic levels, was a transient protecting whole roots and whole seedlings against elimination.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Kinetin induces cell death in root cortex cells of Vicia faba ssp. minor seedlings

2012

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“…This Agrobacterium virulence protein functions in nuclear targeting of the T-DNA to which it is covalently bound (Ballas and Citovsky 1997). Earlier studies had already shown that ipt gene expression limits cell death in hybrid tobacco cells expressing lethality (Kobori et al 2007). Furthermore expression of this gene was linked to delayed senescence in tobacco (Li et al 1992).…”

Section: Discussionmentioning

confidence: 95%

Cytokinin vectors mediate marker-free and backbone-free plant transformation

et al. 2008

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Conventional Agrobacterium-mediated transformation methods rely on complex and genotype-specific tissue culture media for selection, proliferation, and regeneration of genetically modified cells. Resulting transgenic plants may not only contain selectable marker genes but also carry fragments of the vector backbone. Here, we describe a new method for the production of transgenic plants that lack such foreign DNA. This method employs vectors containing the bacterial isopentenyltransferase (ipt) gene as backbone integration marker. Agrobacterium strains carrying the resulting ipt gene-containing "cytokinin" vectors were used to infect explants of various Solanaceous plant species as well as canola (Brassica napus). Upon transfer to hormone-free media, 1.8% to 9.9% of the infected explants produced shoots that contained a marker-free T-DNA while lacking the backbone integration marker. These frequencies often equal or exceed those for backbone-free conventional transformation.

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“…Additionally, BAP has a dual nature and at high concentrations it induces (Carimi et al 2003) while at low inhibits (Kobori et al 2007) PCD. Recently, it has been observed that also kinetin, a cytokinin naturally occurring in plant and animal organisms (Barciszewski et al 2007), induces PCD only in plant cells (Kunikowska et al 2013a, b).…”

Section: Discussionmentioning

confidence: 97%

The crucial elements of the ‘last step’ of programmed cell death induced by kinetin in root cortex of V. faba ssp. minor seedlings

et al. 2014

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Kinetin-induced programmed cell death, manifested by condensation, degradation and methylation of DNA and fluctuation of kinase activities and ATP levels, is an autolytic and root cortex cell-specific process. The last step of programmed cell death (PCD) induced by kinetin in the root cortex of V. faba ssp. minor seedlings was explained using morphologic (nuclear chromatin/aggregation) and metabolic (DNA degradation, DNA methylation and kinases activity) analyses. This step involves: (1) decrease in nuclear DNA content, (2) increase in the number of 4',6-diamidino-2-phenylindole (DAPI)-stained chromocenters, and decrease in chromomycin A3 (CMA3)-stained chromocenters, (3) increase in fluorescence intensity of CMA3-stained chromocenters, (4) condensation of DAPI-stained and loosening of CMA3-stained chromatin, (5) fluctuation of the level of DNA methylation, (6) fluctuation of activities of exo-/endonucleolytic Zn(2+) and Ca(2+)/Mg(2+)-dependent nucleases, (7) changes in H1 and core histone kinase activities and (8) decrease in cellular ATP amount. These results confirmed that kinetin-induced PCD was a specific process. Additionally, based on data presented in this paper (DNA condensation and ATP depletion) and previous studies [increase in vacuole, increase in amount of cytosolic calcium ions, ROS production and cytosol acidification "in Byczkowska et al. (Protoplasma 250:121-128, 2013)"], we propose that the process resembles autolytic type of cell death, the most common type of death during development of plants. Lastly, the observations also suggested that regulation of these processes might be under control of epigenetic (methylation/phosphorylation) mechanisms.

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High levels of the cytokinin BAP suppress programmed cell death in hybrid tobacco cells (Nicotiana suaveolens*N. tabacum) expressing hybrid lethality

Cited by 10 publications

References 23 publications

Kinetin induces cell death in root cortex cells of Vicia faba ssp. minor seedlings

Kinetin induces cell death in root cortex cells of Vicia faba ssp. minor seedlings

Cytokinin vectors mediate marker-free and backbone-free plant transformation

The crucial elements of the ‘last step’ of programmed cell death induced by kinetin in root cortex of V. faba ssp. minor seedlings

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