Abstract
Ethylene is known to influence the cell cycle (CC) via poorly characterized roles whilst nitric oxide (NO) has well-established roles in the animal CC but analogous role(s) have not been reported for plants. As NO and ethylene signaling events often interact we examined their role in CC in cultured cells derived from Arabidopsis thaliana wild-type (Col-0) plants and from ethylene-insensitive mutant ein2-1 plants. Both NO and ethylene were produced mainly during the first 5 days of the sub-cultivation period corresponding to the period of active cell division. However, in ein2-1 cells, ethylene generation was significantly reduced while NO levels were increased. With application of a range of concentrations of the NO donor, sodium nitroprusside (SNP) (between 20 and 500 μM) ethylene production was significantly diminished in Col-0 but unchanged in ein2-1 cells. Flow cytometry assays showed that in Col-0 cells treatments with 5 and 10 μM SNP concentrations led to an increase in S-phase cell number indicating the stimulation of G1/S transition. However, at ≥20 μM SNP CC progression was restrained at G1/S transition. In the mutant ein2-1 strain, the index of S-phase cells was not altered at 5–10 μM SNP but decreased dramatically at higher SNP concentrations. Concomitantly, 5 μM SNP induced transcription of genes encoding CDKA;1 and CYCD3;1 in Col-0 cells whereas transcription of CDKs and CYCs were not significantly altered in ein2-1 cells at any SNP concentrations examined. Hence, it is appears that EIN2 is required for full responses at each SNP concentration. In ein2-1 cells, greater amounts of NO, reactive oxygen species, and the tyrosine-nitrating peroxynitrite radical were detected, possibly indicating NO-dependent post-translational protein modifications which could stop CC. Thus, we suggest that in Arabidopsis cultured cells NO affects CC progression as a concentration-dependent modulator with a dependency on EIN2 for both ethylene production and a NO/ethylene regulatory function.
Highlights
The cell cycle (CC) is one of the most conserved processes operating in eukaryotic cells and its integrity is essential for an organism’s shape and function
Using actively growing Arabidopsis Col-0 and ein2-1 suspension cells (Figure S1), we studied the roles of ethylene and nitric oxide (NO) in CC progression
The effect of sodium nitroprusside (SNP) on Col-0 cells suggested that NO could repress rather than initiate ethylene production in Col-0 cells (Table 2). This was in contrast to the hypersensitive response during plant-pathogen interactions, where NO was required for ethylene production (Mur et al, 2008)
Summary
The cell cycle (CC) is one of the most conserved processes operating in eukaryotic cells and its integrity is essential for an organism’s shape and function. The CC has been extensively described in both plants (Dewitte and Murray, 2003) and animals (Norbury and Nurse, 1992) and is regulated by the sequential expression of cyclin-dependent kinases (CDK) which are activated by binding to the cyclins (CYC) (Dorée and Galas, 1994). Newly emerging CC regulatory steps, especially in plants, require further definition. Ethylene can positively or negatively affect CC progression but these steps have been poorly defined. Ortega-Martínez et al (2007) suggested that ethylene production and ethylene-modulated cell division was suppressed in the quiescent center of Arabidopsis thaliana roots. CC arrest in parallel with an increase in 1-aminocyclopropane-1-carboxylate (ACC) levels and the activation of ethylene signaling in A. thaliana leaves was observed during osmotic stress (Skirycz et al, 2011)
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