Gibberellin promotes histone H1 kinase activity and the expression of cdc2 and cyclin genes during the induction of rapid growth in deepwater rice internodes

Abstract

SummaryPartial submergence or treatment with either ethylene or gibberellin (GA) promotes rapid internodal growth in deepweter rice (Oryza sativa L.). Earlier work has shown that GA is the immediate hormonal signal for this growth response, which involves induction of the cell cycle at the G2/M phase transition and subsequent enhancement in the rate of DNA synthesis. In all eukaryotes, onset of mitosis is regulated by the p34 cdca/c°cas protein kinase, whose activity is assayed by in vitro phosphorylation of histone H1. It was found that GA enhanced the activity of p34~'z/coCn-like histone H1 kinase in the intercalary meristem of rice internodes. The enzyme activity showed a sharp peak that correlated with a decrease in the population of cells in the G2 phase during the first 4 h of GA treatment but not with changes in DNA synthesis. The level of histone H1 kinase activity increased again when cell division activity in the intercalary meristem is known to be high. The expression of two cdc2 homologs was examined. The mRNA level of one of these, cdc2Os-2, was increased after 1 h of GA treatment, whereas the mRNA level of the other, cdc2Os-1, was not affected. Two cDNAs, cycOsl and cycOs2, which show high homology to cyclin cDNAs, were cloned from rice. They share 75.1% sequence identity at the amino acid level, and both of them are encoded by mRNAs of 1.6 kb. Expression of the two corresponding cyclin genes was enhanced by GA, and the time course of the induction was compatible with a role for both cyclins in regulating the G2/M phase transition. The cyclins were expressed in the intercalary meristem and the elongation zone of the internode, but the GAinduced increase in transcript levels was restricted to the meristem only. The results support the hypothesis that induction of mitosis by GA is brought about by increased p34 cdc2/coc2s protein kinaee activity, which may be the result of transcriptional activation of the cdc2Os-2, cycOsl and cycOs2 genes.

Deepwater Rice: A Model Plant to Study Stem Elongation

“…Progression of cells in the IM through the cell cycle has been followed by measuring [ 3 H]thymidine incorporation, by flow cytometry and by determining the expression of genes whose products regulate the entry of cells into mitosis and the S phase (Sauter and Kende, 1992a;Sauter et al, 1995;Lorbiecke and Sauter, 1998). The activation of the cell cycle by GA and submergence was reflected in increased expression of a gene encoding a p34 cdc2 -like histone H1 kinase (cdc2Os-2) and of the corresponding enzymatic activity (Sauter et al, 1995;Lorbiecke and Sauter, 1998).…”

“…The activation of the cell cycle by GA and submergence was reflected in increased expression of a gene encoding a p34 cdc2 -like histone H1 kinase (cdc2Os-2) and of the corresponding enzymatic activity (Sauter et al, 1995;Lorbiecke and Sauter, 1998). Similarly, the transcript levels of two cyclin genes, cycOs1 and cycOs2, increased in GA-treated and submerged internodes during the G2 phase, indicating that the corresponding cyclins control entry into the M phase (Sauter et al, 1995;Lorbiecke and Sauter, 1998). In a screen for GA-regulated genes using differential display of mRNA, two genes were identified whose products function in the cell cycle.…”

Gibberellins Promote Trichome Formation by Up-RegulatingGLABROUS1in Arabidopsis1

“…DNA content analysis of isolated trichomes indicate that spy-5 overbranched trichomes indeed have twice as much DNA as wild-type trichomes on average (D. Perazza, unpublished data). The role of GAs in cell division has been suggested since GAs induce a rapid rise in the abundance of a CDK1 homolog transcript in rice (Sauter et al, 1995;Jacobs, 1997). Endoreduplication can be seen as an alternative to cell division.…”

“…The gain-offunction gai mutant resembles mutants partially deficient in GA biosynthesis but exhibits a reduced sensitivity to exogenous GAs, whereas the spy mutants show an enhanced elongation or slender phenotype together with pale green foliage, early flowering, partial male sterility, and parthenogenic fruit development. At the cellular level GAs influence a full spectrum of processes ranging from microtubule arrangement in mesocotyl epidermal cells, cell wall growth, lipid metabolism, calcium transport (Hooley, 1994), and regulation of cyclin genes (Sauter et al, 1995). Until now, only a limited number of genes involved in these processes have been characterized, mainly encoding hydrolytic enzymes required during monocotyledon germination (Ni and Bradford, 1993).…”

Expression of an ortholog of replication protein A1 (RPA1) is induced by gibberellin in deepwater rice

“…The fraction of meristematic cells in the G 2 phase declined within 4 hr of GA treatment, indicating that these cells had entered mitosis (7). The expression of two cyclin genes in the intercalary meristem was enhanced by GA, and the time course of induction was compatible with a role for both cyclins in regulating the transition from the G 2 to M phase (11). Between 4 and 7 hr of incubation in GA, the rate of [ 3 H]thymidine incorporation into DNA doubled, showing an increase in DNA synthesis (7).…”