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RSS1 regulates the cell cycle and maintains meristematic activity under stress conditions in rice.

Ogawa D, Abe K, Miyao A, Kojima M, Sakakibara H, Mizutani M, Morita H, Toda Y, Hobo T, Sato Y, Hattori T, Hirochika H, Takeda S - Nat Commun (2011)

Bottom Line: Here we show that a rice protein, RSS1, whose stability is controlled by cell cycle phases, contributes to the vigour of meristematic cells and viability under salinity conditions.These effects of RSS1 are exerted by regulating the G1-S transition, possibly through an interaction of RSS1 with protein phosphatase 1, and are mediated by the phytohormone, cytokinin.RSS1 is conserved widely in plant lineages, except eudicots, suggesting that RSS1-dependent mechanisms might have been adopted in specific lineages during the evolutionary radiation of angiosperms.

View Article: PubMed Central - PubMed

Affiliation: Bioscience and Biotechnology Center, Nagoya University, Chikusa, Nagoya 464-8601, Japan.

ABSTRACT
Plant growth and development are sustained by continuous cell division in the meristems, which is perturbed by various environmental stresses. For the maintenance of meristematic functions, it is essential that cell division be coordinated with cell differentiation. However, it is unknown how the proliferative activities of the meristems and the coordination between cell division and differentiation are maintained under stressful conditions. Here we show that a rice protein, RSS1, whose stability is controlled by cell cycle phases, contributes to the vigour of meristematic cells and viability under salinity conditions. These effects of RSS1 are exerted by regulating the G1-S transition, possibly through an interaction of RSS1 with protein phosphatase 1, and are mediated by the phytohormone, cytokinin. RSS1 is conserved widely in plant lineages, except eudicots, suggesting that RSS1-dependent mechanisms might have been adopted in specific lineages during the evolutionary radiation of angiosperms.

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Altered expression of genes in rss1.(a) The classification of the genes whose expression was affected by the defects in rss1. RNA levels in the shoot basal proliferative tissues of 1-week-old WT and rss1-2 seedlings grown in the absence (−) or presence of 150 mM NaCl (+) were examined by microarray with three biological replicates. Differentially expressed genes were statistically determined by the rank product (P<0.01) and two-way ANOVA (P<0.01). The ratio of the number of genes, whose expression was significantly upregulated (magenta) or downregulated (blue) in rss1, to the number of genes in the indicated gene category is shown. Among the total number of 29,859 genes examined, 1,129 genes (3.8%) and 792 genes (2.7%) were up- and downregulated in rss1, respectively, under the normal growth condition, whereas 1,607 genes (5.4%) and 1,581 genes (5.3%) were up- and downregulated in rss1, respectively, under conditions of salinity. Categories included in 'Biological process' were selected from the Gene Ontology (GO) database (http://www.gramene.org/plant_ontology/index.html). Categories of 'Shoot apex-specific,' stress responsive (long-term) and stress responsive (short-term) were selected from our microarray data and public array databases (see Methods). (b) A heat map view of the expression pattern of down- or upregulated genes selected from the indicated categories. 'Salt-inducible' (or 'salt-repressible') genes are a mixture of genes that were commonly up- (or down)regulated under the both long- and short-term salinity conditions. The levels of expression are shown with log2-transformed values (bottom) based on the microarray data, as in (a). The patterns of expression with the three biological replicates are shown. (c, d) The expression of PCNA (c) and CycB2;1 (d) in the basal shoot tissues of one-week-old WT and rss1-2 seedlings, as determined by microarray analysis (magenta), or of WT and rss1-1, as determined by quantitative RT-PCR (yellow). Seedlings were grown in the absence (−) or presence of 150 mM NaCl (+). Mean±s.d., n=3. The relative expression levels in the real-time RT-PCR analysis were normalized by the expression level of ubiquitin E2.
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f4: Altered expression of genes in rss1.(a) The classification of the genes whose expression was affected by the defects in rss1. RNA levels in the shoot basal proliferative tissues of 1-week-old WT and rss1-2 seedlings grown in the absence (−) or presence of 150 mM NaCl (+) were examined by microarray with three biological replicates. Differentially expressed genes were statistically determined by the rank product (P<0.01) and two-way ANOVA (P<0.01). The ratio of the number of genes, whose expression was significantly upregulated (magenta) or downregulated (blue) in rss1, to the number of genes in the indicated gene category is shown. Among the total number of 29,859 genes examined, 1,129 genes (3.8%) and 792 genes (2.7%) were up- and downregulated in rss1, respectively, under the normal growth condition, whereas 1,607 genes (5.4%) and 1,581 genes (5.3%) were up- and downregulated in rss1, respectively, under conditions of salinity. Categories included in 'Biological process' were selected from the Gene Ontology (GO) database (http://www.gramene.org/plant_ontology/index.html). Categories of 'Shoot apex-specific,' stress responsive (long-term) and stress responsive (short-term) were selected from our microarray data and public array databases (see Methods). (b) A heat map view of the expression pattern of down- or upregulated genes selected from the indicated categories. 'Salt-inducible' (or 'salt-repressible') genes are a mixture of genes that were commonly up- (or down)regulated under the both long- and short-term salinity conditions. The levels of expression are shown with log2-transformed values (bottom) based on the microarray data, as in (a). The patterns of expression with the three biological replicates are shown. (c, d) The expression of PCNA (c) and CycB2;1 (d) in the basal shoot tissues of one-week-old WT and rss1-2 seedlings, as determined by microarray analysis (magenta), or of WT and rss1-1, as determined by quantitative RT-PCR (yellow). Seedlings were grown in the absence (−) or presence of 150 mM NaCl (+). Mean±s.d., n=3. The relative expression levels in the real-time RT-PCR analysis were normalized by the expression level of ubiquitin E2.

Mentions: To obtain further insight into the function of RSS1, we characterized the transcriptomic profiles in the basal proliferative region of the shoot between wild type and rss1 grown under normal or high-salt conditions. In agreement with the proposed function of RSS1, genes involved in the cell cycle and DNA replication were preferentially downregulated in rss1 under high-salt conditions (Fig. 4a,b), as exemplified by an S-phase-specific gene, PCNA, and an M-phase cyclin, CycB2;1 (Fig. 4c,d). Moreover, ploidy analysis demonstrated that the relative number of cells in G2-M phase (4C cells) compared with G1 phase (2C cells) was decreased in rss1 under salinity (Fig. 5a,b). These results suggest that RSS1 is required for the G1–S transition and subsequent cell cycle progression under stressful conditions. Conspicuously, more than 30% of the genes that were expressed specifically in the shoot apex were coordinately downregulated in rss1 under high-salt conditions (Fig. 4a,b), supporting the proposed function of RSS1 in maintaining proliferative tissue activity.


RSS1 regulates the cell cycle and maintains meristematic activity under stress conditions in rice.

Ogawa D, Abe K, Miyao A, Kojima M, Sakakibara H, Mizutani M, Morita H, Toda Y, Hobo T, Sato Y, Hattori T, Hirochika H, Takeda S - Nat Commun (2011)

Altered expression of genes in rss1.(a) The classification of the genes whose expression was affected by the defects in rss1. RNA levels in the shoot basal proliferative tissues of 1-week-old WT and rss1-2 seedlings grown in the absence (−) or presence of 150 mM NaCl (+) were examined by microarray with three biological replicates. Differentially expressed genes were statistically determined by the rank product (P<0.01) and two-way ANOVA (P<0.01). The ratio of the number of genes, whose expression was significantly upregulated (magenta) or downregulated (blue) in rss1, to the number of genes in the indicated gene category is shown. Among the total number of 29,859 genes examined, 1,129 genes (3.8%) and 792 genes (2.7%) were up- and downregulated in rss1, respectively, under the normal growth condition, whereas 1,607 genes (5.4%) and 1,581 genes (5.3%) were up- and downregulated in rss1, respectively, under conditions of salinity. Categories included in 'Biological process' were selected from the Gene Ontology (GO) database (http://www.gramene.org/plant_ontology/index.html). Categories of 'Shoot apex-specific,' stress responsive (long-term) and stress responsive (short-term) were selected from our microarray data and public array databases (see Methods). (b) A heat map view of the expression pattern of down- or upregulated genes selected from the indicated categories. 'Salt-inducible' (or 'salt-repressible') genes are a mixture of genes that were commonly up- (or down)regulated under the both long- and short-term salinity conditions. The levels of expression are shown with log2-transformed values (bottom) based on the microarray data, as in (a). The patterns of expression with the three biological replicates are shown. (c, d) The expression of PCNA (c) and CycB2;1 (d) in the basal shoot tissues of one-week-old WT and rss1-2 seedlings, as determined by microarray analysis (magenta), or of WT and rss1-1, as determined by quantitative RT-PCR (yellow). Seedlings were grown in the absence (−) or presence of 150 mM NaCl (+). Mean±s.d., n=3. The relative expression levels in the real-time RT-PCR analysis were normalized by the expression level of ubiquitin E2.
© Copyright Policy - open-access
Related In: Results  -  Collection

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f4: Altered expression of genes in rss1.(a) The classification of the genes whose expression was affected by the defects in rss1. RNA levels in the shoot basal proliferative tissues of 1-week-old WT and rss1-2 seedlings grown in the absence (−) or presence of 150 mM NaCl (+) were examined by microarray with three biological replicates. Differentially expressed genes were statistically determined by the rank product (P<0.01) and two-way ANOVA (P<0.01). The ratio of the number of genes, whose expression was significantly upregulated (magenta) or downregulated (blue) in rss1, to the number of genes in the indicated gene category is shown. Among the total number of 29,859 genes examined, 1,129 genes (3.8%) and 792 genes (2.7%) were up- and downregulated in rss1, respectively, under the normal growth condition, whereas 1,607 genes (5.4%) and 1,581 genes (5.3%) were up- and downregulated in rss1, respectively, under conditions of salinity. Categories included in 'Biological process' were selected from the Gene Ontology (GO) database (http://www.gramene.org/plant_ontology/index.html). Categories of 'Shoot apex-specific,' stress responsive (long-term) and stress responsive (short-term) were selected from our microarray data and public array databases (see Methods). (b) A heat map view of the expression pattern of down- or upregulated genes selected from the indicated categories. 'Salt-inducible' (or 'salt-repressible') genes are a mixture of genes that were commonly up- (or down)regulated under the both long- and short-term salinity conditions. The levels of expression are shown with log2-transformed values (bottom) based on the microarray data, as in (a). The patterns of expression with the three biological replicates are shown. (c, d) The expression of PCNA (c) and CycB2;1 (d) in the basal shoot tissues of one-week-old WT and rss1-2 seedlings, as determined by microarray analysis (magenta), or of WT and rss1-1, as determined by quantitative RT-PCR (yellow). Seedlings were grown in the absence (−) or presence of 150 mM NaCl (+). Mean±s.d., n=3. The relative expression levels in the real-time RT-PCR analysis were normalized by the expression level of ubiquitin E2.
Mentions: To obtain further insight into the function of RSS1, we characterized the transcriptomic profiles in the basal proliferative region of the shoot between wild type and rss1 grown under normal or high-salt conditions. In agreement with the proposed function of RSS1, genes involved in the cell cycle and DNA replication were preferentially downregulated in rss1 under high-salt conditions (Fig. 4a,b), as exemplified by an S-phase-specific gene, PCNA, and an M-phase cyclin, CycB2;1 (Fig. 4c,d). Moreover, ploidy analysis demonstrated that the relative number of cells in G2-M phase (4C cells) compared with G1 phase (2C cells) was decreased in rss1 under salinity (Fig. 5a,b). These results suggest that RSS1 is required for the G1–S transition and subsequent cell cycle progression under stressful conditions. Conspicuously, more than 30% of the genes that were expressed specifically in the shoot apex were coordinately downregulated in rss1 under high-salt conditions (Fig. 4a,b), supporting the proposed function of RSS1 in maintaining proliferative tissue activity.

Bottom Line: Here we show that a rice protein, RSS1, whose stability is controlled by cell cycle phases, contributes to the vigour of meristematic cells and viability under salinity conditions.These effects of RSS1 are exerted by regulating the G1-S transition, possibly through an interaction of RSS1 with protein phosphatase 1, and are mediated by the phytohormone, cytokinin.RSS1 is conserved widely in plant lineages, except eudicots, suggesting that RSS1-dependent mechanisms might have been adopted in specific lineages during the evolutionary radiation of angiosperms.

View Article: PubMed Central - PubMed

Affiliation: Bioscience and Biotechnology Center, Nagoya University, Chikusa, Nagoya 464-8601, Japan.

ABSTRACT
Plant growth and development are sustained by continuous cell division in the meristems, which is perturbed by various environmental stresses. For the maintenance of meristematic functions, it is essential that cell division be coordinated with cell differentiation. However, it is unknown how the proliferative activities of the meristems and the coordination between cell division and differentiation are maintained under stressful conditions. Here we show that a rice protein, RSS1, whose stability is controlled by cell cycle phases, contributes to the vigour of meristematic cells and viability under salinity conditions. These effects of RSS1 are exerted by regulating the G1-S transition, possibly through an interaction of RSS1 with protein phosphatase 1, and are mediated by the phytohormone, cytokinin. RSS1 is conserved widely in plant lineages, except eudicots, suggesting that RSS1-dependent mechanisms might have been adopted in specific lineages during the evolutionary radiation of angiosperms.

Show MeSH
Related in: MedlinePlus