Limits...
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.

Show MeSH

Related in: MedlinePlus

RSS1 ensures cell division activity at the G1–S transition.(a, b) Flow cytometry measurements of nuclei from the basal shoot tissues in 1-week-old WT and rss1-2 plants grown under non-stressed (−NaCl) and salt-stressed (+150 mM NaCl) conditions. (a) The representative data of the 2C and 4C cells. The number of nuclei is plotted according to their fluorescence intensity. (b) The ratio of the 2C (top) and 4C (bottom) cells in WT (blue) and rss1-2 (magenta). Mean±s.d., n=5–9. Asterisks, a significant difference between WT and rss1-2 (P=0.0052 (top panel), P=0.0002 (bottom panel); one-tailed t-test). (c, d) In situ analysis of the expression of histone H4 (red) and cyclin B2 (purple). Antisense probes for histone H4 and cyclin B2 were labelled differentially and hybridized with longitudinal sections of the basal shoot in WT and rss1-2 seedlings grown in the presence of 150 mM NaCl. (c) Overviews of the longitudinal sections, including the shoot apical meristem (SAM) and leaf primordia of WT (left) and rss1-2 (right). (d) Magnified views of the in situ detection of transcripts for histone H4 (red) and cyclin B2 (purple) in the shoot basal tissue. (top) WT. (bottom) rss1-2. Black lines trace the leaf margin of primordium 3 (P3). (e) Rate of cells that express transcripts for histone H4 (magenta) and cyclin B2 (blue) in the leaf margin of P3 in (d). Two seedlings (nos. 1 and 2) were analysed for WT and rss1-2, respectively. The average scores based on the observation of two to three serial sections are shown. (f, g) In situ detection of histone H4 mRNA (red signals) in the SAM region in WT (left each) and rss1-2 (right each) plants grown under non-stressed (f) and salt-stressed conditions (g). The regions of layer 1 (L1) in the SAM used for counting the cell number are traced by black lines. Arrows indicate the SAM in (c, d). Bars indicate 200 μm in (c, d), and 50 μm in (f, g).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3104554&req=5

f5: RSS1 ensures cell division activity at the G1–S transition.(a, b) Flow cytometry measurements of nuclei from the basal shoot tissues in 1-week-old WT and rss1-2 plants grown under non-stressed (−NaCl) and salt-stressed (+150 mM NaCl) conditions. (a) The representative data of the 2C and 4C cells. The number of nuclei is plotted according to their fluorescence intensity. (b) The ratio of the 2C (top) and 4C (bottom) cells in WT (blue) and rss1-2 (magenta). Mean±s.d., n=5–9. Asterisks, a significant difference between WT and rss1-2 (P=0.0052 (top panel), P=0.0002 (bottom panel); one-tailed t-test). (c, d) In situ analysis of the expression of histone H4 (red) and cyclin B2 (purple). Antisense probes for histone H4 and cyclin B2 were labelled differentially and hybridized with longitudinal sections of the basal shoot in WT and rss1-2 seedlings grown in the presence of 150 mM NaCl. (c) Overviews of the longitudinal sections, including the shoot apical meristem (SAM) and leaf primordia of WT (left) and rss1-2 (right). (d) Magnified views of the in situ detection of transcripts for histone H4 (red) and cyclin B2 (purple) in the shoot basal tissue. (top) WT. (bottom) rss1-2. Black lines trace the leaf margin of primordium 3 (P3). (e) Rate of cells that express transcripts for histone H4 (magenta) and cyclin B2 (blue) in the leaf margin of P3 in (d). Two seedlings (nos. 1 and 2) were analysed for WT and rss1-2, respectively. The average scores based on the observation of two to three serial sections are shown. (f, g) In situ detection of histone H4 mRNA (red signals) in the SAM region in WT (left each) and rss1-2 (right each) plants grown under non-stressed (f) and salt-stressed conditions (g). The regions of layer 1 (L1) in the SAM used for counting the cell number are traced by black lines. Arrows indicate the SAM in (c, d). Bars indicate 200 μm in (c, d), and 50 μm in (f, g).

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)

RSS1 ensures cell division activity at the G1–S transition.(a, b) Flow cytometry measurements of nuclei from the basal shoot tissues in 1-week-old WT and rss1-2 plants grown under non-stressed (−NaCl) and salt-stressed (+150 mM NaCl) conditions. (a) The representative data of the 2C and 4C cells. The number of nuclei is plotted according to their fluorescence intensity. (b) The ratio of the 2C (top) and 4C (bottom) cells in WT (blue) and rss1-2 (magenta). Mean±s.d., n=5–9. Asterisks, a significant difference between WT and rss1-2 (P=0.0052 (top panel), P=0.0002 (bottom panel); one-tailed t-test). (c, d) In situ analysis of the expression of histone H4 (red) and cyclin B2 (purple). Antisense probes for histone H4 and cyclin B2 were labelled differentially and hybridized with longitudinal sections of the basal shoot in WT and rss1-2 seedlings grown in the presence of 150 mM NaCl. (c) Overviews of the longitudinal sections, including the shoot apical meristem (SAM) and leaf primordia of WT (left) and rss1-2 (right). (d) Magnified views of the in situ detection of transcripts for histone H4 (red) and cyclin B2 (purple) in the shoot basal tissue. (top) WT. (bottom) rss1-2. Black lines trace the leaf margin of primordium 3 (P3). (e) Rate of cells that express transcripts for histone H4 (magenta) and cyclin B2 (blue) in the leaf margin of P3 in (d). Two seedlings (nos. 1 and 2) were analysed for WT and rss1-2, respectively. The average scores based on the observation of two to three serial sections are shown. (f, g) In situ detection of histone H4 mRNA (red signals) in the SAM region in WT (left each) and rss1-2 (right each) plants grown under non-stressed (f) and salt-stressed conditions (g). The regions of layer 1 (L1) in the SAM used for counting the cell number are traced by black lines. Arrows indicate the SAM in (c, d). Bars indicate 200 μm in (c, d), and 50 μm in (f, g).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3104554&req=5

f5: RSS1 ensures cell division activity at the G1–S transition.(a, b) Flow cytometry measurements of nuclei from the basal shoot tissues in 1-week-old WT and rss1-2 plants grown under non-stressed (−NaCl) and salt-stressed (+150 mM NaCl) conditions. (a) The representative data of the 2C and 4C cells. The number of nuclei is plotted according to their fluorescence intensity. (b) The ratio of the 2C (top) and 4C (bottom) cells in WT (blue) and rss1-2 (magenta). Mean±s.d., n=5–9. Asterisks, a significant difference between WT and rss1-2 (P=0.0052 (top panel), P=0.0002 (bottom panel); one-tailed t-test). (c, d) In situ analysis of the expression of histone H4 (red) and cyclin B2 (purple). Antisense probes for histone H4 and cyclin B2 were labelled differentially and hybridized with longitudinal sections of the basal shoot in WT and rss1-2 seedlings grown in the presence of 150 mM NaCl. (c) Overviews of the longitudinal sections, including the shoot apical meristem (SAM) and leaf primordia of WT (left) and rss1-2 (right). (d) Magnified views of the in situ detection of transcripts for histone H4 (red) and cyclin B2 (purple) in the shoot basal tissue. (top) WT. (bottom) rss1-2. Black lines trace the leaf margin of primordium 3 (P3). (e) Rate of cells that express transcripts for histone H4 (magenta) and cyclin B2 (blue) in the leaf margin of P3 in (d). Two seedlings (nos. 1 and 2) were analysed for WT and rss1-2, respectively. The average scores based on the observation of two to three serial sections are shown. (f, g) In situ detection of histone H4 mRNA (red signals) in the SAM region in WT (left each) and rss1-2 (right each) plants grown under non-stressed (f) and salt-stressed conditions (g). The regions of layer 1 (L1) in the SAM used for counting the cell number are traced by black lines. Arrows indicate the SAM in (c, d). Bars indicate 200 μm in (c, d), and 50 μm in (f, g).
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