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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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rss1 is hypersensitive to salt.(a, b) The phenotype of rss1. WT and rss1-1 seedlings were grown in the absence (−) or presence of 150 mM NaCl (+) for 15 days. (a) Seedlings. (b) The roots in (a) were visualized by floating in water. Left, WT (−NaCl); middle-left, rss1-1 (−NaCl); middle-right, WT (+NaCl); right, rss1-1 (+NaCl). (c) Root tips of WT (top) and rss1-1 (bottom) seedlings grown in the absence (left panels) or presence of 150 mM NaCl (right panels). (d) The root branching pattern of rss1-1 grown in the presence of 150 mM NaCl. (e) A schematic illustration of rss1-1 root branching under high-salt conditions. (f, g) Propidium iodide (PI) staining of the root cells of WT (f) and rss1-2 (g) plants grown under high-salt conditions (150 mM NaCl, 5 days). (h) The length of (top) and the number of cells in (bottom) the MZ and EZ in the root of WT (blue) and rss1-1 (magenta) plants grown under normal (−NaCl, 4 days) or high-salt conditions (+150 mM NaCl, 5 days). Mean±s.d., n=4. (i) PI staining of root cells of WT grown in the presence of 150 mM NaCl and 10 mg/l aphidicolin. (j) The amount of Na+ (top) and K+ (bottom) in the shoot of WT (blue) and rss1 (magenta) seedlings grown in the absence (−) or presence (+) of 150 mM NaCl for 14 days. The data represent the mean±s.d., n=5. The K+/Na+ ratios were 211.1±46.2 in WT versus 164.4±32.2 in rss1-1 under normal conditions and 1.23±0.17 in WT versus 1.19±0.24 in rss1-1 under high-salt conditions (mean±s.d., n=5). (k) rss1 calli are hypersensitive to salt. WT or rss1-1 calli derived from seeds were grown in MS medium containing 2 mg/l 2,4-dichlorophenoxy acetic acid. Fresh callus pieces were then transferred to fresh medium of the indicated concentrations of NaCl and cultured at 25 °C for 3 weeks. Bars: 2 cm (a, b), 0.5 mm (f, g, i), 1 cm (k). EZ, elongation zone; MTZ, maturation zone; MZ, meristematic zone.
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f1: rss1 is hypersensitive to salt.(a, b) The phenotype of rss1. WT and rss1-1 seedlings were grown in the absence (−) or presence of 150 mM NaCl (+) for 15 days. (a) Seedlings. (b) The roots in (a) were visualized by floating in water. Left, WT (−NaCl); middle-left, rss1-1 (−NaCl); middle-right, WT (+NaCl); right, rss1-1 (+NaCl). (c) Root tips of WT (top) and rss1-1 (bottom) seedlings grown in the absence (left panels) or presence of 150 mM NaCl (right panels). (d) The root branching pattern of rss1-1 grown in the presence of 150 mM NaCl. (e) A schematic illustration of rss1-1 root branching under high-salt conditions. (f, g) Propidium iodide (PI) staining of the root cells of WT (f) and rss1-2 (g) plants grown under high-salt conditions (150 mM NaCl, 5 days). (h) The length of (top) and the number of cells in (bottom) the MZ and EZ in the root of WT (blue) and rss1-1 (magenta) plants grown under normal (−NaCl, 4 days) or high-salt conditions (+150 mM NaCl, 5 days). Mean±s.d., n=4. (i) PI staining of root cells of WT grown in the presence of 150 mM NaCl and 10 mg/l aphidicolin. (j) The amount of Na+ (top) and K+ (bottom) in the shoot of WT (blue) and rss1 (magenta) seedlings grown in the absence (−) or presence (+) of 150 mM NaCl for 14 days. The data represent the mean±s.d., n=5. The K+/Na+ ratios were 211.1±46.2 in WT versus 164.4±32.2 in rss1-1 under normal conditions and 1.23±0.17 in WT versus 1.19±0.24 in rss1-1 under high-salt conditions (mean±s.d., n=5). (k) rss1 calli are hypersensitive to salt. WT or rss1-1 calli derived from seeds were grown in MS medium containing 2 mg/l 2,4-dichlorophenoxy acetic acid. Fresh callus pieces were then transferred to fresh medium of the indicated concentrations of NaCl and cultured at 25 °C for 3 weeks. Bars: 2 cm (a, b), 0.5 mm (f, g, i), 1 cm (k). EZ, elongation zone; MTZ, maturation zone; MZ, meristematic zone.

Mentions: To explore the mechanisms underlying salt tolerance in monocots, we performed a genetic screen of rice populations mutagenized with the retrotransposon, Tos17 (ref. 17), and we identified a gene whose defect caused an extreme dwarf and short-root phenotype under high-salt, but not normal growth conditions (Fig. 1a). The obtained loss-of-function mutant, designated rss1 (rice salt sensitive 1), exhibited irreversible growth inhibition after exposure to 150 mM NaCl for 2 weeks. The rss1 seedlings exhibited highly branched roots, possibly reflecting impaired root apex activity (Fig. 1b–e). Such a branching pattern was not observed in wild-type (WT) plants treated with various concentrations of salt, including those higher than 150 mM. In the root apex of young rss1 seedlings, the size of the meristematic zone (MZ) and the elongation zone (EZ) decreased under salinity, concomitant with a reduction in the number of cells in both zones (Fig. 1f–h and Supplementary Fig. S1). Interestingly, the defects in rss1 were mimicked in WT roots by the application of the DNA synthesis inhibitor, aphidicolin, which induces the cell cycle arrest at the G1–S boundary (Fig. 1i). The dramatic reduction in the sizes of both the MZ and EZ in the rss1 root under high salinities probably indicates that the number of cells supplied from the MZ to EZ was considerably decreased, while the rate of differentiation was less affected. A decreased rate of cell division and a constant rate of differentiation will result in the reduction of the MZ size. The salt hypersensitivity of rss1 was not due to the overloading of Na+ because the shoot K+/Na+ ratio in the mutant was nearly the same as that in WT under high-salt conditions (Fig. 1j). Moreover, rss1 calli were hypersensitive to salt, suggesting that RSS1 confers salt tolerance primarily at the cellular level (Fig. 1k and Supplementary Fig. S2). Salinity is known to cause detrimental effects through not only ionic toxicity but also a water deficit that results from hyper-osmotic stress1018. Notably, rss1 was hypersensitive to both ionic and hyper-osmotic stress caused by low concentrations of LiCl and high concentrations of sorbitol, respectively (Supplementary Fig. S3).


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 is hypersensitive to salt.(a, b) The phenotype of rss1. WT and rss1-1 seedlings were grown in the absence (−) or presence of 150 mM NaCl (+) for 15 days. (a) Seedlings. (b) The roots in (a) were visualized by floating in water. Left, WT (−NaCl); middle-left, rss1-1 (−NaCl); middle-right, WT (+NaCl); right, rss1-1 (+NaCl). (c) Root tips of WT (top) and rss1-1 (bottom) seedlings grown in the absence (left panels) or presence of 150 mM NaCl (right panels). (d) The root branching pattern of rss1-1 grown in the presence of 150 mM NaCl. (e) A schematic illustration of rss1-1 root branching under high-salt conditions. (f, g) Propidium iodide (PI) staining of the root cells of WT (f) and rss1-2 (g) plants grown under high-salt conditions (150 mM NaCl, 5 days). (h) The length of (top) and the number of cells in (bottom) the MZ and EZ in the root of WT (blue) and rss1-1 (magenta) plants grown under normal (−NaCl, 4 days) or high-salt conditions (+150 mM NaCl, 5 days). Mean±s.d., n=4. (i) PI staining of root cells of WT grown in the presence of 150 mM NaCl and 10 mg/l aphidicolin. (j) The amount of Na+ (top) and K+ (bottom) in the shoot of WT (blue) and rss1 (magenta) seedlings grown in the absence (−) or presence (+) of 150 mM NaCl for 14 days. The data represent the mean±s.d., n=5. The K+/Na+ ratios were 211.1±46.2 in WT versus 164.4±32.2 in rss1-1 under normal conditions and 1.23±0.17 in WT versus 1.19±0.24 in rss1-1 under high-salt conditions (mean±s.d., n=5). (k) rss1 calli are hypersensitive to salt. WT or rss1-1 calli derived from seeds were grown in MS medium containing 2 mg/l 2,4-dichlorophenoxy acetic acid. Fresh callus pieces were then transferred to fresh medium of the indicated concentrations of NaCl and cultured at 25 °C for 3 weeks. Bars: 2 cm (a, b), 0.5 mm (f, g, i), 1 cm (k). EZ, elongation zone; MTZ, maturation zone; MZ, meristematic zone.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f1: rss1 is hypersensitive to salt.(a, b) The phenotype of rss1. WT and rss1-1 seedlings were grown in the absence (−) or presence of 150 mM NaCl (+) for 15 days. (a) Seedlings. (b) The roots in (a) were visualized by floating in water. Left, WT (−NaCl); middle-left, rss1-1 (−NaCl); middle-right, WT (+NaCl); right, rss1-1 (+NaCl). (c) Root tips of WT (top) and rss1-1 (bottom) seedlings grown in the absence (left panels) or presence of 150 mM NaCl (right panels). (d) The root branching pattern of rss1-1 grown in the presence of 150 mM NaCl. (e) A schematic illustration of rss1-1 root branching under high-salt conditions. (f, g) Propidium iodide (PI) staining of the root cells of WT (f) and rss1-2 (g) plants grown under high-salt conditions (150 mM NaCl, 5 days). (h) The length of (top) and the number of cells in (bottom) the MZ and EZ in the root of WT (blue) and rss1-1 (magenta) plants grown under normal (−NaCl, 4 days) or high-salt conditions (+150 mM NaCl, 5 days). Mean±s.d., n=4. (i) PI staining of root cells of WT grown in the presence of 150 mM NaCl and 10 mg/l aphidicolin. (j) The amount of Na+ (top) and K+ (bottom) in the shoot of WT (blue) and rss1 (magenta) seedlings grown in the absence (−) or presence (+) of 150 mM NaCl for 14 days. The data represent the mean±s.d., n=5. The K+/Na+ ratios were 211.1±46.2 in WT versus 164.4±32.2 in rss1-1 under normal conditions and 1.23±0.17 in WT versus 1.19±0.24 in rss1-1 under high-salt conditions (mean±s.d., n=5). (k) rss1 calli are hypersensitive to salt. WT or rss1-1 calli derived from seeds were grown in MS medium containing 2 mg/l 2,4-dichlorophenoxy acetic acid. Fresh callus pieces were then transferred to fresh medium of the indicated concentrations of NaCl and cultured at 25 °C for 3 weeks. Bars: 2 cm (a, b), 0.5 mm (f, g, i), 1 cm (k). EZ, elongation zone; MTZ, maturation zone; MZ, meristematic zone.
Mentions: To explore the mechanisms underlying salt tolerance in monocots, we performed a genetic screen of rice populations mutagenized with the retrotransposon, Tos17 (ref. 17), and we identified a gene whose defect caused an extreme dwarf and short-root phenotype under high-salt, but not normal growth conditions (Fig. 1a). The obtained loss-of-function mutant, designated rss1 (rice salt sensitive 1), exhibited irreversible growth inhibition after exposure to 150 mM NaCl for 2 weeks. The rss1 seedlings exhibited highly branched roots, possibly reflecting impaired root apex activity (Fig. 1b–e). Such a branching pattern was not observed in wild-type (WT) plants treated with various concentrations of salt, including those higher than 150 mM. In the root apex of young rss1 seedlings, the size of the meristematic zone (MZ) and the elongation zone (EZ) decreased under salinity, concomitant with a reduction in the number of cells in both zones (Fig. 1f–h and Supplementary Fig. S1). Interestingly, the defects in rss1 were mimicked in WT roots by the application of the DNA synthesis inhibitor, aphidicolin, which induces the cell cycle arrest at the G1–S boundary (Fig. 1i). The dramatic reduction in the sizes of both the MZ and EZ in the rss1 root under high salinities probably indicates that the number of cells supplied from the MZ to EZ was considerably decreased, while the rate of differentiation was less affected. A decreased rate of cell division and a constant rate of differentiation will result in the reduction of the MZ size. The salt hypersensitivity of rss1 was not due to the overloading of Na+ because the shoot K+/Na+ ratio in the mutant was nearly the same as that in WT under high-salt conditions (Fig. 1j). Moreover, rss1 calli were hypersensitive to salt, suggesting that RSS1 confers salt tolerance primarily at the cellular level (Fig. 1k and Supplementary Fig. S2). Salinity is known to cause detrimental effects through not only ionic toxicity but also a water deficit that results from hyper-osmotic stress1018. Notably, rss1 was hypersensitive to both ionic and hyper-osmotic stress caused by low concentrations of LiCl and high concentrations of sorbitol, respectively (Supplementary Fig. S3).

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