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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 affects cytokinin action.(a) The exogenous application of cytokinins alleviated the lethality of rss1 under high-salt conditions. The basal shoot segments without roots (2.5 cm long) were excised from 1-week-old WT and rss1-2 plants, transferred to the medium containing 150 mM NaCl with or without the indicated concentrations of kinetin, and grown for 19 days. Bars, 5 cm. (b) The expression of CKX2 (top) and RR1 (bottom) in the basal shoot tissues of 1-week-old WT and rss1-2 seedlings, as determined by microarray analysis (magenta), or of WT and rss1-1 plants, as determined by quantitative RT-PCR (yellow). Seedlings grown under the normal (−NaCl) and saline (+NaCl) conditions were tested. The expression levels of the tested genes quantified by RT-PCR were normalized with that of ubiquitin E2. Mean±s.d., n=3. Asterisks, a significant difference between WT and rss1-2 under the saline condition. (P=0.002 (by real-time RT-PCR), P=0.001 (by microarray); one-tailed t-test). (c) A schematic illustration of the metabolic pathway of trans-zeatin (tZ) adapted from previous reports3334. tZR, tZ riboside; tZRMP, tZR 5′-monophosphate; tZOG, tZ-O-glucoside; tZROG, tZ O-glucoside riboside; tZ7G, tZ-N-7-glucoside; CKX, cytokinin oxidase. (d) The levels of tZ and related metabolites in the 1-cm-long shoot basal tissues from 1-week-old seedlings of WT (blue and magenta) and rss1-2 seedlings (yellow and light blue) grown in the absence (blue and yellow) or presence of 150 mM NaCl (magenta and light blue) (mean±s.d., n=3). ND(1), the average of two independent samples due to one value being below the detection limit. ND(3), all values were below the detection limit in triplicate samples.
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f6: rss1 affects cytokinin action.(a) The exogenous application of cytokinins alleviated the lethality of rss1 under high-salt conditions. The basal shoot segments without roots (2.5 cm long) were excised from 1-week-old WT and rss1-2 plants, transferred to the medium containing 150 mM NaCl with or without the indicated concentrations of kinetin, and grown for 19 days. Bars, 5 cm. (b) The expression of CKX2 (top) and RR1 (bottom) in the basal shoot tissues of 1-week-old WT and rss1-2 seedlings, as determined by microarray analysis (magenta), or of WT and rss1-1 plants, as determined by quantitative RT-PCR (yellow). Seedlings grown under the normal (−NaCl) and saline (+NaCl) conditions were tested. The expression levels of the tested genes quantified by RT-PCR were normalized with that of ubiquitin E2. Mean±s.d., n=3. Asterisks, a significant difference between WT and rss1-2 under the saline condition. (P=0.002 (by real-time RT-PCR), P=0.001 (by microarray); one-tailed t-test). (c) A schematic illustration of the metabolic pathway of trans-zeatin (tZ) adapted from previous reports3334. tZR, tZ riboside; tZRMP, tZR 5′-monophosphate; tZOG, tZ-O-glucoside; tZROG, tZ O-glucoside riboside; tZ7G, tZ-N-7-glucoside; CKX, cytokinin oxidase. (d) The levels of tZ and related metabolites in the 1-cm-long shoot basal tissues from 1-week-old seedlings of WT (blue and magenta) and rss1-2 seedlings (yellow and light blue) grown in the absence (blue and yellow) or presence of 150 mM NaCl (magenta and light blue) (mean±s.d., n=3). ND(1), the average of two independent samples due to one value being below the detection limit. ND(3), all values were below the detection limit in triplicate samples.

Mentions: Cytokinin is a phytohormone with central roles in cell division323334 and in the maintenance of stem cells in the SAM3536, and it negatively regulates abiotic stress-induced senescence37. Hence, the function of RSS1 in the regulation of the cell cycle under conditions of high salinity and the effects of rss1 on stress-regulated gene expression led us to examine the possible mediation of cytokinins. The exogenous application of cytokinins alleviated the lethality of the rss1 mutation in the shoot under high-salt conditions (Fig. 6a). In the basal region of the shoot, the expression of OsCKX2, which encodes a cytokinin oxidase that inactivates cytokinins38, was upregulated in rss1 (Fig. 6b). Moreover, the levels of an active cytokinin, trans-zeatin (tZ), were increased under high-salt conditions in WT plants, but not in rss1 (Fig. 6c,d), although the level of another cytokinin, N6-(Δ2-isopentenyl) adenine (iP), was decreased in both WT and rss1 plants (Supplementary Fig. S13). The reduced level of tZ in rss1 was accompanied by a decline in the level of its precursor and an increase in the inactive tZ-O-glucoside (tZOG) content (Fig. 6c,d). Decreased cytokinin activity in rss1 was also evident from the downregulation of the cytokinin-inducible response regulator gene, OsRR139 (Fig. 6b). These results suggest that the function of RSS1 is somehow connected to the sustainment of proliferating shoot tissues by maintaining the active cytokinin level in the face of salt stress.


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 affects cytokinin action.(a) The exogenous application of cytokinins alleviated the lethality of rss1 under high-salt conditions. The basal shoot segments without roots (2.5 cm long) were excised from 1-week-old WT and rss1-2 plants, transferred to the medium containing 150 mM NaCl with or without the indicated concentrations of kinetin, and grown for 19 days. Bars, 5 cm. (b) The expression of CKX2 (top) and RR1 (bottom) in the basal shoot tissues of 1-week-old WT and rss1-2 seedlings, as determined by microarray analysis (magenta), or of WT and rss1-1 plants, as determined by quantitative RT-PCR (yellow). Seedlings grown under the normal (−NaCl) and saline (+NaCl) conditions were tested. The expression levels of the tested genes quantified by RT-PCR were normalized with that of ubiquitin E2. Mean±s.d., n=3. Asterisks, a significant difference between WT and rss1-2 under the saline condition. (P=0.002 (by real-time RT-PCR), P=0.001 (by microarray); one-tailed t-test). (c) A schematic illustration of the metabolic pathway of trans-zeatin (tZ) adapted from previous reports3334. tZR, tZ riboside; tZRMP, tZR 5′-monophosphate; tZOG, tZ-O-glucoside; tZROG, tZ O-glucoside riboside; tZ7G, tZ-N-7-glucoside; CKX, cytokinin oxidase. (d) The levels of tZ and related metabolites in the 1-cm-long shoot basal tissues from 1-week-old seedlings of WT (blue and magenta) and rss1-2 seedlings (yellow and light blue) grown in the absence (blue and yellow) or presence of 150 mM NaCl (magenta and light blue) (mean±s.d., n=3). ND(1), the average of two independent samples due to one value being below the detection limit. ND(3), all values were below the detection limit in triplicate samples.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f6: rss1 affects cytokinin action.(a) The exogenous application of cytokinins alleviated the lethality of rss1 under high-salt conditions. The basal shoot segments without roots (2.5 cm long) were excised from 1-week-old WT and rss1-2 plants, transferred to the medium containing 150 mM NaCl with or without the indicated concentrations of kinetin, and grown for 19 days. Bars, 5 cm. (b) The expression of CKX2 (top) and RR1 (bottom) in the basal shoot tissues of 1-week-old WT and rss1-2 seedlings, as determined by microarray analysis (magenta), or of WT and rss1-1 plants, as determined by quantitative RT-PCR (yellow). Seedlings grown under the normal (−NaCl) and saline (+NaCl) conditions were tested. The expression levels of the tested genes quantified by RT-PCR were normalized with that of ubiquitin E2. Mean±s.d., n=3. Asterisks, a significant difference between WT and rss1-2 under the saline condition. (P=0.002 (by real-time RT-PCR), P=0.001 (by microarray); one-tailed t-test). (c) A schematic illustration of the metabolic pathway of trans-zeatin (tZ) adapted from previous reports3334. tZR, tZ riboside; tZRMP, tZR 5′-monophosphate; tZOG, tZ-O-glucoside; tZROG, tZ O-glucoside riboside; tZ7G, tZ-N-7-glucoside; CKX, cytokinin oxidase. (d) The levels of tZ and related metabolites in the 1-cm-long shoot basal tissues from 1-week-old seedlings of WT (blue and magenta) and rss1-2 seedlings (yellow and light blue) grown in the absence (blue and yellow) or presence of 150 mM NaCl (magenta and light blue) (mean±s.d., n=3). ND(1), the average of two independent samples due to one value being below the detection limit. ND(3), all values were below the detection limit in triplicate samples.
Mentions: Cytokinin is a phytohormone with central roles in cell division323334 and in the maintenance of stem cells in the SAM3536, and it negatively regulates abiotic stress-induced senescence37. Hence, the function of RSS1 in the regulation of the cell cycle under conditions of high salinity and the effects of rss1 on stress-regulated gene expression led us to examine the possible mediation of cytokinins. The exogenous application of cytokinins alleviated the lethality of the rss1 mutation in the shoot under high-salt conditions (Fig. 6a). In the basal region of the shoot, the expression of OsCKX2, which encodes a cytokinin oxidase that inactivates cytokinins38, was upregulated in rss1 (Fig. 6b). Moreover, the levels of an active cytokinin, trans-zeatin (tZ), were increased under high-salt conditions in WT plants, but not in rss1 (Fig. 6c,d), although the level of another cytokinin, N6-(Δ2-isopentenyl) adenine (iP), was decreased in both WT and rss1 plants (Supplementary Fig. S13). The reduced level of tZ in rss1 was accompanied by a decline in the level of its precursor and an increase in the inactive tZ-O-glucoside (tZOG) content (Fig. 6c,d). Decreased cytokinin activity in rss1 was also evident from the downregulation of the cytokinin-inducible response regulator gene, OsRR139 (Fig. 6b). These results suggest that the function of RSS1 is somehow connected to the sustainment of proliferating shoot tissues by maintaining the active cytokinin level in the face of salt stress.

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