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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 expressed preferentially in dividing cells.(a) The expression of RSS1 in seedlings and calli. Two-week-old seedlings of rice were dissected into the three parts as in the left panel and used for northern blot analysis with an RSS1-specific probe (right). The basal region of the shoot contains the shoot apical meristem (SAM) and leaf primordia (LP). rRNA, loading control. (b) GFP signals detected in the root of transgenic rice carrying GFP driven by the RSS1 promoter. Dark-field GFP images (top) and bright-field images (middle) are merged in the panels on the bottom. (left panels) The MTZ of the root with an emerging lateral root primordium (LRP). (right panels) The apex of an adventitious root. Bars, 200 μm. (c) In situ localization of RSS1 mRNA in the shoot. Longitudinal sections were hybridized with anti-sense and sense DIG-labelled RNA probes specific for RSS1, respectively. LM, lateral meristem. Insets Increased magnification of the SAM region. Bars, 100 μm. (d) Expression of RSS1 during the cell cycle. The synchronized rice Oc cells were harvested at the indicated cell cycle phases and analysed by northern blotting using histone H4- or RSS1-specific probes. rRNA, loading control.
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f3: RSS1 is expressed preferentially in dividing cells.(a) The expression of RSS1 in seedlings and calli. Two-week-old seedlings of rice were dissected into the three parts as in the left panel and used for northern blot analysis with an RSS1-specific probe (right). The basal region of the shoot contains the shoot apical meristem (SAM) and leaf primordia (LP). rRNA, loading control. (b) GFP signals detected in the root of transgenic rice carrying GFP driven by the RSS1 promoter. Dark-field GFP images (top) and bright-field images (middle) are merged in the panels on the bottom. (left panels) The MTZ of the root with an emerging lateral root primordium (LRP). (right panels) The apex of an adventitious root. Bars, 200 μm. (c) In situ localization of RSS1 mRNA in the shoot. Longitudinal sections were hybridized with anti-sense and sense DIG-labelled RNA probes specific for RSS1, respectively. LM, lateral meristem. Insets Increased magnification of the SAM region. Bars, 100 μm. (d) Expression of RSS1 during the cell cycle. The synchronized rice Oc cells were harvested at the indicated cell cycle phases and analysed by northern blotting using histone H4- or RSS1-specific probes. rRNA, loading control.

Mentions: RSS1 mRNA is expressed abundantly in proliferating tissue, such as the basal region of the shoot, which contains apical and lateral shoot meristems and leaf primordia, and, to a lesser extent, in the upper region of the shoot (Fig. 3a). RSS1 expression was upregulated by low temperatures, but not by high-salt conditions (Supplementary Fig. S10). In the root, RSS1 promoter activity was detected predominantly in the MZ or lateral root primordia (Fig. 3b). At the reproductive stages, RSS1 was expressed preferentially in immature inflorescences, as compared with mature florets or leaves (Supplementary Fig. S10). In situ hybridization analysis revealed patchy signals for RSS1 mRNA in the leaf primordia and in the meristems of the shoot and root apices, which are the major sites of cell cycling (Fig. 3c and Supplementary Figs. S10 and S11). In the shoot apical meristem (SAM), RSS1 mRNA was detected only weakly in the central zone, where the cells are less active in terms of division and are completely undifferentiated. This is in sharp contrast to the expression pattern of OSH1, a homeobox gene orthologous to Arabidopsis STM, which is expressed in indeterminate cells, but not in leaf primordia, and is suggested to function in the maintenance of undifferentiated states24. The spatial expression pattern of RSS1 is reminiscent of those of genes encoding histones, cyclins or CDKs242526. The expression of these cell cycle-related genes is often associated with specific phases of the cell cycle. RSS1 was expressed most abundantly during the G1 and S phases (Fig. 3d and Supplementary Fig. S10), similar to cyclin D27. These results, together with the finding of cell cycle phase-dependent proteolysis, suggest that RSS1 functions in cell division.


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 expressed preferentially in dividing cells.(a) The expression of RSS1 in seedlings and calli. Two-week-old seedlings of rice were dissected into the three parts as in the left panel and used for northern blot analysis with an RSS1-specific probe (right). The basal region of the shoot contains the shoot apical meristem (SAM) and leaf primordia (LP). rRNA, loading control. (b) GFP signals detected in the root of transgenic rice carrying GFP driven by the RSS1 promoter. Dark-field GFP images (top) and bright-field images (middle) are merged in the panels on the bottom. (left panels) The MTZ of the root with an emerging lateral root primordium (LRP). (right panels) The apex of an adventitious root. Bars, 200 μm. (c) In situ localization of RSS1 mRNA in the shoot. Longitudinal sections were hybridized with anti-sense and sense DIG-labelled RNA probes specific for RSS1, respectively. LM, lateral meristem. Insets Increased magnification of the SAM region. Bars, 100 μm. (d) Expression of RSS1 during the cell cycle. The synchronized rice Oc cells were harvested at the indicated cell cycle phases and analysed by northern blotting using histone H4- or RSS1-specific probes. rRNA, loading control.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f3: RSS1 is expressed preferentially in dividing cells.(a) The expression of RSS1 in seedlings and calli. Two-week-old seedlings of rice were dissected into the three parts as in the left panel and used for northern blot analysis with an RSS1-specific probe (right). The basal region of the shoot contains the shoot apical meristem (SAM) and leaf primordia (LP). rRNA, loading control. (b) GFP signals detected in the root of transgenic rice carrying GFP driven by the RSS1 promoter. Dark-field GFP images (top) and bright-field images (middle) are merged in the panels on the bottom. (left panels) The MTZ of the root with an emerging lateral root primordium (LRP). (right panels) The apex of an adventitious root. Bars, 200 μm. (c) In situ localization of RSS1 mRNA in the shoot. Longitudinal sections were hybridized with anti-sense and sense DIG-labelled RNA probes specific for RSS1, respectively. LM, lateral meristem. Insets Increased magnification of the SAM region. Bars, 100 μm. (d) Expression of RSS1 during the cell cycle. The synchronized rice Oc cells were harvested at the indicated cell cycle phases and analysed by northern blotting using histone H4- or RSS1-specific probes. rRNA, loading control.
Mentions: RSS1 mRNA is expressed abundantly in proliferating tissue, such as the basal region of the shoot, which contains apical and lateral shoot meristems and leaf primordia, and, to a lesser extent, in the upper region of the shoot (Fig. 3a). RSS1 expression was upregulated by low temperatures, but not by high-salt conditions (Supplementary Fig. S10). In the root, RSS1 promoter activity was detected predominantly in the MZ or lateral root primordia (Fig. 3b). At the reproductive stages, RSS1 was expressed preferentially in immature inflorescences, as compared with mature florets or leaves (Supplementary Fig. S10). In situ hybridization analysis revealed patchy signals for RSS1 mRNA in the leaf primordia and in the meristems of the shoot and root apices, which are the major sites of cell cycling (Fig. 3c and Supplementary Figs. S10 and S11). In the shoot apical meristem (SAM), RSS1 mRNA was detected only weakly in the central zone, where the cells are less active in terms of division and are completely undifferentiated. This is in sharp contrast to the expression pattern of OSH1, a homeobox gene orthologous to Arabidopsis STM, which is expressed in indeterminate cells, but not in leaf primordia, and is suggested to function in the maintenance of undifferentiated states24. The spatial expression pattern of RSS1 is reminiscent of those of genes encoding histones, cyclins or CDKs242526. The expression of these cell cycle-related genes is often associated with specific phases of the cell cycle. RSS1 was expressed most abundantly during the G1 and S phases (Fig. 3d and Supplementary Fig. S10), similar to cyclin D27. These results, together with the finding of cell cycle phase-dependent proteolysis, suggest that RSS1 functions in cell division.

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