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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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A possible model of the stress tolerance mechanism conferred by RSS1.RSS1 ensures cell cycle progression, and thereby contributes to the maintenance of meristematic cells under undesirable environmental conditions. RSS1 stability is controlled by the APC/C-26S proteasome pathway, leading to RSS1 accumulation from G1/S to M phase. RSS1 functions primarily at the G1–S transition, possibly through the regulation of protein phosphatase 1 (PP1), which antagonizes the cyclin-dependent protein kinase (CDK) activity. The phosphorylation states of the substrate X are the determinants of G1–S transition (and subsequent cell cycle progression). Under stressful conditions, the G1/S checkpoint is conducted by cyclin-dependent kinase inhibitor (CKI) to inhibit the CDK activity that leads to a restrained transition to S phase, whereas RSS1 sustains cell cycle progression to balance cell division with cell differentiation. Defects in the cell cycle progression in rss1 plants affect, at least, the maintenance of proliferative tissues in the roots and the number of dividing cells and the organization of the shoot apical meristems. The latter interferes with cytokinin metabolism, which in turn influences cell division control and anti-senescence activity. Taken together, the role of RSS1 is essential for growth and viability under stressful conditions.
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f8: A possible model of the stress tolerance mechanism conferred by RSS1.RSS1 ensures cell cycle progression, and thereby contributes to the maintenance of meristematic cells under undesirable environmental conditions. RSS1 stability is controlled by the APC/C-26S proteasome pathway, leading to RSS1 accumulation from G1/S to M phase. RSS1 functions primarily at the G1–S transition, possibly through the regulation of protein phosphatase 1 (PP1), which antagonizes the cyclin-dependent protein kinase (CDK) activity. The phosphorylation states of the substrate X are the determinants of G1–S transition (and subsequent cell cycle progression). Under stressful conditions, the G1/S checkpoint is conducted by cyclin-dependent kinase inhibitor (CKI) to inhibit the CDK activity that leads to a restrained transition to S phase, whereas RSS1 sustains cell cycle progression to balance cell division with cell differentiation. Defects in the cell cycle progression in rss1 plants affect, at least, the maintenance of proliferative tissues in the roots and the number of dividing cells and the organization of the shoot apical meristems. The latter interferes with cytokinin metabolism, which in turn influences cell division control and anti-senescence activity. Taken together, the role of RSS1 is essential for growth and viability under stressful conditions.

Mentions: In this study, we demonstrated that RSS1 functions in the regulation of the cell cycle and is required for the maintenance of meristems in both the shoot and root under stressful environmental conditions. We propose that RSS1 functions to antagonize the G1–S checkpoint of the cell in response to stress, such that the cell cycle is slowed through the activity of cyclin-dependent kinase inhibitors2678 (Fig. 8). This function is probably required to balance cell division and differentiation under undesirable growth conditions. In rice, cell differentiation is presumably not arrested immediately upon exposure to stress. In such a situation, the population of meristematic cells would be depleted unless cell division was maintained. Supporting this idea, the size and cell number of the MZ in rss1 roots were decreased under high-salt conditions, eventually leading to the loss of the MZ.


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)

A possible model of the stress tolerance mechanism conferred by RSS1.RSS1 ensures cell cycle progression, and thereby contributes to the maintenance of meristematic cells under undesirable environmental conditions. RSS1 stability is controlled by the APC/C-26S proteasome pathway, leading to RSS1 accumulation from G1/S to M phase. RSS1 functions primarily at the G1–S transition, possibly through the regulation of protein phosphatase 1 (PP1), which antagonizes the cyclin-dependent protein kinase (CDK) activity. The phosphorylation states of the substrate X are the determinants of G1–S transition (and subsequent cell cycle progression). Under stressful conditions, the G1/S checkpoint is conducted by cyclin-dependent kinase inhibitor (CKI) to inhibit the CDK activity that leads to a restrained transition to S phase, whereas RSS1 sustains cell cycle progression to balance cell division with cell differentiation. Defects in the cell cycle progression in rss1 plants affect, at least, the maintenance of proliferative tissues in the roots and the number of dividing cells and the organization of the shoot apical meristems. The latter interferes with cytokinin metabolism, which in turn influences cell division control and anti-senescence activity. Taken together, the role of RSS1 is essential for growth and viability under stressful conditions.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f8: A possible model of the stress tolerance mechanism conferred by RSS1.RSS1 ensures cell cycle progression, and thereby contributes to the maintenance of meristematic cells under undesirable environmental conditions. RSS1 stability is controlled by the APC/C-26S proteasome pathway, leading to RSS1 accumulation from G1/S to M phase. RSS1 functions primarily at the G1–S transition, possibly through the regulation of protein phosphatase 1 (PP1), which antagonizes the cyclin-dependent protein kinase (CDK) activity. The phosphorylation states of the substrate X are the determinants of G1–S transition (and subsequent cell cycle progression). Under stressful conditions, the G1/S checkpoint is conducted by cyclin-dependent kinase inhibitor (CKI) to inhibit the CDK activity that leads to a restrained transition to S phase, whereas RSS1 sustains cell cycle progression to balance cell division with cell differentiation. Defects in the cell cycle progression in rss1 plants affect, at least, the maintenance of proliferative tissues in the roots and the number of dividing cells and the organization of the shoot apical meristems. The latter interferes with cytokinin metabolism, which in turn influences cell division control and anti-senescence activity. Taken together, the role of RSS1 is essential for growth and viability under stressful conditions.
Mentions: In this study, we demonstrated that RSS1 functions in the regulation of the cell cycle and is required for the maintenance of meristems in both the shoot and root under stressful environmental conditions. We propose that RSS1 functions to antagonize the G1–S checkpoint of the cell in response to stress, such that the cell cycle is slowed through the activity of cyclin-dependent kinase inhibitors2678 (Fig. 8). This function is probably required to balance cell division and differentiation under undesirable growth conditions. In rice, cell differentiation is presumably not arrested immediately upon exposure to stress. In such a situation, the population of meristematic cells would be depleted unless cell division was maintained. Supporting this idea, the size and cell number of the MZ in rss1 roots were decreased under high-salt conditions, eventually leading to the loss of the MZ.

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