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The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth.

Anderson GH, Veit B, Hanson MR - BMC Biol. (2005)

Bottom Line: AtRaptor transcripts accumulate in dividing and expanding cells and tissues.The data implicate the TOR signaling pathway, a major regulator of cell growth in yeast and metazoans, in the maintenance of growth from the shoot apical meristem in plants.These results provide insights into the ways in which TOR/Raptor signaling has been adapted to regulate plant growth and development, and indicate that in plants, as in other eukaryotes, there is some Raptor-independent TOR activity.

View Article: PubMed Central - HTML - PubMed

Affiliation: Molecular Biology and Genetics, Cornell University, Ithaca, 14853, USA. ganderson@salk.edu

ABSTRACT

Background: Flowering plant development is wholly reliant on growth from meristems, which contain totipotent cells that give rise to all post-embryonic organs in the plant. Plants are uniquely able to alter their development throughout their lifespan through the generation of new organs in response to external signals. To identify genes that regulate meristem-based growth, we considered homologues of Raptor proteins, which regulate cell growth in response to nutrients in yeast and metazoans as part of a signaling complex with the target of rapamycin (TOR) kinase.

Results: We identified AtRaptor1A and AtRaptor1B, two loci predicted to encode Raptor proteins in Arabidopsis. Disruption of AtRaptor1B yields plants with a wide range of developmental defects: roots are thick and grow slowly, leaf initiation and bolting are delayed and the shoot inflorescence shows reduced apical dominance. AtRaptor1A AtRaptor1B double mutants show normal embryonic development but are unable to maintain post-embryonic meristem-driven growth. AtRaptor transcripts accumulate in dividing and expanding cells and tissues.

Conclusion: The data implicate the TOR signaling pathway, a major regulator of cell growth in yeast and metazoans, in the maintenance of growth from the shoot apical meristem in plants. These results provide insights into the ways in which TOR/Raptor signaling has been adapted to regulate plant growth and development, and indicate that in plants, as in other eukaryotes, there is some Raptor-independent TOR activity.

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TOR functions in two complexes in eukaryotes. (A) TOR participates in two complexes in yeast and mammals. The first of these, TORC1, regulates cell growth in response to nutrient and hormonal signals. Raptor is integral for TORC1 activity. The second of these, TORC2, regulates cytoskeletal organization. Its activity is nutrient-independent, and Raptor is not a component of TORC2. (B) Model of TOR function in plants. Embryonic development is indicated by the single horizontal arrow from zygote to seedling; meristem-driven post-embryonic development is indicated by the arrows emanating from the seedling root and shoot apices. TOR, acting independent of Raptor in a putative complex homologous to yeast and mammalian TORC2, is essential for embryonic development. TOR via TORC2 may play a role in post-embryonic development as well; the embryonic lethal AtTOR knockout phenotype precludes a definitive answer on this point. Raptor activity, in a putative plant homologue of TORC1, is dispensable for embryonic development but is essential for meristem-driven post-embryonic growth.
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Figure 8: TOR functions in two complexes in eukaryotes. (A) TOR participates in two complexes in yeast and mammals. The first of these, TORC1, regulates cell growth in response to nutrient and hormonal signals. Raptor is integral for TORC1 activity. The second of these, TORC2, regulates cytoskeletal organization. Its activity is nutrient-independent, and Raptor is not a component of TORC2. (B) Model of TOR function in plants. Embryonic development is indicated by the single horizontal arrow from zygote to seedling; meristem-driven post-embryonic development is indicated by the arrows emanating from the seedling root and shoot apices. TOR, acting independent of Raptor in a putative complex homologous to yeast and mammalian TORC2, is essential for embryonic development. TOR via TORC2 may play a role in post-embryonic development as well; the embryonic lethal AtTOR knockout phenotype precludes a definitive answer on this point. Raptor activity, in a putative plant homologue of TORC1, is dispensable for embryonic development but is essential for meristem-driven post-embryonic growth.

Mentions: In both yeast and mammalian cells, TOR functions in two distinct complexes (Fig. 8A). The first of these, TORC1, involves Raptor and regulates cell growth and translation in response to nutrients [14-17]. The second of these complexes, TORC2, regulates cytoskeletal organization and does not involve Raptor [13,17,20].


The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth.

Anderson GH, Veit B, Hanson MR - BMC Biol. (2005)

TOR functions in two complexes in eukaryotes. (A) TOR participates in two complexes in yeast and mammals. The first of these, TORC1, regulates cell growth in response to nutrient and hormonal signals. Raptor is integral for TORC1 activity. The second of these, TORC2, regulates cytoskeletal organization. Its activity is nutrient-independent, and Raptor is not a component of TORC2. (B) Model of TOR function in plants. Embryonic development is indicated by the single horizontal arrow from zygote to seedling; meristem-driven post-embryonic development is indicated by the arrows emanating from the seedling root and shoot apices. TOR, acting independent of Raptor in a putative complex homologous to yeast and mammalian TORC2, is essential for embryonic development. TOR via TORC2 may play a role in post-embryonic development as well; the embryonic lethal AtTOR knockout phenotype precludes a definitive answer on this point. Raptor activity, in a putative plant homologue of TORC1, is dispensable for embryonic development but is essential for meristem-driven post-embryonic growth.
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Related In: Results  -  Collection

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Figure 8: TOR functions in two complexes in eukaryotes. (A) TOR participates in two complexes in yeast and mammals. The first of these, TORC1, regulates cell growth in response to nutrient and hormonal signals. Raptor is integral for TORC1 activity. The second of these, TORC2, regulates cytoskeletal organization. Its activity is nutrient-independent, and Raptor is not a component of TORC2. (B) Model of TOR function in plants. Embryonic development is indicated by the single horizontal arrow from zygote to seedling; meristem-driven post-embryonic development is indicated by the arrows emanating from the seedling root and shoot apices. TOR, acting independent of Raptor in a putative complex homologous to yeast and mammalian TORC2, is essential for embryonic development. TOR via TORC2 may play a role in post-embryonic development as well; the embryonic lethal AtTOR knockout phenotype precludes a definitive answer on this point. Raptor activity, in a putative plant homologue of TORC1, is dispensable for embryonic development but is essential for meristem-driven post-embryonic growth.
Mentions: In both yeast and mammalian cells, TOR functions in two distinct complexes (Fig. 8A). The first of these, TORC1, involves Raptor and regulates cell growth and translation in response to nutrients [14-17]. The second of these complexes, TORC2, regulates cytoskeletal organization and does not involve Raptor [13,17,20].

Bottom Line: AtRaptor transcripts accumulate in dividing and expanding cells and tissues.The data implicate the TOR signaling pathway, a major regulator of cell growth in yeast and metazoans, in the maintenance of growth from the shoot apical meristem in plants.These results provide insights into the ways in which TOR/Raptor signaling has been adapted to regulate plant growth and development, and indicate that in plants, as in other eukaryotes, there is some Raptor-independent TOR activity.

View Article: PubMed Central - HTML - PubMed

Affiliation: Molecular Biology and Genetics, Cornell University, Ithaca, 14853, USA. ganderson@salk.edu

ABSTRACT

Background: Flowering plant development is wholly reliant on growth from meristems, which contain totipotent cells that give rise to all post-embryonic organs in the plant. Plants are uniquely able to alter their development throughout their lifespan through the generation of new organs in response to external signals. To identify genes that regulate meristem-based growth, we considered homologues of Raptor proteins, which regulate cell growth in response to nutrients in yeast and metazoans as part of a signaling complex with the target of rapamycin (TOR) kinase.

Results: We identified AtRaptor1A and AtRaptor1B, two loci predicted to encode Raptor proteins in Arabidopsis. Disruption of AtRaptor1B yields plants with a wide range of developmental defects: roots are thick and grow slowly, leaf initiation and bolting are delayed and the shoot inflorescence shows reduced apical dominance. AtRaptor1A AtRaptor1B double mutants show normal embryonic development but are unable to maintain post-embryonic meristem-driven growth. AtRaptor transcripts accumulate in dividing and expanding cells and tissues.

Conclusion: The data implicate the TOR signaling pathway, a major regulator of cell growth in yeast and metazoans, in the maintenance of growth from the shoot apical meristem in plants. These results provide insights into the ways in which TOR/Raptor signaling has been adapted to regulate plant growth and development, and indicate that in plants, as in other eukaryotes, there is some Raptor-independent TOR activity.

Show MeSH
Related in: MedlinePlus