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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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AtRaptor1A-/- 1B-/- double mutants. (A) Col, A-, B- and A-B- seedlings at seven days on growth medium with no sucrose. (B) 1A-/- 1B+/- progeny germinated on growth medium supplemented with 0%, 1% or 6% sucrose. Shown for each treatment is an A-B- seedling and an A-/- B+ sibling. A-B- seedlings on 1% sucrose show significant root growth and minimal leaf buds. Scale bar for A, B = 5 mm. (C) Quantification of results in (B). (D) A-B- root tips grown on 1% sucrose lack an epidermal cell layer. (E) A-B- roots form root hairs on 1% sucrose. Scale bar = 100 μm. Compare to 3H, I. (F, G, H, I) Scanning electron microscopy on Col, A-B- shoot apices from growth medium plates. As in (B), A-B- seedlings show minimal (SAM) activity. Primordia for leaves 1 and 2 form but do not expand significantly. Scale bar = 50 μm (F, G) or 15 μm (H, I).
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Figure 7: AtRaptor1A-/- 1B-/- double mutants. (A) Col, A-, B- and A-B- seedlings at seven days on growth medium with no sucrose. (B) 1A-/- 1B+/- progeny germinated on growth medium supplemented with 0%, 1% or 6% sucrose. Shown for each treatment is an A-B- seedling and an A-/- B+ sibling. A-B- seedlings on 1% sucrose show significant root growth and minimal leaf buds. Scale bar for A, B = 5 mm. (C) Quantification of results in (B). (D) A-B- root tips grown on 1% sucrose lack an epidermal cell layer. (E) A-B- roots form root hairs on 1% sucrose. Scale bar = 100 μm. Compare to 3H, I. (F, G, H, I) Scanning electron microscopy on Col, A-B- shoot apices from growth medium plates. As in (B), A-B- seedlings show minimal (SAM) activity. Primordia for leaves 1 and 2 form but do not expand significantly. Scale bar = 50 μm (F, G) or 15 μm (H, I).

Mentions: The high degree of similarity between AtRaptor1A and AtRaptor1B led us to suspect that they may be at least partially functionally redundant. To eliminate all AtRaptor activity in a single line, 1A-/- and 1B-/- lines were crossed. No 1A-/- 1B-/- plants could be identified among the F2 of this cross on soil. Phenotypically wild-type 1A-/- 1B+/- plants were identified via PCR using the primer pairs described in Materials and Methods and their progeny (205 seedlings) were examined on agar plates. Of these, 165 seedlings (80%) appeared wild type (Fig. 7A). It was determined by PCR that these seedlings carried a wild-type 1B allele (32/32 tested). The remaining seedlings (40/205; 20%) germinated but showed minimal postembryonic shoot meristem growth (Fig. 7A). It was determined by PCR that these seedlings were genetically 1A-/- 1B-/- (32/32 tested). This genotyping confirmed that the seedling arrest mutant phenotype co-segregated with homozygosity for the AtRaptor1B mutant allele in the AtRaptor1A mutant background. We concluded that this seedling phenotype corresponded to the 1A-/- 1B-/- double mutant.


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

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

AtRaptor1A-/- 1B-/- double mutants. (A) Col, A-, B- and A-B- seedlings at seven days on growth medium with no sucrose. (B) 1A-/- 1B+/- progeny germinated on growth medium supplemented with 0%, 1% or 6% sucrose. Shown for each treatment is an A-B- seedling and an A-/- B+ sibling. A-B- seedlings on 1% sucrose show significant root growth and minimal leaf buds. Scale bar for A, B = 5 mm. (C) Quantification of results in (B). (D) A-B- root tips grown on 1% sucrose lack an epidermal cell layer. (E) A-B- roots form root hairs on 1% sucrose. Scale bar = 100 μm. Compare to 3H, I. (F, G, H, I) Scanning electron microscopy on Col, A-B- shoot apices from growth medium plates. As in (B), A-B- seedlings show minimal (SAM) activity. Primordia for leaves 1 and 2 form but do not expand significantly. Scale bar = 50 μm (F, G) or 15 μm (H, I).
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Figure 7: AtRaptor1A-/- 1B-/- double mutants. (A) Col, A-, B- and A-B- seedlings at seven days on growth medium with no sucrose. (B) 1A-/- 1B+/- progeny germinated on growth medium supplemented with 0%, 1% or 6% sucrose. Shown for each treatment is an A-B- seedling and an A-/- B+ sibling. A-B- seedlings on 1% sucrose show significant root growth and minimal leaf buds. Scale bar for A, B = 5 mm. (C) Quantification of results in (B). (D) A-B- root tips grown on 1% sucrose lack an epidermal cell layer. (E) A-B- roots form root hairs on 1% sucrose. Scale bar = 100 μm. Compare to 3H, I. (F, G, H, I) Scanning electron microscopy on Col, A-B- shoot apices from growth medium plates. As in (B), A-B- seedlings show minimal (SAM) activity. Primordia for leaves 1 and 2 form but do not expand significantly. Scale bar = 50 μm (F, G) or 15 μm (H, I).
Mentions: The high degree of similarity between AtRaptor1A and AtRaptor1B led us to suspect that they may be at least partially functionally redundant. To eliminate all AtRaptor activity in a single line, 1A-/- and 1B-/- lines were crossed. No 1A-/- 1B-/- plants could be identified among the F2 of this cross on soil. Phenotypically wild-type 1A-/- 1B+/- plants were identified via PCR using the primer pairs described in Materials and Methods and their progeny (205 seedlings) were examined on agar plates. Of these, 165 seedlings (80%) appeared wild type (Fig. 7A). It was determined by PCR that these seedlings carried a wild-type 1B allele (32/32 tested). The remaining seedlings (40/205; 20%) germinated but showed minimal postembryonic shoot meristem growth (Fig. 7A). It was determined by PCR that these seedlings were genetically 1A-/- 1B-/- (32/32 tested). This genotyping confirmed that the seedling arrest mutant phenotype co-segregated with homozygosity for the AtRaptor1B mutant allele in the AtRaptor1A mutant background. We concluded that this seedling phenotype corresponded to the 1A-/- 1B-/- double mutant.

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