Disruption of a DNA Topoisomerase I Gene Affects Morphogenesis in Arabidopsis

Takahashi, Taku; Matsuhara, Shio; Abe, Mitsutomo; Komeda, Yoshibumi

doi:10.1105/tpc.001925

Cited by 50 publications

(56 citation statements)

References 47 publications

(56 reference statements)

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“…To generate the TRV:TopoI VIGS line, a 0.6-kb Nicotiana benthamiana cDNA fragment encoding a homolog of Arabidopsis thaliana topoisomerase I (Takahashi et al, 2002) was cloned into the pTV00 vector using BamHI and ApaI sites. The recombinant pTV00 plasmids and the pBINTRA6 vector containing RNA1, which is required for virus replication, were separately transformed into Agrobacterium tumefaciens GV3101.…”

Section: Methods Vigsmentioning

confidence: 99%

“…Protoplasts from the TRV:TopoI line, in which topoisomerase I expression is suppressed by VIGS, and protoplasts from the TRV line served as controls. Topoisomerase I has been predicted to be targeted to the nucleus in Arabidopsis (Takahashi et al, 2002). In both TRV:GyrA and TRV:GyrB, almost all of the protoplasts, most of which originated from leaf mesophyll cells, exhibited drastically reduced chloroplast numbers (;28 and 22% of those in the TRV control, respectively).…”

Section: Numbers Of Chloroplasts and Mitochondriamentioning

confidence: 99%

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DNA Gyrase Is Involved in Chloroplast Nucleoid Partitioning

et al. 2004

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DNA gyrase, which catalyzes topological transformation of DNA, plays an essential role in replication and transcription in prokaryotes. Virus-induced gene silencing of NbGyrA or NbGyrB, which putatively encode DNA gyrase subunits A and B, respectively, resulted in leaf yellowing phenotypes in Nicotiana benthamiana. NbGyrA and NbGyrB complemented the gyrA and gyrB temperature-sensitive mutations of Escherichia coli, respectively, which indicates that the plant and bacterial subunits are functionally similar. NbGyrA and NbGyrB were targeted to both chloroplasts and mitochondria, and depletion of these subunits affected both organelles by reducing chloroplast numbers and inducing morphological and physiological abnormalities in both organelles. Flow cytometry analysis revealed that the average DNA content in the affected chloroplasts and mitochondria was significantly higher than in the control organelles. Furthermore, 49,6-diamidino-2-phenylindole staining revealed that the abnormal chloroplasts contained one or a few large nucleoids instead of multiple small nucleoids dispersed throughout the stroma. Pulse-field gel electrophoresis analyses of chloroplasts demonstrated that the sizes and/ or structure of the DNA molecules in the abnormal chloroplast nucleoids are highly aberrant. Based on these results, we propose that DNA gyrase plays a critical role in chloroplast nucleoid partitioning by regulating DNA topology.

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Section: Methods Vigsmentioning

confidence: 99%

Section: Numbers Of Chloroplasts and Mitochondriamentioning

confidence: 99%

DNA Gyrase Is Involved in Chloroplast Nucleoid Partitioning

et al. 2004

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“…The pattern of organ initiation is also irregular in the serrate (se) mutant where the meristem is enlarged compared with wild type (Clarke et al, 1999;Ori et al, 2000;Prigge and Wagner, 2001). Reduced meristem size is associated with phyllotaxy defects in the DNA topoisomerase mutant top1α (Takahashi et al, 2002). Alternatively, the abphyl1 mutant in maize has a phyllotaxy defect associated with an enlarged meristem.…”

Section: Introductionmentioning

confidence: 99%

Phyllotactic pattern and stem cell fate are determined by theArabidopsishomeobox geneBELLRINGER

Byrne

Groover²,

Fontana³

et al. 2003

Development

193

257

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Lateral organs in plants arise from the meristem in a stereotypical pattern known as phyllotaxy. Spiral patterns result from initiation of successive organs at a fixed angle of divergence but variable patterns of physical contact. Such patterns ultimately give rise to individual leaves and flowers at positions related to each other by consecutive terms in the mathematical series first described by Leonardo Fibonacci. We demonstrate that a BELL1 related homeodomain protein in Arabidopsis, BELLRINGER, maintains the spiral phyllotactic pattern. In the absence of BELLRINGER, the regular pattern of organ initiation is disturbed and lateral organs are initiated more frequently. BELLRINGER is also required for maintenance of stem cell fate in the absence of the regulatory genes SHOOT MERISTEMLESS and ASYMMETRIC LEAVES1. We propose a model whereby BELLRINGER coordinates the maintenance of stem cells with differentiation of daughter cells in stem cell lineages.

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“…However, numerous observations argue against this simple partition of roles and indicate that topo II participates also in DNA relaxation tasks. Although topo I is required during development in higher eukaryotes (Zhang et al, 2000;Takahashi et al, 2002), it is dispensable for cell viability in Saccharomyces cerevisiae and Schizosaccharomyces pombe (Uemura and Yanagida, 1984). In these cells, topo II relaxes DNA supercoils in the absence of topo I (Saavedra and Huberman, 1986;Brill and Sternglanz, 1988;Giaever and Wang, 1988).…”

Section: Introductionmentioning

confidence: 99%

Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA

Salceda¹,

Fernández²,

Roca

2006

EMBO J

101

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Eukaryotic topoisomerases I and II efficiently remove helical tension in naked DNA molecules. However, this activity has not been examined in nucleosomal DNA, their natural substrate. Here, we obtained yeast minichromosomes holding DNA under ( þ ) helical tension, and incubated them with topoisomerases. We show that DNA supercoiling density can rise above þ 0.04 without displacement of the histones and that the typical nucleosome topology is restored upon DNA relaxation. However, in contrast to what is observed in naked DNA, topoisomerase II relaxes nucleosomal DNA much faster than topoisomerase I. The same effect occurs in cell extracts containing physiological dosages of topoisomerase I and II. Apparently, the DNA strand-rotation mechanism of topoisomerase I does not efficiently relax chromatin, which imposes barriers for DNA twist diffusion. Conversely, the DNA cross-inversion mechanism of topoisomerase II is facilitated in chromatin, which favor the juxtaposition of DNA segments. We conclude that topoisomerase II is the main modulator of DNA topology in chromatin fibers. The nonessential topoisomerase I then assists DNA relaxation where chromatin structure impairs DNA juxtaposition but allows twist diffusion.

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Disruption of a DNA Topoisomerase I Gene Affects Morphogenesis in Arabidopsis

Cited by 50 publications

References 47 publications

DNA Gyrase Is Involved in Chloroplast Nucleoid Partitioning

DNA Gyrase Is Involved in Chloroplast Nucleoid Partitioning

Phyllotactic pattern and stem cell fate are determined by theArabidopsishomeobox geneBELLRINGER

Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA

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