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Physiological and transcriptomic evidence for a close coupling between chloroplast ontogeny and cell cycle progression in the pennate diatom Seminavis robusta

Jeroen Gillard, Valerie Devos (UGent) , Marie Huysman (UGent) , Lieven De Veylder (UGent) , Sofie D'hondt (UGent) , Cindy Martens (UGent) , Pieter Vanormelingen (UGent) , Katrijn Vannerum (UGent) , Koen Sabbe (UGent) , Victor A Chepurnov, et al.
(2008) PLANT PHYSIOLOGY. 148(3). p.1394-1411
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Abstract
Despite the growing interest in diatom genomics, detailed time series of gene expression in relation to key cellular processes are still lacking. Here, we investigated the relationships between the cell cycle and chloroplast development in the pennate diatom Seminavis robusta. This diatom possesses two chloroplasts with a well-orchestrated developmental cycle, common to many pennate diatoms. By assessing the effects of induced cell cycle arrest with microscopy and flow cytometry, we found that division and reorganization of the chloroplasts are initiated only after S-phase progression. Next, we quantified the expression of the S. robusta FtsZ homolog to address the division status of chloroplasts during synchronized growth and monitored microscopically their dynamics in relation to nuclear division and silicon deposition. We show that chloroplasts divide and relocate during the S/G2 phase, after which a girdle band is deposited to accommodate cell growth. Synchronized cultures of two genotypes were subsequently used for a cDNA-amplified fragment length polymorphism-based genome-wide transcript profiling, in which 917 reproducibly modulated transcripts were identified. We observed that genes involved in pigment biosynthesis and coding for light-harvesting proteins were up-regulated during G2/M phase and cell separation. Light and cell cycle progression were both found to affect fucoxanthin-chlorophyll a/c-binding protein expression and accumulation of fucoxanthin cell content. Because chloroplasts elongate at the stage of cytokinesis, cell cycle-modulated photosynthetic gene expression and synthesis of pigments in concert with cell division might balance chloroplast growth, which confirms that chloroplast biogenesis in S. robusta is tightly regulated.
Keywords
SCENEDESMUS-QUADRICAUDA, PHAEODACTYLUM-TRICORNUTUM, CYCLOTELLA-CRYPTICA, THALASSIOSIRA-PSEUDONANA, MANGANESE SUPEROXIDE-DISMUTASE, CYLINDROTHECA-FUSIFORMIS, ALGA CYANIDIOSCHYZON MEROLAE, SILICA SHELL FORMATION, MARINE DIATOMS, FINE-STRUCTURE

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Chicago
Gillard, Jeroen, Valerie Devos, Marie Huysman, Lieven De Veylder, Sofie D’hondt, Cindy Martens, Pieter Vanormelingen, et al. 2008. “Physiological and Transcriptomic Evidence for a Close Coupling Between Chloroplast Ontogeny and Cell Cycle Progression in the Pennate Diatom Seminavis Robusta.” Plant Physiology 148 (3): 1394–1411.
APA
Gillard, J., Devos, V., Huysman, M., De Veylder, L., D’hondt, S., Martens, C., Vanormelingen, P., et al. (2008). Physiological and transcriptomic evidence for a close coupling between chloroplast ontogeny and cell cycle progression in the pennate diatom Seminavis robusta. PLANT PHYSIOLOGY, 148(3), 1394–1411.
Vancouver
1.
Gillard J, Devos V, Huysman M, De Veylder L, D’hondt S, Martens C, et al. Physiological and transcriptomic evidence for a close coupling between chloroplast ontogeny and cell cycle progression in the pennate diatom Seminavis robusta. PLANT PHYSIOLOGY. 2008;148(3):1394–411.
MLA
Gillard, Jeroen, Valerie Devos, Marie Huysman, et al. “Physiological and Transcriptomic Evidence for a Close Coupling Between Chloroplast Ontogeny and Cell Cycle Progression in the Pennate Diatom Seminavis Robusta.” PLANT PHYSIOLOGY 148.3 (2008): 1394–1411. Print.
@article{509728,
  abstract     = {Despite the growing interest in diatom genomics, detailed time series of gene expression in relation to key cellular processes are still lacking. Here, we investigated the relationships between the cell cycle and chloroplast development in the pennate diatom Seminavis robusta. This diatom possesses two chloroplasts with a well-orchestrated developmental cycle, common to many pennate diatoms. By assessing the effects of induced cell cycle arrest with microscopy and flow cytometry, we found that division and reorganization of the chloroplasts are initiated only after S-phase progression. Next, we quantified the expression of the S. robusta FtsZ homolog to address the division status of chloroplasts during synchronized growth and monitored microscopically their dynamics in relation to nuclear division and silicon deposition. We show that chloroplasts divide and relocate during the S/G2 phase, after which a girdle band is deposited to accommodate cell growth. Synchronized cultures of two genotypes were subsequently used for a cDNA-amplified fragment length polymorphism-based genome-wide transcript profiling, in which 917 reproducibly modulated transcripts were identified. We observed that genes involved in pigment biosynthesis and coding for light-harvesting proteins were up-regulated during G2/M phase and cell separation. Light and cell cycle progression were both found to affect fucoxanthin-chlorophyll a/c-binding protein expression and accumulation of fucoxanthin cell content. Because chloroplasts elongate at the stage of cytokinesis, cell cycle-modulated photosynthetic gene expression and synthesis of pigments in concert with cell division might balance chloroplast growth, which confirms that chloroplast biogenesis in S. robusta is tightly regulated.},
  author       = {Gillard, Jeroen and Devos, Valerie and Huysman, Marie and De Veylder, Lieven and D'hondt, Sofie and Martens, Cindy and Vanormelingen, Pieter and Vannerum, Katrijn and Sabbe, Koen and Chepurnov, Victor A and Inz{\'e}, Dirk and Vuylsteke, Marnik and Vyverman, Wim},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  language     = {eng},
  number       = {3},
  pages        = {1394--1411},
  title        = {Physiological and transcriptomic evidence for a close coupling between chloroplast ontogeny and cell cycle progression in the pennate diatom Seminavis robusta},
  url          = {http://dx.doi.org/10.1104/pp.108.122176},
  volume       = {148},
  year         = {2008},
}

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