From the nematode and mammals back to the pine tree: on the diversity and evolution of programmed cell death

Zhivotovsky, Boris

doi:10.1038/sj.cdd.4401084

Cited by 21 publications

(9 citation statements)

References 23 publications

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“…There is growing evidence of the autophagic nature of PCD in plants, where ''cell-dismantling'' and ''corpse-clearance'' tasks are fulfilled simultaneously by growing vacuoles (1,2,(26)(27)(28). Although the elimination of the embryo suspensor is a typical example of autophagic PCD (2), we have previously reported that nuclear degradation does not correlate morphologically with the progression of autophagic dismantling of the cytoplasm in the suspensor (19).…”

Section: Discussionmentioning

confidence: 99%

Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis

Bozhkov

Suárez

Filonova

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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224

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Programmed cell death (PCD) is indispensable for eukaryotic development. In animals, PCD is executed by the caspase family of cysteine proteases. Plants do not have close homologues of caspases but possess a phylogenetically distant family of cysteine proteases named metacaspases. The cellular function of metacaspases in PCD is unknown. Here we show that during plant embryogenesis, metacaspase mcII-Pa translocates from the cytoplasm to nuclei in terminally differentiated cells that are destined for elimination, where it colocalizes with the nuclear pore complex and chromatin, causing nuclear envelope disassembly and DNA fragmentation. The cell-death function of mcII-Pa relies on its cysteine-dependent arginine-specific proteolytic activity. Accordingly, mutation of catalytic cysteine abrogates the proteolytic activity of mcII-Pa and blocks nuclear degradation. These results establish metacaspase as an executioner of PCD during embryo patterning and provide a functional link between PCD and embryogenesis in plants. Although mcII-Pa and metazoan caspases have different substrate specificity, they serve a common function during development, demonstrating the evolutionary parallelism of PCD pathways in plants and animals.embryo suspensor ͉ metacaspase ͉ nuclear degradation P rogrammed cell death (PCD) is indispensable for normal embryo development both in animals and in plants, where temporary, surplus, or aberrantly formed tissues and organs are removed for correct pattern formation (1, 2). The key morphogenetic event in plant embryogenesis is formation of the apicalbasal pattern via establishment of the proliferating embryo proper (apical) and the terminally differentiated suspensor (basal). Developmental programs of the embryo proper and the suspensor are closely coordinated, and imbalance causes embryonic defects or lethality (2-4). While the embryo proper gives rise to the plant, the suspensor functions during a brief period as a conduit of growth factors to the developing embryo and is subsequently eliminated by PCD (2). The terminal differentiation of the embryo suspensor is the earliest manifestation of cellular suicide in plant ontogenesis. However, the molecular mechanisms that regulate PCD in plant embryos are unknown.The nucleus is the major target of cell degradation machinery during PCD. Nuclear degradation processes encompass chromatin events (i.e., chromatin condensation and DNA fragmentation) and nuclear envelope events (i.e., lobing of the nuclear surface and disassembly of nuclear pore complex) that occur simultaneously in the same cell (2, 5). The structural organization of plant and animal nuclei is conserved (6), explaining why the morphological pattern of nuclear degradation is also conserved (2). However, the molecular composition of plant and animal nuclear envelopes is not conserved (6), implying that different molecular mechanisms are responsible for nuclear envelope events during PCD in plants.In animals, nuclear degradation during PCD is executed by a caspase family of cysteine proteases...

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Section: Discussionmentioning

confidence: 99%

Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis

Bozhkov

Suárez

Filonova

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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224

235

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“…62,63 Morphologically different cell death processes have proven to be an integral part of pine embryogenesis, 2,7,10 and the pine seed has been suggested as a model for studying the origin and evolution of eukaryotic PCD machinery. 64 Furthermore, the unique reproductive features of gymnosperms together with the occurrence of cell death in various tissues which differ from each other either in the number or parental origin of the genomes make the pine seed special compared with many other PCD model systems. Thus, the pine seed provides a unique window for studies on the genetic control of developmentally regulated cell death processes in plants.…”

Section: Discussionmentioning

confidence: 99%

Pine embryogenesis

Vuosku

Sutela

Tillman-Sutela³

et al. 2009

Plant Signaling & Behavior

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“…Being a bona fide route of physiological cell death in plants, autophagic PCD is an evolutionarily ancient and phylogenetically conserved type of PCD from which animal-specific apoptosis is believed to have evolved (Zhivotovsky, 2002;Golstein and Kroemer, 2005;Bozhkov and Jansson, 2007). Finding a potent role for zinc in the regulation of autophagic PCD establishes zinc deprivation as a universal cell death signal, regardless of which route of degradation-apoptotic or autophagic -is chosen by cells.…”

Section: Discussionmentioning

confidence: 99%

The Level of Free Intracellular Zinc Mediates Programmed Cell Death/Cell Survival Decisions in Plant Embryos

2008

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Zinc is a potent regulator of programmed cell death (PCD) in animals. While certain, cell-type-specific concentrations of intracellular free zinc are required to protect cells from death, zinc depletion commits cells to death in diverse systems. As in animals, PCD has a fundamental role in plant biology, but its molecular regulation is poorly understood. In particular, the involvement of zinc in the control of plant PCD remains unknown. Here, we used somatic embryos of Norway spruce (Picea abies) to investigate the role of zinc in developmental PCD, which is crucial for correct embryonic patterning. Staining of the early embryos with zinc-specific molecular probes (Zinquin-ethyl-ester and Dansylaminoethyl-cyclen) has revealed high accumulation of zinc in the proliferating cells of the embryonal masses and abrupt decrease of zinc content in the dying terminally differentiated suspensor cells. Exposure of early embryos to a membrane-permeable zinc chelator N,N,N#,N#-tetrakis(2-pyridylmethyl)ethylenediamine led to embryonic lethality, as it induced ectopic cell death affecting embryonal masses. This cell death involved the loss of plasma membrane integrity, metacaspase-like proteolytic activity, and nuclear DNA fragmentation. To verify the anti-cell death effect of zinc, we incubated early embryos with increased concentrations of zinc sulfate. Zinc supplementation inhibited developmental PCD and led to suppression of terminal differentiation and elimination of the embryo suspensors, causing inhibition of embryo maturation. Our data demonstrate that perturbation of zinc homeostasis disrupts the balance between cell proliferation and PCD required for plant embryogenesis. This establishes zinc as an important cue governing cell fate decisions in plants.

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From the nematode and mammals back to the pine tree: on the diversity and evolution of programmed cell death

Cited by 21 publications

References 23 publications

Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis

Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis

Pine embryogenesis

The Level of Free Intracellular Zinc Mediates Programmed Cell Death/Cell Survival Decisions in Plant Embryos

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