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Controlled cell death, plant survival and development

Key Points

  • Controlled cellular suicide in plants is important for the sculpting of organ shapes and the differentiation of specific cell types with diverse functions, as well as the removal of damaged or infected cells. These various types of programmed cell death (PCD) can have diverse morphotypes that are defined by their sequence of cytological changes, as well as the expression of various biochemical and molecular markers.

  • With the presence of a cell wall, the content of the dying cell inevitably leaks into the extracellular milieu and is then presumably recycled during the late stages of cell death in plants. This is a key differentiating feature compared with animal apoptosis where engulfment of the contents of the dead cell by neighbouring cells or macrophages prevents the activation of the inflammatory response.

  • Various phytohormones are known to function as signal molecules for cell-death pathways that are activated during pathogen defence or at a particular stage of plant development. However, their action could be dependent on the cellular context and environmental conditions.

  • Reactive oxygen species (ROS) and the mitochondrion are common mediators of PCD in plants and animals, whereas plastids provide an additional source of cell-death signalling that is specific for plant cells. Precise mechanisms and pathways through which ROS and organelle-derived signals regulate PCD in plants remain to be elucidated.

  • In spite of the lack of apparent orthologues for core regulators of cell death in animals, plants seem to use some similar molecules to serve analogous functions. These include caspase-like activities detected in different plant-cell-death model systems, the demonstration that expression of animal BAX can induce PCD in plants and fungi, and the identification of a conserved protein, BAX inhibitor-1 (BI-1), that can suppress cell death in both plants and animals.

  • The prominent vacuole and its associated process of autophagy could have important roles in plant PCD, as has been found for the animal lysosome in developmental cell death. In the future, genetic and molecular approaches with model plants such as Arabidopsis thaliana should help to delineate the possible overlaps in the autophagic and cell-death pathways in plant cells.

Abstract

For plants to develop properly and survive, programmed cell death is an important response strategy to various internal and external cues. Morphologically, a key difference between programmed cell death of plant cells and apoptosis in animals is the absence of engulfment by neighbouring cells in plants. Recent genetic, molecular and biochemical approaches have begun to reveal interesting candidate regulators in plants that show both similar and new properties compared with their animal counterparts.

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Figure 1: Examples of programmed cell death in plants.
Figure 2: Morphological comparison between programmed cell death in plants and animal apoptosis.

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Acknowledgements

Support by the United States Department of Agriculture on work related to plant cell death in my laboratory is gratefully acknowledged. I would also like to thank the New Jersey Commission on Science and Technology and the University of Hong Kong for partial support.

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DATABASES

Saccharomyces genome database

Yca1

Apg6

Swiss-Prot

GP91 phox

TAIR

acd2

acd5

acd6

agd2

BI-1

cpr1

cpr6

DND1

eds1

hlm1

lin2

LOL1

LOL2

lsd1

pad4

ssi2

Glossary

HYPERSENSITIVE RESPONSE

A rapid plant programmed cell death that is orchestrated in and surrounding the initial site of plant pathogen entry that is typically associated with the activation of disease resistance.

TRACHEARY ELEMENTS

Specialized cells in the xylem of vascular plants that are responsible for the conductance of fluids as well as providing mechanical support.

XYLEM

A tissue that comprises a large collection of specialized cells that are involved in the transport of water and solutes in vascular plants. Mature xylem vessels contain essentially only the cell wall.

MESOPHYLL

The photosynthetic tissue of a leaf that is internal to the epidermis, and contains both palisade and spongy cell types.

AERENCHYMA

Cortical cells that have undergone programmed cell death in the roots of grasses under low-oxygen conditions.

BLEBBING

Invagination of the membrane.

GYMNOSPERM

Non-flowering plants represented by pine and spruce.

LESION MIMICS

Also known as 'disease lesion mimics', this describes a class of phenotypes in which spontaneous cell death occurs as discrete 'zones' or 'lesions' that resemble the cell death that is observed during the hypersensitive response.

SYSTEMIC ACQUIRED RESISTANCE

(SAR). General, long-lasting plant defence that is activated at a distance from the initial site of attempted invasion by an avirulent pathogen of a host plant.

ENDOSPERM

Storage tissue surrounding the embryo in the seeds of flowering plants to provide nutrients for the developing seed as well as the germinating seedling.

ALEURONE

Specialized cell layer surrounding the starchy endosperm of cereal seeds that is responsible for the secretion of hydrolytic enzymes to degrade the endosperm upon seed germination.

ELICITOR

Pathogen-derived molecules, such as fungal-cell-wall fragments and secreted proteins, that can trigger defence responses of plant cells that resemble the hypersensitive response.

CYCLIC-NUCLEOTIDE-GATED CHANNEL

(CNGC). Conserved protein family with six predicted transmembrane helices that can form cation-conducting channels and is activated by the binding of lipophilic cyclic nucleotides such as cAMP and cGMP.

CASPASES

A family of cysteine proteases with specific target-site sequences that contain an aspartate residue at the P1 position. In addition to activating programmed cell death (PCD), caspases also function in non-PCD-related roles such as the processing of cytokines.

CALMODULIN

A Ca2+ protein that is found in all eukaryotes, calmodulin has a high degree of structural conservation and can bind to target enzymes and modulate their activity as a function of the cytosolic Ca2+ concentration.

PARACASPASES

A class of cysteine protease that is found in animals and slime mould and was identified as being structurally related to caspases by iterative sequence comparison.

METACASPASES

Predicted cysteine proteases that are found in plants, fungi and protozoa and which contain homologous sequences and domains that are structurally related to metazoan caspases.

AUTOPHAGY

A pathway for the recycling of cellular contents, in which materials inside the cell are packaged into vesicles and are then targeted to the vacuole or lysosome for bulk turnover.

AUTOPHAGOSOME

A double-membraned structure containing content for turnover that fuses with the vacuole, or the animal lysosome, during autophagy.

BIOTROPHIC

A lifestyle of pathogens that is dependent on a living host.

TYPE-III EFFECTORS

Proteins that are injected by gram-negative bacterial pathogens into their host cells via a conserved type-III secretory system.

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Lam, E. Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5, 305–315 (2004). https://doi.org/10.1038/nrm1358

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  • DOI: https://doi.org/10.1038/nrm1358

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