Only in dying, life: programmed cell death during plant development

doi:10.1016/j.tplants.2014.10.003

Trends in Plant Science

Volume 20, Issue 2, February 2015, Pages 102-113

https://doi.org/10.1016/j.tplants.2014.10.003 Get rights and content

Highlights

•
Programmed cell death (PCD) is an integral part of plant life.
•
Numerous PCD instances occur during regular plant development.
•
Developmental PCD is tightly linked with cellular differentiation.
•
Successful vegetative and reproductive development depends on precise PCD control.

Programmed cell death (PCD) is a fundamental process of life. During the evolution of multicellular organisms, the actively controlled demise of cells has been recruited to fulfil a multitude of functions in development, differentiation, tissue homeostasis, and immune systems. In this review we discuss some of the multiple cases of PCD that occur as integral parts of plant development in a remarkable variety of cell types, tissues, and organs. Although research in the last decade has discovered a number of PCD regulators, mediators, and executers, we are still only beginning to understand the mechanistic complexity that tightly controls preparation, initiation, and execution of PCD as a process that is indispensable for successful vegetative and reproductive development of plants.

Section snippets

Programmed cell death in plants and animals

Although it may seem paradoxical, programmed cell death (PCD) is a fundamental process of life, and as such may have originated before the advent of eukaryotes [1]. With the evolution of increasingly complex multicellular organisms, PCD has been adapted to diverse functions in developmental patterning, cell differentiation, cell number homeostasis, and immune systems. Different PCD types have been distinguished by function, occurrence, and morphological and biochemical features [2]. However, a

Nonfunctional megaspores

The female gametophyte (embryo sac) develops inside the ovules after meiosis of the megaspore mother cell. Similar to animal oogenesis, a single meiotic product, the functional megaspore, is selected for further development, whereas the three nonfunctional megaspores degenerate. The selection of the functional megaspore is position-dependent and varies between species [11]. This position-dependency, and the fact that in some species more than one functional megaspore can survive suggest that

Tapetum

Male gametophytes (pollen grains) are produced by sporogenic tissue inside anthers. Numerous microspore mother cells undergo meiosis, each forming four haploid microspores, which subsequently develop into mature pollen grains consisting of one accessory cell (vegetative cell) surrounding two gametes (sperm cells) (Figure 1). The developing microspores are supported by the ephemeral tapetum layer, which undergoes dPCD during pollen development (see [31] for recent review). Aberrations in tapetum

Embryonic suspensor

After fertilization, the plant zygote undergoes a first, unequal division. The smaller apical cell develops into the embryo proper, whereas the larger basal cell forms the embryo suspensor. The suspensor occurs in a variety of shapes and sizes in different species, ranging from a few cells in Arabidopsis to hundreds or thousands of cells in some other dicots, or in gymnosperms such as Norway spruce (Picea abies). The suspensor fixes the embryo proper within the seed and contributes to the setup

Xylem tracheary elements

In the angiosperm xylem, tracheary elements undergo PCD as a terminal differentiation step, creating an interconnected system of hollow tubes for water transport (see [73] for a detailed review). The formation of tracheary elements involves several processes, including cell specification, secondary cell wall formation and lignification, PCD, and clearance of cellular contents, processes that have been suggested to increase the efficiency of tracheary elements as water conductors [74]. Much

Concluding remarks – common themes and future challenges

Traditionally PCD has been viewed as important for disease resistance in plants, but it has not received much attention from plant developmental biologists. In this review, we have highlighted its ubiquity and importance for plant development and successful reproduction. The acquisition of the competency to undergo PCD often appears to be an inherent part of cellular development that is tightly coordinated with other cellular differentiation processes. Therefore, dPCD might be fundamentally

Acknowledgements

We thank Matthias Van Durme for artwork in Figure 1, and Annick Bleys for help with preparing the manuscript. T.V.H. and M.K.N. gratefully acknowledge funding from FWO, and A.J.W. and J.G. acknowledge funding from the BBSRC.

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Citation Excerpt :
It occurs during both development (known as dPCD) and the responses to environment (known as ePCD). In plants, dPCD is involved in many processes including xylem formation, embryogenesis, pollen maturation, seed maturation, and leaf senescence (Van Hautegem et al., 2015). ePCD is very important for plants to defense against environmental stresses including both abiotic stresses (e.g., salt stress, drought stress, cold stress, and heat stress) and biotic stresses (e.g., pathogens and insects).
Programmed cell death (PCD) is essential for both plant development and stress responses including immunity. However, how plants control PCD is not well-understood. The shikimate pathway is one of the most important metabolic pathways in plants, but its relationship to PCD is unknown. Here, we show that the shikimate pathway promotes PCD in Arabidopsis. We identify a photoperiod-dependent lesion-mimic mutant named Lesion in short-day (lis), which forms spontaneous lesions in short-day conditions. Map-based cloning and whole-genome resequencing reveal that LIS encodes MEE32, a bifunctional enzyme in the shikimate pathway. Metabolic analysis shows that the level of shikimate is dramatically increased in lis. Through genetic screenings, three suppressors of lis (slis) are identified and the causal genes are cloned. SLISes encode proteins upstream of MEE32 in the shikimate pathway. Furthermore, exogenous shikimate treatment causes PCD. Our study uncovers a link between the shikimate pathway and PCD, and suggests that the accumulation of shikimate is an alternative explanation for the action of glyphosate, the most successful herbicide.

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^☆: ‘Only in silence the word, Only in dark the light, Only in dying life: Bright the hawk's flight On the empty sky.’ The Earthsea Trilogy – Ursula K. LeGuin.

^*: These authors contributed equally to this work.

View full text

Trends in Plant Science

Feature ReviewOnly in dying, life: programmed cell death during plant development☆

Highlights

Section snippets

Programmed cell death in plants and animals

Nonfunctional megaspores

Tapetum

Embryonic suspensor

Xylem tracheary elements

Concluding remarks – common themes and future challenges

Acknowledgements

Cell

J. Proteomics

Curr. Biol.

Curr. Biol.

Dev. Cell

Dev. Cell

Trends Plant Sci.

Plant Sci.

Curr. Biol.

Curr. Biol.

Curr. Biol.

Curr. Biol.

Dev. Cell

Trends Plant Sci.

Trends Plant Sci.

Mol. Plant

C. R. Biol.

Trends Plant Sci.

Curr. Biol.

Trends Plant Sci.

Trends Plant Sci.

Field Crops Res.

On the origin, evolution, and nature of programmed cell death: a timeline of four billion years

Cell Death Differ.

Classes of programmed cell death in plants, compared to those in animals

J. Exp. Bot.

The biochemistry of apoptosis

Nature

The BCL-2 protein family: opposing activities that mediate cell death

Nat. Rev. Mol. Cell Biol.

Regulation of apoptosis in Drosophila

Cell Death Differ.

Alternative cell death mechanisms in development and beyond

Genes Dev.

The death of plant cells: from proteases to field applications

Cell Death Differ.

Programmed cell death in the plant immune system

Cell Death Differ.

Strategies to ameliorate abiotic stress-induced plant senescence

Plant Mol. Biol.

Callose in cell walls during megasporogenesis in angiosperms

Planta

Reconstructing the ancestral female gametophyte of angiosperms: insights from Amborella and other ancient lineages of flowering plants

Am. J. Bot.

The classical arabinogalactan protein AGP18 mediates megaspore selection in Arabidopsis

Plant Cell

Megasporogenesis and programmed cell death in Tillandsia (Bromeliaceae)

Protoplasma

Female gametophyte and early seed development in Peperomia (Piperaceae)

Am. J. Bot.

Family life at close quarters: communication and constraint in angiosperm seed development

Protoplasma

The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development

Planta

The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development

Plant Cell

Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth

J. Exp. Bot.

Jekyll encodes a novel protein involved in the sexual reproduction of barley

Plant Cell

Love is a battlefield: programmed cell death during fertilization

J. Exp. Bot.

Synergid cell death in Arabidopsis is triggered following direct interaction with the pollen tube

Plant Physiol.

Conserved molecular components for pollen tube reception and fungal invasion

Science

FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development

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

Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis

Feature Review
Only in dying, life: programmed cell death during plant development☆