By Jessica Lu
Programmed cell death (PCD) is a genetically regulated form of cell death that occurs in response to intracellular events. 1 PCD is employed to remove damaged or redundant cells, and is an essential process for development and survival in both animals and plants. 2 The mechanisms underlying PCD differ between animals and plants. Whilst apoptosis is one of the most well-studied forms of programmed cell death in animals, neither apoptosis nor apoptotic machinery have been identified in plants. During apoptosis, animal cells are dismantled gradually into fragments called apoptotic bodies. However, rigid plant cell walls prevent cell fragmentation. 3 In plants, the mechanisms underlying PCD involve a complex network of signalling pathways that remains poorly understood. This makes it challenging to classify PCD in plants based on morphological and molecular features. Instead, PCD in plants can be broadly categorised depending on whether it is developmentally or environmentally induced. 1
During development, PCD occurs in plants to remodel cells, tissues, or organs. Developmentally induced PCD is precisely orchestrated in time and space to selectively remove cells during plant embryogenesis. 1 One example of PCD during plant development occurs during the early stages of cereal seed development. Maternal tissues including the nucellus, pericarp and nucellar projections are broken down to nourish new filial tissues including the embryo and the endosperm. This progressive degeneration of maternal tissues occurs via PCD. PCD must be tightly regulated both spatially and temporally to coordinate the flow of nutrients between different seed tissues. Both hormones and reactive oxygen species (ROS) are likely involved in regulating PCD to occur with well-defined spatial and temporal patterns. 4
PCD is also critical for plant reproductive development. All seeded plants are heterosporous, meaning that they produce two different sizes of spores: a larger megaspore and a smaller microspore. 5 These two sizes spores both give rise to reproductive cells via processes requiring PCD. The larger megaspore gives rise to the female gametophyte (embryo sac) after undergoing meiosis in the ovules. Initially four megaspores are created during development. However, only one megaspore is functional and selected to become the female gametophyte. The other three megaspores are degenerated by PCD. 6 On the other hand, the smaller microspore gives rise to male gametophytes (pollen grains). Whilst microspores develop into pollen, they are provided with nutrients and enzymes by a cell layer called the tapetum. Eventually, the tapetum undergoes PCD. 6 The timing of tapetum PCD is critical for male fertility, since premature or delayed PCD leads to pollen abortion. 7
Plant PCD can also be environmentally induced. Environmental triggers for PCD in plants include flooding, drought, and high light intensity. 4 During flooding, activation of PCD allows beneficial rearrangement of plant tissue morphology to adapt to adverse environmental conditions. Flooding causes soil to become waterlogged and air spaces between soil particles to be lost. This results in a condition called hypoxia, in which plant roots are deprived of oxygen. 1 In an adaptive response regulated by ethylene and ROS, PCD allows the cortex of the root to form internal air spaces called aerenchyma. 8 The aerenchyma create longitudinal channels, allowing air to diffuse from shoots to the waterlogged roots. 1 Aerenchyma are formed by PCD in many important crop species, such as in barley, wheat, rice and maize. 9
In contrast to flooding, drought is another unfavourable environmental condition for plants. During water deficit, photosynthesis is inhibited, causing photorespiration to predominate. This generates ROS, which induce leaf senescence. PCD allows shedding of these senescent leaves, beneficial to prevent further water loss through transpiration. Nutrients from shed leaves are also reallocated to other tissues, helping the rest of the plant to survive. 4As well as plant leaves, drought also induces PCD in plant root tips, forming an altered root system architecture as an important adaptive strategy to resist drought. 4,10 In Arabidopsis thaliana, PCD first causes undifferentiated root meristem cells to die, whilst mature root cells remain alive. After a prolonged period of drought, lateral roots emerge that are thicker and shorter compared to normal roots. These short roots grow very slowly but remain alive even during extreme drought. Upon rehydration, short roots quickly recover normal growth and new, morphologically normal roots are formed. 10
Finally, PCD also occurs in response to high levels of light. Although light is essential for plant growth, at high light intensities, plants absorb more light energy than can be used for photosynthetic metabolism. This excess light energy leads to the production of ROS. If the plant antioxidant systems are overwhelmed by the extra reactive oxygen species produced, this can cause cellular damage. 4 Old leaves are more sensitive to photooxidative damage than young leaves. Light induced PCD could serve a physiological function by sacrificing photodamaged old leaves to recover important nutrients, rather than investing resources into their repair. Furthermore, stomatal systems may also be damaged by high levels of light. By removing photodamaged leaves, PCD may also promote plant survival by preventing excessive water loss through the stomata. 11
Overall, PCD is critical for plant development and survival. During development, PCD is used to selectively break down tissues that are no longer required. Additionally, PCD is crucial for the development of plant reproductive morphology. 6 PCD also takes place as an adaptive response to stressful environmental conditions, including flooding, high light intensity, and drought. 4 In general, PCD in plants is often triggered by the production of reactive oxygen species. 1 Future research is required to uncover the precise molecular details underlying the processes of PCD in plants.
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