Plant leaves can get wounded and this physical damage of a leaf ruptures cells and disrupts outer cell layers. A gaping wound must be healed quickly in order to prevent water loss or pathogen entry. In most dicot leaves the wound is closed by the death of cells immediately adjacent to the wound and these cells are then sealed (Cui et al., in this issue of New Phytologist, pp. 634–640) . This wave of death in some respects resembles the island of death that accompanies the hypersensitive response (HR). As with the HR, the death programme needs to be tightly regulated as the death signal is quite capable of spreading from cell layer to cell layer and a controlled wave of death can become a runaway tsunami, which cataclysmically spreads throughout the entire leaf, or indeed, the entire plant. The ability of the death signal to spread throughout the plant, resulting in every cell in the plant dying, suggests all cell types in the plant are capable of dying and that the machinery for cell death is present throughout the plant. In his seminal paper, Martin Raff suggested that all mammalian cells constitutively maintain the machinery for cell death and he hypothesized that cell death may be the preselected option for a cell (Raff, 1992). This preselected option will always then be activated when no alternative has been specified by signals from the cell itself, or from its neighbouring cells (social signalling). This cellular default setting can mean cell death must be constantly switched off. Survival signals are required to culture plant cells below a certain critical threshold (McCabe et al., 1997) but it is not clear yet whether this mode of cell survival signalling is unbiquitous in plant cells. However, there is evidence that there are signalling pathways that switch on cell death in neighbouring plant cells but, just as importantly, cell regulation must also be activated to limit the spread of this death (Lorrain et al., 2003).
‘… the death programme needs to be tightly regulated as the death signal is quite capable of spreading from cell layer to cell layer and a controlled wave of death can become a runaway tsunami …’
Propagation, and subsequent limitation, of cell death is a fascinating topic as mutants that exhibit misregulation of cell death are useful tools in the understanding of cell death control in plants. For example, even in the absence of pathogens, lesion mimic mutants (LMMs) undergo cell death activation which resembles the HR. There are two main types of LMMs, the initiation LMMs that undergo constitutive formation of lesions, and the propagation LMMs which are characterized by ‘runaway’ cell death that can spread throughout the plant (Lorrain et al., 2003). An understanding of the control and regulation of death and survival may provide insights into the underlying regulation of life and death decisions in plant cells in general. Much of our understanding of this process: the propagation of the cell death signal, and the dampening of the cell death wave, comes from spontaneous cell death mutants such as lesions stimulating disease resistance1 (lsd1; Lorrain et al., 2003). In this issue, Cui et al. have investigated the regulation of cell death activation, and suppression, in wound induced death and specifically death in cells that are adjacent to compromised wounded cells. Wound induced death needs to be regulated by signals from the wound area – too weak a signal and you do not get any death – and the wound may not be closed. However regulation of this process does not end with the initiation of death in the cells that border the wound but, of equal importance, is the limitation of this death, to stop the wave of death from spreading throughout the plant.
Cui et al. investigated the control and regulation of death in a mutant that lacks BOTRYTIS SENSITIVE1/MYB108. This mutant was first identified in a screen for fungal susceptibility and the bos1 mutant lacks the MYB108 transcription factor (Mengiste et al., 2003). In addition to susceptibility to Botrytis, bos1 exhibits increased sensitivity to abiotic stresses such as elevated salinity, water deficit or oxidative stress (Mengiste et al., 2003). Cui et al. demonstrated that the bos1 mutant exhibits misregulated wound induced cell death that leads to runaway cell death. Unlike wild-type plants, where death is confined to a few layers beyond the wound, cell death in wounded bos1 plants spreads slowly from the wound site throughout the entire plant. Cui et al. convincingly demonstrated that abscisic acid (ABA) is involved in the spread of the wound induced cell death as exogenous ABA visibly enhanced the cell death. Indeed exogenous ABA was sufficient to induce cell death in unwounded bos1 plants and could even induce low levels of death in unwounded wild-type plants. Cui et al. concluded that the role of BOS1 is to act as a negative regulator of both ABA production and ABA induced cell death, thereby limiting cell death to cells adjacent to wounds. Reactive oxygen species (ROS) production was shown to be associated with ABA enhanced wound cell death but, unlike HR-like spreading cell death, ROS produced via the NADPH oxidases, RESPIRATORY BURST OXIDASE HOMOLOGS (RBOH; Torres et al., 2005) does not appear to have a role in the wound induced cell death, similarly there was no evidence that metacaspases are involved in the death process as they are in the lsd1 mutants (Coll et al., 2010). Again, unlike other runaway death programmes, this wound sealing death programme is independent of the stress hormones salicylate biosynthesis, ethylene or jasmonate. So while the bos1 mutant wound induced death has similarities to LMMs it appears to also have a significantly different control mechanism than other HR-associated runaway cell deaths.
Jones & Dangl (1996) asked several important questions about programmed cell death (PCD) using the analogy of death in Greek mythology, where the path from life to death began at the edge of the river Styx and there the souls of the dead waited for the ferryman Charon to transport the dead across the river to Hades. Using this analogy Jones & Dangl (1996) asked how many PCD pathways lead to the boundary of life and death, how many biological ferrymen exist to transport the doomed across this boundary and how many fates awaited the corpses on the other side? Cui et al. have provided further evidence that the answer to the first question is that there are many pathways that lead to the boundary of life and death, cells are continually processing external and internal information that leads to cellular responses, one of which can be the activation of a death programme (Reape & McCabe, 2008). Programmed cell death can be thought of as a three stage process of signal, activation, and degradation. We have seen that the process of degradation in plant cells seems to be carried out in a number of ways by several different nucleases and proteases, for example caspases, metacaspases or vacuolar processing enzymes (Lord & Gunawardena, 2012). Cui et al. demonstrate that the signalling pathway to death is also varied. Whether these various signals converge on a single core PCD activator or not remains to be determined. However answering the question of one, a few or many activators will be much easier by the elucidation of a range of well defined cell death pathways, and the article by Cui et al. adds ABA-regulated wounding to the collection of model systems with which to study cell death in plants.