Programmed Cell Death in Development and Defense

A. M. Jones
2001 Plant Physiology  
Around the time of this journal's first volume, the concept of PCD, i.e. the cell's active participation in its own demise, was introduced using the example of a plant cell infected by a fungus (1). This was 7 decades before the flurry of apoptosis research in animals. Death during an incompatible interaction between a plant and a pathogen was proposed to function as a physical block to further pathogen ingress. This "program" concept profoundly influenced the mindset of a large number of
more » ... logists studying cell death in various contexts for the rest of the century. Plant physiologists knew that cell death is essential for normal development. Carl Leopold made this point to the general scientific audience in his influential 1961 paper (16) by enumerating the evidence for the selective ecological and evolutionary fitness conferred by cell death in plants, its importance for normal plant physiology, and its control by the balance between both survival and death signals. His publication marked the revival of interest in PCD in the modern era, a decade before Kerr et al. (13) coined the term "apoptosis" to describe the first cell death morphotype in animal cells. Three strands of research came together to shape today's research agenda about plant PCD: terminal differentiation, senescence, and disease resistance. Cell death fulfills several essential functions in plant development: (a) Senescence removes cells by recycling much of its carbon, nitrogen, and phosphorous; (b) cell death is important in sculpting tissues such as the formation of lysigenous aerenchyma, flower primordia during floral abortion, and aleurone layers during germination; (c) cells invaded by pathogens may be self eliminated as part of a hypersensitive response against the pathogen; (d) cell death also occurs during terminal differentiation and the classic example is the formation of vessel members and tracheids, collectively termed tracheary elements (TE); and (e) cell death is programmed when the metabolism of cells is perturbed either by coping with abiotic stresses imposed upon it or by bioengineering. Research up to the 1970s focused primarily on the cytology of death, biochemical characterization of dying cells, and the discovery of survival-and death-inducing signals. The 1980s saw the introduc-tion of genetics to study cell death and the last decade focused primarily on identifying the signal intermediates in this pathway. I intend to take a broad view of plant cell death, and from it, identify features of cell death that are shared among all PCDs. The conclusion will be a testable model on how death is triggered and the corpse managed. CELL DEATH IS AN ACTIVE PROGRAM INDUCED BY SIGNALS The evidence that death is an active program came first and primarily from work on leaf senescence. Yoshio Yoshida elegantly showed that the nucleus is required for cellular disassembly (21) and so it is not surprising that many labs independently showed that inhibitors of protein translation block leaf senescence. Non-senescencing (stay-green) mutants have been isolated indicating that components of plant PCD are genetically programmed and senescence has been shown to be reversible and regulated by signals such as hormones and light (18). For example, it is long known that cytokinin blocks senescence. This was shown more recently by a clever strategy from Amasino's group at the University of Wisconsin (Madison). They generated plants that do not senesce by simply engineering a cytokinin synthesis gene driven by a senescence-inducible promoter (7). In contrast to cytokinin, ethylene accelerates senescence consistent with the observed delay in senescence by ethylene-insensitive plants (8). In lesion formation of the hypersensitive response, evidence suggests that salicylic acid plays an early and a later potentiating role (19). These results taken together indicate unequivocally that plant PCD defines an active process of death, genetically dissectable and cytoplasmically driven. Moreover, it is now clear that plant cells integrate death and survival signals to make decisions when to die. As will be discussed further below, we now know that these signals also instruct cells how to process their own corpse. An active program of death has also been shown for terminal differentiation, lysigenous aerenchyma formation, and aleurone degradation, although in all cases with much less rigor than by researchers working on senescence. Most of the evidence was published in the 1990s in the form of pharmacological studies showing that death can be inhibited, thus eliminating the possibility that death is a consequence of metabolic run-down. Moreover, these *
doi:10.1104/pp.125.1.94 pmid:11154305 fatcat:i2eisbx5dbh2jpz2wiegshebxa