Plant Molecular Biology44: vii–viii, 2000.E. Lam, H. Fukuda and J. Greenberg (Eds.), Programmed Cell Death in Higher Plants. vii

Preface

Cell death: the ‘Yin’ path in the balancing act of the life cycle

Eric Lam1 and Jean Greenberg2

1Biotech Center, Foran Hall, Cook College, Rutgers University, 59 Dudley Road, New Brunswick, NJ 08903, USA;2Molecular Genetics and Cell Biology Department, University of Chicago, 1103 E57 Street, Chicago, IL 60637,USA

For the Taoists of China in the ancient world, the bal-ance between Yin and Yang is considered the ultimatepath of becoming one with Nature. Yin, the Chineseword for shade, symbolizes repose, darkness, as wellas death. Yang represents the opposite of these qual-ities – vigor, light, and life. Thus, it seems that theancients recognized a long time ago that life is contin-uously being balanced by opposing forces in order toachieve the optimal state. In an analogous fashion, bi-ologists now also appreciate that organisms are underan equilibrium determined by opposite forces: signalsfor cellular destruction and others that drive prolifer-ation and/or differentiation. The delicate balance andcontrol of these processes determine the size, shapeand well-being of the organism as a whole.

The number of cells contained by a multicellularorganism at any specific point in time is the net re-sult of two opposite pathways: cell division and celldeath. Of the two processes, cell death has tradition-ally been more difficult to study since the cells understudy are continuously being destroyed and removed.Thus, it is not surprising that our understanding of celldeath is lagging behind that of cell division. However,like the study of mitosis, the virtual explosion in celldeath research during the past 6 years was ignited bya convergence of results from studies with differentmodel systems. For mitosis, the cloning of thecdc2kinase gene from yeasts, the finding that this gene isconserved in all eukaryotes and, finally, the demon-stration that its product is the homologue of the kinasesubunit of the maturation-promoting factor (MPF) de-fined in frog eggs united the field of cell division.Perhaps the most spectacular consequence from thisunification is the cross-feeding of information, toolsand expertise that have been gained from studies us-

ing divergent model systems. For cell death research,the breakthrough came about in 1993 with the cloningof theced-3gene from the nematodeCaenorhabditiselegans. ced-3is required for the programmed deathof the 131 cells that are normally produced and subse-quently removed by this worm. Its sequence revealedced-3encodes a homologue of a mammalian cysteineprotease, called ICE, previously identified by its proin-terleukin 1-β processing activity. With the cloning ofced-9, whose product encodes a negative regulator ofcell death inC. elegans, and its homology with themammalian cell death suppressor geneBCL2 realizedin 1994, the field of programmed cell death (PCD)began its steep rise and it is still in its rapid phase ofinformation expansion since these seminal findings.

For plants, it is perhaps ironic that the field of PCDhas lagged behind that of the animal systems, sincetwo terms closely associated with this field are botan-ical in origin. The descriptive noun ‘cell’ originatedfrom the early microscopist Robert Hooke in the 1650swho examined cork slices under crude light micro-scopes and likened the regular arrangement of ‘pores’to those of cells in a monastery. These are now recog-nized as plant cells that had underwent PCD in orderto form a functional structure that is vital to the plant’ssurvival. Apoptosis, the most well-characterized formof animal PCD, is a Greek word that describes thefalling of leaves and petals during their natural senes-cence process. In spite of the late entry into the fieldof PCD, we believe that plants promise to hold manysurprises and differences from their animal counter-parts in the way that their cells may carry out their owndemise. As many articles in this special issue ofPlantMolecular Biologyillustrate, plant PCD occurs in awide variety of cell types with distinct purposes. Un-

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like animal apoptosis, where the dead cell’s corpse israpidly ‘removed’ through ingestion by its neighbors,with perhaps the exception of keratinocytes wheredead skin cells are continuously shed from the body,most plant cells remain at least for a time after theirdeath. In many instances, such as the tracheary ele-ments, the dead cells serve an important function andare not actively removed during the life of the plant.Comparison of key players in plant PCD with thosedefined in animal systems should provide interestingclues to the evolution of PCD in multicellular organ-isms. Several interesting new pieces of informationthat may help to integrate plant research into that ofthe general field of PCD studies are: (1) cloning ofplant homologues to the retinoblastoma (Rb) gene, atumor-suppressor gene from animal systems that canalso regulate PCD; the cooperation of its product withplant viral factors for infection may be one componentthat determines the ability of the virus to proliferate inthe plant host; (2) flow cytometry studies with tobaccocells revealed that reactive oxygen species, an inducerof PCD in animals, can induce cell cycle arrest atthe G1/S boundary, and accelerate their entry into thedeath pathway; (3) detection of caspase-like proteaseactivity in plant extracts and the evidence for theiressential role in cell death during the hypersensitiveresponse (HR). This result suggests the first biochem-

ical component critical for PCD induction that may beconserved between plants and animals. Recent studiesalso suggest that plant mitochondria could be playingan important role during plant PCD, at least in thecontext of the HR. Together with the view that thisorganelle may also control different forms of cell deathin animal systems as well as yeast, these findings areconsistent with the view that a conserved pathway forcell death induction may eventually emerge.

With rapid advances being made in genomic sci-ences, molecular genetics, and cell biological tech-nologies, we anticipate the ramp-up of PCD researchin higher plants is merely beginning. Together with ourincreased understanding of related pathways such ascell cycle control, hormonal signaling, plant-pathogeninteractions and cloning of marker genes that mayallow us to differentiate between different death path-ways, we are optimistic that plant PCD research willmake a significant impact on general plant biology inaddition to enriching our understanding of the central,conserved mechanisms of the ‘death engine’. Fromcell death in reproductive tissues to xylem differen-tiation to plant disease responses, we especially hopethat this special issue will serve as a timely guide to theyoung plant scientists who are looking for a new nicheof plant biology the potential of which is waiting to betapped.