12 Programmed Cell Death in Fungus–Plant Interactions AMIR SHARON 1 , ALIN FINKELSHTEIN 1 CONTENTS I. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219 II. Apoptosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 220 A. Apoptosis in Metazoan Organisms . . . . . 220 1. Apoptotic Pathways . . . . . . . . . . . . . . 220 2. Major Classes of Apoptosis-Related Proteins. . . . . . . . . . . . . . . . . . . . . . . . . 221 a) Caspases . . . . . . . . . . . . . . . . . . . . 221 b) Bcl-2 Proteins . . . . . . . . . . . . . . . 221 c) Inhibitor of Apoptosis Proteins 221 d) Mitochondria-Secreted Proteins 222 3. ROI and Apoptosis . . . . . . . . . . . . . . . 222 III. Plant PCD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 222 A. ROI Production . . . . . . . . . . . . . . . . . . . 222 B. HR and PCD . . . . . . . . . . . . . . . . . . . . . . 223 C. Plant PCD Pathways and Disease . . . . . 223 D. Effect of Anti-Apoptotic Genes on Disease Development . . . . . . . . . . . . 224 1. Baculovirus Protein p35 . . . . . . . . . 224 2. Bcl-2 Proteins. . . . . . . . . . . . . . . . . . 224 3. BI-1 and Mlo . . . . . . . . . . . . . . . . . . 225 IV. Apoptosis in Yeasts and Fungi . . . . . . . . . . . . . 226 A. Apoptosis in Yeasts. . . . . . . . . . . . . . . . . 226 1. Induction of Yeast Apoptosis . . . . . 226 2. Regulation of Yeast Apoptosis by Human Bcl-2 Proteins . . . . . . . . 226 3. Functional Analysis of Yeast Apoptotic Genes . . . . . . . . . . . . . . . 226 a) Aif1p and AIMD . . . . . . . . . . . 227 b) Yca1p . . . . . . . . . . . . . . . . . . . . 227 c) HtrA2/Nma111p . . . . . . . . . . . 227 d) IAP/Bir1p . . . . . . . . . . . . . . . . . 227 B. Apoptosis in Filamentous Fungi . . . . . 227 1. Morphological and Cytological Evidences . . . . . . . . . . . . . . . . . . . . . 227 2. Genomic Data . . . . . . . . . . . . . . . . . 228 3. Functional Characterization of Fungal PCD-Related Genes . . . . 228 4. Involvement of Fungal Apoptosis Pathways in Disease . . . . . . . . . . . . 229 a) Role of Fungal ROI . . . . . . . . . 229 b) Role of Fungal PCD . . . . . . . . 230 V. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231 I. Introduction Apoptosis was originally defined in mammals, where it plays a major role in controlling normal development. Apoptosis and several other forms of programmed cell death (PCD) have since been defined in metazoan as well as in plants, fungi and even in bacteria (Bredesen et al. 2006). For simplic- ity, when referring to cell death processes in plants and fungi we use the terms apoptosis or PCD throughout this chapter. Hypersensitive cell death (HR) is a plant resistance response in which spreading of incom- patible pathogens is restricted to a small number of plant cells. A hallmark of HR is appearance of small necroses that result from the local death of the host cells. Cell death observed during HR is preceded by enhanced production of reactive oxy- gen intermediates (ROI) and has typical markers of apoptosis. PCD is also observed during other types of plant–pathogen interactions including non-host as well as in compatible interactions. In some systems PCD was necessary for develop- ment of plant resistance, whereas in others it was harmful to the plant. Moreover, various pathogens developed ways to overcome, or even manipulate the plant PCD machinery for their advantage. Apoptosis is also emerging as an important mechanism in fungi. Yeasts and filamentous fungi undergo cell death with classic markers of meta- zoan apoptosis during various stages of develop- ment. PCD is observed in fungi during vegetative incompatibility, in sexual and asexual reproduction, at stationary phase, and in aged cultures. Homologs of mammalian apoptotic genes have been identified in fungi, supporting a conservation of apoptotic machinery between mammals and fungi. Several recent studies also imply that fungal PCD might be involved in mediating fungus–plant interactions. In this chapter we review the literature on PCD in plants and fungi and the role it may play in medi- ating fungus–plant interactions. 1 Department of Plant Sciences, Tel Aviv University, Tel Aviv 69978, Israel; e-mail: amirsh@ex.tau.ac.il, alinf@ex.tau.ac.il Plant Relationships, 2nd Edition The Mycota V H. Deising (Ed.) © Springer-Verlag Berlin Heidelberg 2009 mycota-chap12.indd 219 mycota-chap12.indd 219 10/20/2008 3:36:49 PM 10/20/2008 3:36:49 PM