Abstract
Plants have evolved various means for controlled and organized cell destruction, known as programmed cell death (PCD). PCD is a crucial event in plant immunity against microbial infection that prevents the spread of pathogens. Plants lack homologs of most apoptosis-related genes in animals and have evolved specific mechanisms for PCD. Cryptogein-triggered defense responses and PCD in tobacco BY-2 cells are a useful simple model system to monitor cellular events in which most plant defense responses can be mimicked. Recent live cell imaging techniques have revealed the dynamic features and significant roles of the cytoskeleton, such as actin microfilaments and microtubules, as well as the vacuole, an organelle occupying most of the cell volume, during defense responses and PCD. Both the production of reactive oxygen species (ROS) by NADPH oxidase and its temporal pattern have been suggested to play a crucial role in triggering and regulating PCD. Prior to the induction of defense responses and PCD, cell cycle arrest is induced either at G1 or G2 phase. In turn, defense signaling and responses including PCD are dependent on cell cycle phases and are only induced following cell cycle arrest. Here, we overview the dynamic reorganization of the cellular architecture, signaling events, and interrelationship between the cell cycle and innate immunity/PCD.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Bozhkov PV, Lam E (2011) Green death: revealing programmed cell death in plants. Cell Death Differ 18:1239–1240
Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 147:742–758
Teng X, Cheng WC, Qi B et al (2011) Gene-dependent cell death in yeast. Cell Death Dis 2:e188
Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168
Greenberg JT (1996) Programmed cell death: a way of life for plants. Proc Natl Acad Sci U S A 93:12094–12097
Wei CX, Lan SY, Xu ZX (2002) Ultrastructural features of nucleus degradation during programmed cell death of starchy endosperm cells in rice. Acta Bot Sin 44:1396–1402
Hanamata S, Kurusu T, Kuchitsu K (2014) Roles of autophagy in male reproductive development in plants. Front Plant Sci 5:457
Kurusu T, Kimura S, Tada Y et al (2013) Plant signaling networks involving reactive oxygen species and Ca2+. In: Suzuki M, Yamamoto S (eds) Handbook on reactive oxygen species (ROS): formation mechanisms, physiological roles and common harmful effects. Nova Science, New York, pp 315–324
Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334
Mur LA, Kenton P, Lloyd AJ et al (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59:501–520
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548
Cacas JL (2010) Devil inside: does plant programmed cell death involve the endomembrane system? Plant Cell Environ 33:1453–1473
Reape TJ, McCabe PF (2010) Apoptotic-like regulation of programmed cell death in plants. Apoptosis 15:249–256
Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18:1247–1256
Kobayashi I, Kobayashi Y, Hardham AR (1994) Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195:237–247
Skalamera D, Heath MC (1996) Cellular mechanisms of callose deposition in response to fungal infection or chemical damage. Can J Bot 74:1236–1242
Kobayashi Y, Kobayashi I, Funaki Y et al (1997) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J 11:525–537
Takemoto D, Jones DA, Hardham AR (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33:775–792
Koh S, André A, Edwards H et al (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44:516–529
Reichheld JP, Vernoux T, Lardon F et al (1999) Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J 17:647–656
Sano T, Higaki T, Handa K et al (2006) Calcium ions are involved in the delay of plant cell cycle progression by abiotic stresses. FEBS Lett 580:597–602
Bailey-Serres J, Voesenek LA (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339
De Schutter K, Joubès J, Cools T et al (2007) Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19:211–225
Mannuss A, Trapp O, Puchta H (2012) Gene regulation in response to DNA damage. Biochim Biophys Acta 1819:154–165
Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18:277–284
Logemann E, Wu SC, Schröder J et al (1995) Gene activation by UV light, fungal elicitor or fungal infection in Petroselinum crispum is correlated with repression of cell cycle-related genes. Plant J 8:865–876
Suzuki K, Nishiuchi T, Nakayama Y et al (2006) Elicitor-induced down-regulation of cell cycle-related genes in tobacco cells. Plant Cell Environ 29:183–191
Kawaguchi Y, Nishiuchi T, Kodama H et al (2012) Fungal elicitor-induced retardation and its restoration of root growth in tobacco seedlings. Plant Growth Regul 66:59–68
Yoshiyama K, Conklin PA, Huefner ND et al (2009) Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proc Natl Acad Sci U S A 106:12843–12848
Gross P, Julius C, Schmelzer E et al (1993) Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defense gene activation in infected, cultured parsley cells. EMBO J 12:1735–1744
Lecourieux D, Mazars C, Pauly N et al (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14:2627–2641
Kadota Y, Goh T, Tomatsu H et al (2004) Cryptogein-induced initial events in tobacco BY-2 cells: pharmacological characterization of molecular relationship among cytosolic Ca2+ transients, anion efflux and production of reactive oxygen species. Plant Cell Physiol 45:160–170
Kadota Y, Kuchitsu K (2006) Regulation of elicitor-induced defense responses by Ca2+ channels and the cell cycle in tobacco BY-2 cells. In: Nagata T, Matsuoka K, Inze D (eds) Biotechnology in agriculture and forestry 58 Tobacco BY-2 cells: from cellular dynamics to omics. Springer, Berlin, pp 207–221
Franklin-Tong VE, Gourlay CW (2008) A role for actin in regulating apoptosis/programmed cell death: evidence spanning yeast, plants and animals. Biochem J 413:389–404
Higaki T, Kurusu T, Hasezawa S et al (2011) Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants. J Plant Res 124:315–324
Kutsuna N, Hasezawa S (2002) Dynamic organization of vacuolar and microtubule structures during cell cycle progression in synchronized tobacco BY-2 cells. Plant Cell Physiol 43:965–973
Kumagai F, Yoneda A, Tomida T et al (2001) Fate of nascent microtubules organized at the M/G1 interface, as visualized by synchronized tobacco BY-2 cells stably expressing GFP-tubulin: time-sequence observations of the reorganization of cortical microtubules in living plant cells. Plant Cell Physiol 42:723–732
Sano T, Higaki T, Oda Y et al (2005) Appearance of actin microfilament ‘twin peaks’ in mitosis and their function in cell plate formation, as visualized in tobacco BY-2 cells expressing GFP-fimbrin. Plant J 44:595–605
Higaki T, Goh T, Hayashi T et al (2007) Elicitor-induced cytoskeletal rearrangement relates to vacuolar dynamics and execution of cell death: in vivo imaging of hypersensitive cell death in tobacco BY-2 cells. Plant Cell Physiol 48:1414–1425
Higaki T, Kadota Y, Goh T et al (2008) Vacuolar and cytoskeletal dynamics during elicitor-induced programmed cell death in tobacco BY-2 cells. Plant Signal Behav 3:700–703
Marty F (1999) Plant vacuoles. Plant Cell 11:587–600
Oda Y, Higaki T, Hasezawa S et al (2009) New insights into plant vacuolar structure and dynamics. Int Rev Cell Mol Biol 277:103–135
Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125:94–97
Hara-Nishimura I, Hatsugai N (2011) The role of vacuole in plant cell death. Cell Death Differ 18:1298–1304
Hatsugai N, Kuroyanagi M, Yamada K et al (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–858
Hatsugai N, Kuroyanagi M, Nishimura M et al (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11:905–911
Hatsugai N, Iwasaki S, Tamura K et al (2009) A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23:2496–2506
Saito C, Ueda T, Abe H et al (2002) A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J 29:245–255
Saito C, Uemura T, Awai C et al (2011) The occurrence of ‘bulbs’, a complex configuration of the vacuolar membrane, is affected by mutations of vacuolar SNARE and phospholipase in Arabidopsis. Plant J 68:64–73
Saito C, Uemura T, Awai C et al (2011) Qualitative difference between “bulb” membranes and other vacuolar membranes. Plant Signal Behav 6:1914–1917
Obara K, Kuriyama H, Fukuda H (2001) Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol 125:615–626
Smertenko AP, Bozhkov PV, Filonova LH et al (2003) Re-organisation of the cytoskeleton during developmental programmed cell death in Picea abies embryos. Plant J 33:813–824
Gunawardena AH (2008) Programmed cell death and tissue remodelling in plants. J Exp Bot 59:445–451
Guo WJ, Ho TH (2008) An abscisic acid-induced protein, HVA22, inhibits gibberellin-mediated programmed cell death in cereal aleurone cells. Plant Physiol 147:1710–1722
Wright H, van Doorn WG, Gunawardena AH (2009) In vivo study of developmental programmed cell death using the lace plant (Aponogeton madagascariensis; Aponogetonaceae) leaf model system. Am J Bot 96:865–876
Stone SL, Williams LA, Farmer LM et al (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18:3415–3428
Gu Y, Innes RW (2012) The KEEP ON GOING protein of Arabidopsis regulates intracellular protein trafficking and is degraded during fungal infection. Plant Cell 24:4717–4730
Gu Y, Innes RW (2011) The KEEP ON GOING protein of Arabidopsis recruits the ENHANCED DISEASE RESISTANCE1 protein to trans-Golgi network/early endosome vesicles. Plant Physiol 155:1827–1838
Wawrzynska A, Christiansen KM, Lan Y et al (2008) Powdery mildew resistance conferred by loss of the ENHANCED DISEASE RESISTANCE1 protein kinase is suppressed by a missense mutation in KEEP ON GOING, a regulator of abscisic acid signaling. Plant Physiol 148:1510–1522
Higaki T, Kutsuna N, Okubo E et al (2006) Actin microfilaments regulate vacuolar structures and dynamics: dual observation of actin microfilaments and vacuolar membrane in living tobacco BY-2 Cells. Plant Cell Physiol 47:839–852
Pajerowska-Mukhtar K, Dong X (2009) A kiss of death-proteasome-mediated membrane fusion and programmed cell death in plant defense against bacterial infection. Genes Dev 23:2449–2454
Lampl N, Alkan N, Davydov O et al (2013) Set-point control of RD21 protease activity by AtSerpin1 controls cell death in Arabidopsis. Plant J 74:498–510
Lampl N, Budai-Hadrian O, Davydov O et al (2010) Arabidopsis AtSerpin1, crystal structure and in vivo interaction with its target protease RESPONSIVE TO DESICCATION-21 (RD21). J Biol Chem 285:13550–13560
Seybold H, Trempel F, Ranf S (2014) Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms. New Phytol 204:782–790
Kuchitsu K, Kikuyama M, Shibuya N (1993) N-acetylchitooligosaccharides, biotic elicitor for phytoalexin production, induce transient membrane depolarization in suspension-cultured rice cells. Protoplasma 174:79–81
Kikuyama M, Kuchitsu K, Shibuya N (1997) Membrane depolarization induced by N-acetylchitooligosaccharide elicitor in suspension-cultured rice cells. Plant Cell Physiol 38:902–909
Kuchitsu K, Yazaki Y, Sakano K et al (1997) Transient cytoplasmic pH change and ion fluxes through the plasma membrane in suspension-cultured rice cells triggered by N-acetylchitooligosaccharide elicitor. Plant Cell Physiol 38:1012–1018
Kurusu T, Hamada H, Sugiyama Y et al (2011) Negative feedback regulation of microbe-associated molecular pattern-induced cytosolic Ca2+ transients by protein phosphorylation. J Plant Res 124:415–424
Kuchitsu K, Kosaka H, Shiga T et al (1995) EPR evidence for generation of hydroxyl radical triggered by N-acetylchitooligosaccharide elicitor and a protein phosphatase inhibitor in suspension-cultured rice cells. Protoplasma 188:138–142
Kärkönen A, Kuchitsu K (2014) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32
Kadota Y, Watanabe T, Fujii S et al (2005) Cell cycle dependence of elicitor-induced signal transduction in tobacco BY-2 cells. Plant Cell Physiol 46:156–165
Kadota Y, Fujii S, Ogasawara Y et al (2006) Continuous recognition of the elicitor signal for several hours is prerequisite for induction of cell death and prolonged activation of signaling events in tobacco BY-2 cells. Plant Cell Physiol 47:1337–1342
Kadota Y, Watanabe T, Fujii S et al (2004) Crosstalk between elicitor-induced cell death and cell cycle regulation in tobacco BY-2 cells. Plant J 40:131–142
Ohno R, Kadota Y, Fujii S et al (2011) Cryptogein-induced cell cycle arrest at G2 phase is associated with inhibition of cyclin-dependent kinases, suppression of expression of cell cycle-related genes and protein degradation in synchronized tobacco BY-2 cells. Plant Cell Physiol 52:922–932
Torres MA, Jones JD, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130–1134
Suzuki N, Miller G, Morales J et al (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699
Ogasawara Y, Kaya H, Hiraoka G et al (2008) Synergistic activation of Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892
Takeda S, Gapper C, Kaya H et al (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244
Kimura S, Kaya H, Kawarazaki T et al (2012) Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta 1823:398–405
Kobayashi M, Ohura I, Kawakita K et al (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080
Kimura S, Kawarazaki T, Nibori H et al (2013) The CBL-interacting protein kinase CIPK26 is a novel interactor of Arabidopsis NADPH oxidase AtRbohF that negatively modulates its ROS-producing activity in a heterologous expression system. J Biochem 153:191–195
Drerup MM, Schlücking K, Hashimoto K et al (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6:559–569
Hamada H, Kurusu T, Okuma E et al (2012) Regulation of a proteinaceous elicitor-induced Ca2+ influx and production of phytoalexins by a putative voltage-gated cation channel, OsTPC1, in cultured rice cells. J Biol Chem 287:9931–9939
Gauthier A, Lamotte O, Reboutier D et al (2007) Cryptogein-induced anion effluxes: electrophysiological properties and analysis of the mechanisms through which they contribute to the elicitor-triggered cell death. Plant Signal Behav 2:86–95
Kurusu T, Saito K, Horikoshi S et al (2013) An S-type anion channel SLAC1 is involved in cryptogein-induced ion fluxes and modulates hypersensitive responses in tobacco BY-2 Cells. PLoS One 8:e70623
Inagaki S, Umeda M (2011) Cell-cycle control and plant development. Int Rev Cell Mol Biol 291:227–261
Reinhardt HC, Schumacher B (2012) The p53 network: cellular and systemic DNA damage responses in aging and cancer. Trends Genet 28:128–136
Schwessinger B, Zipfel C (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11:389–395
Lorrain S, Vailleau F, Balagué C et al (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263–271
Wu C, Bordeos A, Madamba MR et al (2008) Rice lesion mimic mutants with enhanced resistance to diseases. Mol Genet Genomics 279:605–619
Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the “Hela” cell in the cell biology of higher plants. Int Rev Cyt 132:1–30
Mironov VV, De Veylder L, Van Montagu M et al (1999) Cyclin-dependent kinases and cell division in plants – the nexus. Plant Cell 11:509–522
Umeda M, Shimotohno A, Yamaguchi M (2005) Control of cell division and transcription by cyclin-dependent kinase-activating kinases in plants. Plant Cell Physiol 46:1437–1442
Sperka T, Wang J, Rudolph KL (2012) DNA damage checkpoints in stem cells, ageing and cancer. Nat Rev Mol Cell Biol 13:579–590
Sullivan KD, Gallant-Behm CL, Henry RE et al (2012) The p53 circuit board. Biochim Biophys Acta 1825:229–244
Xiong Y, Hannon GJ, Zhang H et al (1993) p21 is a universal inhibitor of cyclin kinases. Nature 366:701–704
O’connor PM, Ferris DK, Pagano M et al (1993) G2 delay induced by nitrogen mustard in human cells affects cyclin A/cdk2 and cyclin B1/cdc2-kinase complexes differently. J Biol Chem 268:8298–8308
Jin P, Gu Y, Morgan DO (1996) Role of inhibitory CDC2 phosphorylation in radiation-induced G2 arrest in human cells. J Cell Biol 134:963–970
Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12:414–420
Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465
Maekawa T, Kufer TA, Schulze-Lefert P (2011) NLR functions in plant and animal immune systems: so far and yet so close. Nat Immunol 12:817–826
Gassmann W, Bhattacharjee S (2012) Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks. Mol Plant Microbe Interact 25:862–868
Liu W, Liu J, Ning Y et al (2013) Recent progress in understanding PAMP- and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Mol Plant 6:605–620
Mittler R, Vanderauwera S, Suzuki N et al (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309
Livanos P, Apostolakos P, Galatis B (2012) Plant cell division: ROS homeostasis is required. Plant Signal Behav 7:771–778
Kaya H, Nakajima R, Iwano M et al (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–1080
Marino D, Dunand C, Puppo A et al (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15
Burhans WC, Heintz NH (2009) The cell cycle is a redox cycle: linking phase-specific targets to cell fate. Free Radic Biol Med 47:1282–1293
Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 99:517–522
Yoshie Y, Goto K, Takai R et al (2005) Function of the rice gp91phox homologs OsrbohA and OsrbohE genes in ROS-dependent plant immune responses. Plant Biotechnol 22:127–135
Wong HL, Pinontoan R, Hayashi K et al (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19:4022–4034
Zhang S, Du H, Klessig DF (1998) Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell 10:435–450
Yoshioka H, Sugie K, Park HJ et al (2001) Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol Plant Microbe Interact 14:725–736
Yoshioka H, Numata N, Nakajima K et al (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15:706–718
Underwood W, Zhang S, He SY (2007) The Pseudomonas syringae type III effector tyrosine phosphatase HopAO1 suppresses innate immunity in Arabidopsis thaliana. Plant J 52:658–672
Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277:559–565
Menges M, Hennig L, Gruissem W et al (2002) Cell cycle-regulated gene expression in Arabidopsis. J Biol Chem 277:41987–42002
Suzuki K, Yano A, Shinshi H (1999) Slow and prolonged activation of the p47 protein kinase during hypersensitive cell death in a culture of tobacco cells. Plant Physiol 119:1465–1472
Higaki T, Kutsuna N, Sano T et al (2010) Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J 61:156–165
Shimizu S, Kanaseki T, Mizushima N et al (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6:1221–1228
Tsujimoto Y, Shimizu S (2005) Another way to die: autophagic programmed cell death. Cell Death Differ 12(Suppl 2):1528–1534
Patel S, Caplan J, Dinesh-Kumar SP (2006) Autophagy in the control of programmed cell death. Curr Opin Plant Biol 9:391–396
Van Doorn WG, Woltering EJ (2010) What about the role of autophagy in PCD? Trends Plant Sci 15:361–362
Minina EA, Filonova LH, Fukada K et al (2013) Autophagy and metacaspase determine the mode of cell death in plants. J Cell Biol 203:917–927
Teh OK, Hofius D (2014) Membrane trafficking and autophagy in pathogen-triggered cell death and immunity. J Exp Bot 65:1297–1312
Gump JM, Thorburn A (2011) Autophagy and apoptosis: what is the connection? Trends Cell Biol 21:387–392
Tsukamoto S, Kuma A, Murakami M et al (2008) Autophagy is essential for preimplantation development of mouse embryos. Science 321:117–120
Meléndez A, Levine B (2009) Autophagy in C. elegans. In: Kramer JM, Moerman DC (eds) WormBook
Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147:728–741
Kurusu T, Koyano T, Hanamata S et al (2014) OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. Autophagy 10:878–888
Hanamata S, Kurusu T, Okada M et al (2013) In vivo imaging and quantitative monitoring of autophagic flux in tobacco BY-2 cells. Plant Signal Behav 8:e22510
Barna B, Györgyi B (1992) Resistance of young versus old tobacco leaves to necrotrophs, fusaric acid, cell wall-degrading enzymes and autolysis of membrane lipids. Physiol Mol Plant Pathol 40:247–257
Bailey BA, Avni A, Andersen JD (1995) The influence of ethylene and tissue age on the sensitivity of Xanthi tobacco leaves to a Trichoderma viride xylanase. Plant Cell Physiol 36:1669–1676
Nagata T, Takebe I (1970) Cell wall regeneration and cell division in isolated tobacco mesophyll protoplasts. Planta 92:301–308
Ricci P, Bonnet P, Huet JC et al (1989) Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. Eur J Biochem 183:555–563
Menges M, Hennig L, Gruissem W et al (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol 53:423–442
Bao Z, Yang H, Hua J (2013) Perturbation of cell cycle regulation triggers plant immune response via activation of disease resistance genes. Proc Natl Acad Sci U S A 110:2407–2412
Sanchez Mde L, Caro E, Desvoyes B et al (2008) Chromatin dynamics during the plant cell cycle. Semin Cell Dev Biol 19:537–546
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Kurusu, T., Higaki, T., Kuchitsu, K. (2015). Programmed Cell Death in Plant Immunity: Cellular Reorganization, Signaling, and Cell Cycle Dependence in Cultured Cells as a Model System. In: Gunawardena, A.N., McCabe, P.F. (eds) Plant Programmed Cell Death. Springer, Cham. https://doi.org/10.1007/978-3-319-21033-9_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-21033-9_4
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-21032-2
Online ISBN: 978-3-319-21033-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)