Skip to main content
SpringerLink
Log in

Control of Programmed Cell Death During Plant Reproductive Development

  • Chapter
  • First Online:
Biocommunication of Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 14))

Abstract

Programmed cell death (PCD) is an actively controlled, genetically encoded self-destruct mechanism of the cell. While many forms of PCD have been described and molecularly dissected in animals, we know to date only little about the control of PCD processes in plants. Nevertheless, plant PCD is a crucial component of a plant’s reaction to its biotic and abiotic environment and a central theme during plant development. In this chapter, we review the communication events triggering and executing, or preventing, PCD during plant reproductive development. These comprise intracellular communication, as well as signaling between cells and tissues, and the intricate communication between genetically distinct individuals that are necessary for successful plant reproduction.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Antonsson B, Conti F, Ciavatta A, Montessuit S, Lewis S, Martinou I, Bernasconi L, Bernard A, Mermod JJ, Mazzei G, Maundrell K, Gambale F, Sadoul R, Martinou JC (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277:370–372

    Article  PubMed  CAS  Google Scholar 

  • Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21:1453–1472

    Article  PubMed  CAS  Google Scholar 

  • Baek D, Nam J, Koo YD, Kim DH, Lee J, Jeong JC, Kwak SS, Chung WS, Lim CO, Bahk JD, Hong JC, Lee SY, Kawai-Yamada M, Uchimiya H, Yun DJ (2004) Bax-induced cell death of Arabidopsis is meditated through reactive oxygen-dependent and -independent processes. Plant Mol Biol 56:15–27

    Article  PubMed  CAS  Google Scholar 

  • Beeckman T, De Rycke R, Viane R, Inzé D (2000) Histological study of seed coat development in Arabidopsis thaliana. J Plant Res 113:139–148

    Article  Google Scholar 

  • Beers EP, Woffenden BJ, Zhao C (2000) Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol Biol 44:399–415

    Article  PubMed  CAS  Google Scholar 

  • Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650

    Article  PubMed  CAS  Google Scholar 

  • Berger F (2003) Endosperm: the crossroad of seed development. Curr Opin Plant Biol 6:42–50

    Article  PubMed  CAS  Google Scholar 

  • Berger F, Grini PE, Schnittger A (2006) Endosperm: an integrator of seed growth and development. Curr Opin Plant Biol 9:664–670

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Jones RL (2000) Vacuoles and prevacuolar compartments. Curr Opin Plant Biol 3:469–475

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Jones RL (2001) Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J 25:19–29

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Lonsdale JE, Fath A, Jones RL (1999) Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell 11:1033–1046

    PubMed  CAS  Google Scholar 

  • Bethke PC, Fath A, Spiegel YN, Hwang Y, Jones RL (2002) Abscisic acid, gibberellin and cell viability in cereal aleurone. Euphytica 126:3–11

    Article  CAS  Google Scholar 

  • Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Libourel IG, Aoyama N, Chung YY, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143:1173–1188

    Article  PubMed  CAS  Google Scholar 

  • Bewley JD, Black M (1994) Seeds: physiology of development and germination. Plenum Publishing, New York

    Google Scholar 

  • Birchler JA (1993) Dosage analysis of maize endosperm development. Annu Rev Genet 27:181–204

    Article  PubMed  CAS  Google Scholar 

  • Blanvillain R, Young B, Cai YM, Hecht V, Varoquaux F, Delorme V, Lancelin JM, Delseny M, Gallois P (2011) The Arabidopsis peptide kiss of death is an inducer of programmed cell death. EMBO J 30:1173–1183

    Article  PubMed  CAS  Google Scholar 

  • Boren M, Hoglund AS, Bozhkov P, Jansson C (2006) Developmental regulation of a VEIDase caspase-like proteolytic activity in barley caryopsis. J Exp Bot 57:3747–3753

    Article  PubMed  CAS  Google Scholar 

  • Bosch M, Franklin-Tong VE (2008) Self-incompatibility in papaver: signalling to trigger PCD in incompatible pollen. J Exp Bot 59:481–490

    Article  PubMed  CAS  Google Scholar 

  • Bosch M, Poulter NS, Vatovec S, Franklin-Tong VE (2008) Initiation of programmed cell death in self-incompatibility: role for cytoskeleton modifications and several caspase-like activities. Mol Plant 1:879–887

    Article  PubMed  CAS  Google Scholar 

  • Bozhkov PV, Filonova LH, Suarez MF, Helmersson A, Smertenko AP, Zhivotovsky B, von Arnold S (2004) VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Differ 11:175–182

    Article  PubMed  CAS  Google Scholar 

  • Bozhkov PV, Suarez MF, Filonova LH, Daniel G, Zamyatnin AA Jr, Rodriguez-Nieto S, Zhivotovsky B, Smertenko A (2005) Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis. Proc Natl Acad Sci USA 102:14463–14468

    Article  PubMed  CAS  Google Scholar 

  • Bozhkov PV, Smertenko AP, Zhivotovsky B (2010) Aspasing out metacaspases and caspases: proteases of many trades. Sci Signal 3:pe48

    Article  PubMed  CAS  Google Scholar 

  • Cacas JL (2010) Devil inside: does plant programmed cell death involve the endomembrane system? Plant Cell Environ 33:1453–1473

    PubMed  CAS  Google Scholar 

  • Chen G, Zhang B, Zhao Z, Sui Z, Zhang H, Xue Y (2010) ‘A life or death decision’ for pollen tubes in S-RNase-based self-incompatibility. J Exp Bot 61:2027–2037

    Article  PubMed  CAS  Google Scholar 

  • Christensen CA, Subramanian S, Drews GN (1998) Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev Biol 202:136–151

    Article  PubMed  CAS  Google Scholar 

  • Christensen CA, Gorsich SW, Brown RH, Jones LG, Brown J, Shaw JM, Drews GN (2002) Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell 14:2215–2232

    Article  PubMed  CAS  Google Scholar 

  • Costa LM, Gutierrez-Marcos JF, Dickinson HG (2004) More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci 9:507–514

    Article  PubMed  CAS  Google Scholar 

  • Dahiya P (2003) Role of death in providing lifeline to plants. Trends Plant Sci 8:462–465

    Article  PubMed  CAS  Google Scholar 

  • Dominguez F, Moreno J, Cejudo FJ (2001) The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development. Planta 213:352–360

    Article  PubMed  CAS  Google Scholar 

  • Dominguez F, Moreno J, Cejudo FJ (2004) A gibberellin-induced nuclease is localized in the nucleus of wheat aleurone cells undergoing programmed cell death. J Biol Chem 279:11530–11536

    Article  PubMed  CAS  Google Scholar 

  • Dresselhaus T (2006) Cell–cell communication during double fertilization. Curr Opin Plant Biol 9:41–47

    Article  PubMed  CAS  Google Scholar 

  • Duchniewicz M, Germaniuk A, Westermann B, Neupert W, Schwarz E, Marszalek J (1999) Dual role of the mitochondrial chaperone Mdj1p in inheritance of mitochondrial DNA in yeast. Mol Cell Biol 19:8201–8210

    PubMed  CAS  Google Scholar 

  • Fath A, Bethke PC, Jones RL (1999) Barley aleurone cell death is not apoptotic: characterization of nuclease activities and DNA degradation. Plant J 20:305–315

    Article  CAS  Google Scholar 

  • Fath A, Bethke P, Lonsdale J, Meza-Romero R, Jones R (2000) Programmed cell death in cereal aleurone. Plant Mol Biol 44:255–266

    Article  PubMed  CAS  Google Scholar 

  • Fath A, Bethke PC, Jones RL (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156–166

    Article  PubMed  CAS  Google Scholar 

  • Fath A, Bethke P, Beligni V, Jones R (2002) Active oxygen and cell death in cereal aleurone cells. J Exp Bot 53:1273–1282

    Article  PubMed  CAS  Google Scholar 

  • Faure JE, Rotman N, Fortune P, Dumas C (2002) Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 30:481–488

    Article  PubMed  Google Scholar 

  • Gadjev I, Stone JM, Gechev TS (2008) Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. Int Rev Cell Mol Biol 270:87–144

    Article  PubMed  CAS  Google Scholar 

  • Gilroy S, Jones RL (1992) Gibberellic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc Natl Acad Sci USA 89:3591–3595

    Article  PubMed  CAS  Google Scholar 

  • Giuliani C, Consonni G, Gavazzi G, Colombo M, Dolfini S (2002) Programmed cell death during embryogenesis in maize. Ann Bot (Lond) 90:287–292

    Article  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229

    PubMed  CAS  Google Scholar 

  • Greenwood JS, Helm M, Gietl C (2005) Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during ricinus seed development. Proc Natl Acad Sci USA 102:2238–2243

    Article  PubMed  CAS  Google Scholar 

  • Gross-Hardt R, Kagi C, Baumann N, Moore JM, Baskar R, Gagliano WB, Jurgens G, Grossniklaus U (2007) LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol 5:e47

    Article  PubMed  CAS  Google Scholar 

  • Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C (2010) Senescence and death of plant organs: nutrient recycling and developmental regulation. C R Biol 333:382–391

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hamamura Y, Saito C, Awai C, Kurihara D, Miyawaki A, Nakagawa T, Kanaoka MM, Sasaki N, Nakano A, Berger F, Higashiyama T (2011) Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana. Curr Biol 21:497–502

    Article  PubMed  CAS  Google Scholar 

  • Hara-Nishimura I, Hatsugai N (2011) The role of vacuole in plant cell death. Cell Death Differ 18:1298–1304

    Article  PubMed  CAS  Google Scholar 

  • Harper JL, Lovell PH, Moore KG (1970) The shapes and sizes of seeds. Ann Rev Ecol Syst 1:327–356

    Article  Google Scholar 

  • Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–858

    Article  PubMed  CAS  Google Scholar 

  • Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11:905–911

    Article  PubMed  CAS  Google Scholar 

  • Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci 10:472–477

    Article  PubMed  CAS  Google Scholar 

  • Hayward AP, Tsao J, Dinesh-Kumar SP (2009) Autophagy and plant innate immunity: defense through degradation. Semin Cell Dev Biol 20:1041–1047

    Article  PubMed  CAS  Google Scholar 

  • Heimovaara-Dijkstra S, Vanduijn B, Libbenga KR, Heidekamp F, Wang M (1994) Abscisic acid-induced membrane potential changes in barley aleurone protoplasts: a possible relevance for the regulation of Rab gene expression. Plant Cell Physiol 35:743–750

    CAS  Google Scholar 

  • Heine GF, Hernandez JM, Grotewold E (2004) Two cysteines in plant R2R3 MYB domains participate in REDOX-dependent DNA binding. J Biol Chem 279:37878–37885

    Article  PubMed  CAS  Google Scholar 

  • Helm M, Schmid M, Hierl G, Terneus K, Tan L, Lottspeich F, Kieliszewski MJ, Gietl C (2008) KDEL-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds. Am J Bot 95:1049–1062

    Article  PubMed  CAS  Google Scholar 

  • Henke N, Lisak DA, Schneider L, Habicht J, Pergande M, Methner A (2011) The ancient cell death suppressor BAX inhibitor-1. Cell Calcium. 2011 Sep;50(3):251–60

    Google Scholar 

  • Higashiyama T (2002) The synergid cell: attractor and acceptor of the pollen tube for double fertilization. J Plant Res 115:149–160

    Article  PubMed  Google Scholar 

  • Higashiyama T (2010) Peptide signaling in pollen–pistil interactions. Plant Cell Physiol 51:177–89

    Article  PubMed  CAS  Google Scholar 

  • Hiratsuka R, Terasaka O (2011) Pollen tube reuses intracellular components of nucellar cells undergoing programmed cell death in pinus densiflora. Protoplasma 248:339–351

    Article  PubMed  Google Scholar 

  • Hiscock SJ, Allen AM (2008) Diverse cell signalling pathways regulate pollen-stigma interactions: the search for consensus. New Phytol 179:286–317

    Article  PubMed  CAS  Google Scholar 

  • Holdsworth MJ, Bentsink L, Soppe WJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54

    Article  PubMed  CAS  Google Scholar 

  • Holloway SJ, Friedman WE (2008) Embryological features of tofieldia glutinosa and their bearing on the early diversification of monocotyledonous plants. Ann Bot 102:167–182

    Article  PubMed  Google Scholar 

  • Huck N, Moore JM, Federer M, Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130:2149–2159

    Article  PubMed  CAS  Google Scholar 

  • Ingram GC (2010) Family life at close quarters: communication and constraint in angiosperm seed development. Protoplasma 247:195–214

    Article  PubMed  Google Scholar 

  • Ishikawa R, Ohnishi T, Kinoshita Y, Eiguchi M, Kurata N, Kinoshita T (2011) Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J 65:798–806

    Article  PubMed  CAS  Google Scholar 

  • Ito T, Nagata N, Yoshiba Y, Ohme-Takagi M, Ma H, Shinozaki K (2007) Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19:3549–3562

    Article  PubMed  CAS  Google Scholar 

  • Ivanov R, Fobis-Loisy I, Gaude T (2010) When no means no: guide to brassicaceae self-incompatibility. Trends Plant Sci 15:387–394

    Article  PubMed  CAS  Google Scholar 

  • Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722

    Article  PubMed  CAS  Google Scholar 

  • Kagi C, Baumann N, Nielsen N, Stierhof YD, Gross-Hardt R (2010) The gametic central cell of Arabidopsis determines the lifespan of adjacent accessory cells. Proc Natl Acad Sci USA 107:22350–22355

    Article  PubMed  CAS  Google Scholar 

  • Kawai-Yamada M, Jin L, Yoshinaga K, Hirata A, Uchimiya H (2001) Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax inhibitor-1 (AtBI-1). Proc Natl Acad Sci USA 98:12295–12300

    Article  PubMed  CAS  Google Scholar 

  • Kawanabe T, Ariizumi T, Kawai-Yamada M, Uchimiya H, Toriyama K (2006) Abolition of the tapetum suicide program ruins microsporogenesis. Plant Cell Physiol 47:784–787

    Article  PubMed  CAS  Google Scholar 

  • Kawashima T, Goldberg RB (2010) The suspensor: not just suspending the embryo. Trends Plant Sci 15:23–30

    Article  PubMed  CAS  Google Scholar 

  • Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330:968–971

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita T (2007) Reproductive barrier and genomic imprinting in the endosperm of flowering plants. Genes Genet Syst 82:177–186

    Article  PubMed  CAS  Google Scholar 

  • Knetsch M, Wang M, Snaar-Jagalska BE, Heimovaara-Dijkstra S (1996) Abscisic acid induces mitogen-activated protein kinase activation in barley aleurone protoplasts. Plant Cell 8:1061–1067

    PubMed  CAS  Google Scholar 

  • Kondou Y, Nakazawa M, Kawashima M, Ichikawa T, Yoshizumi T, Suzuki K, Ishikawa A, Koshi T, Matsui R, Muto S, Matsui M (2008) RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol 147:1924–1935

    Article  PubMed  CAS  Google Scholar 

  • Kubo K, Entani T, Takara A, Wang N, Fields AM, Hua Z, Toyoda M, Kawashima S, Ando T, Isogai A, Kao TH, Takayama S (2010) Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science 330:796–799

    Article  PubMed  CAS  Google Scholar 

  • Kuo A, Cappelluti S, Cervantes-Cervantes M, Rodriguez M, Bush DS (1996) Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells. Plant Cell 8:259–269

    PubMed  CAS  Google Scholar 

  • Larsson E, Sitbon F, von Arnold S (2008) Polar auxin transport controls suspensor fate. Plant Signal Behav 3:469–470

    Article  PubMed  Google Scholar 

  • Lausser A, Dresselhaus T (2010) Sporophytic control of pollen tube growth and guidance in grasses. Biochem Soc Trans 38:631–634

    Article  PubMed  CAS  Google Scholar 

  • Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014

    Article  PubMed  CAS  Google Scholar 

  • Li DH, Yang X, Cui KM (2007a) Formation of archegonium chamber is associated with nucellar-cell programmed cell death in ginkgo biloba. Protoplasma 231:173–181

    Article  PubMed  Google Scholar 

  • Li S, Samaj J, Franklin-Tong VE (2007b) A mitogen-activated protein kinase signals to programmed cell death induced by self-incompatibility in papaver pollen. Plant Physiol 145:236–245

    Article  PubMed  CAS  Google Scholar 

  • Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D (2011a) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630

    Article  PubMed  CAS  Google Scholar 

  • Li X, Gao X, Wei Y, Deng L, Ouyang Y, Chen G, Zhang Q, Wu C (2011b) Rice APOPTOSIS INHIBITOR5 coupled with Two DEAD-Box adenosine 5′-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant Cell 23:1416–1434

    Article  PubMed  CAS  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  PubMed  CAS  Google Scholar 

  • Lombardi L, Casani S, Ceccarelli N, Galleschi L, Picciarelli P, Lorenzi R (2007a) Programmed cell death of the nucellus during sechium edule Sw. Seed development is associated with activation of caspase-like proteases. J Exp Bot 58:2949–2958

    Article  PubMed  CAS  Google Scholar 

  • Lombardi L, Ceccarelli N, Picciarelli P, Lorenzi R (2007b) DNA degradation during programmed cell death in phaseolus coccineus suspensor. Plant Physiol Biochem 45:221–227

    Article  PubMed  CAS  Google Scholar 

  • Lombardi L, Ceccarelli N, Picciarelli P, Sorce C, Lorenzi R (2010) Nitric oxide and hydrogen peroxide involvement during programmed cell death of sechium edule nucellus. Physiol Plant 140:89–102

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Berkowitz GA (2007) The grateful dead: calcium and cell death in plant innate immunity. Cell Microbiol 9:2571–2585

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Sundaresan V (2010) Development of flowering plant gametophytes. Curr Top Dev Biol 91:379–412

    Article  PubMed  CAS  Google Scholar 

  • Madrid EN, Friedman WE (2010) Female gametophyte and early seed development in peperomia (piperaceae). Am J Bot 97:1–14

    Article  PubMed  Google Scholar 

  • Marton ML, Dresselhaus T (2010) Female gametophyte-controlled pollen tube guidance. Biochem Soc Trans 38:627–630

    Article  PubMed  CAS  Google Scholar 

  • Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata S, Kamiya Y, Sun TP (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45:804–818

    Article  PubMed  CAS  Google Scholar 

  • Moll C, von Lyncker L, Zimmermann S, Kagi C, Baumann N, Twell D, Grossniklaus U, Gross-Hardt R (2008) CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J 56:913–921

    Article  PubMed  CAS  Google Scholar 

  • Moller B, Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harb Perspect Biol 1:a001545

    Article  PubMed  CAS  Google Scholar 

  • Morris K, Linkies A, Muller K, Oracz K, Wang X, Lynn JR, Leubner-Metzger G, Finch-Savage WE (2011) Regulation of seed germination in the close Arabidopsis relative lepidium sativum: a global tissue-specific transcript analysis. Plant Physiol 155:1851–1870

    Article  PubMed  CAS  Google Scholar 

  • Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59:501–520

    Article  PubMed  CAS  Google Scholar 

  • Nakaune S, Yamada K, Kondo M, Kato T, Tabata S, Nishimura M, Hara-Nishimura I (2005) A vacuolar processing enzyme, deltaVPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 17:876–887

    Article  PubMed  CAS  Google Scholar 

  • Nowack MK, Ungru A, Bjerkan KN, Grini PE, Schnittger A (2010) Reproductive cross-talk: seed development in flowering plants. Biochem Soc Trans 38:604–612

    Article  PubMed  CAS  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    Article  PubMed  CAS  Google Scholar 

  • Ohashi-Ito K, Fukuda H (2010) Transcriptional regulation of vascular cell fates. Curr Opin Plant Biol 13:670–676

    Article  PubMed  CAS  Google Scholar 

  • Okuda S, Higashiyama T (2010) Pollen tube guidance by attractant molecules: LUREs. Cell Struct Funct 35:45–52

    Article  PubMed  CAS  Google Scholar 

  • Olsen OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16 Suppl:S214–S227

    PubMed  Google Scholar 

  • Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324:1684–1689

    Article  PubMed  CAS  Google Scholar 

  • Palma K, Kermode AR (2003) Metabolism of hydrogen peroxide during reserve mobilization and programmed cell death of barley (hordeum vulgare L.) aleurone layer cells. Free Radic Biol Med 35:1261–1270

    Article  PubMed  CAS  Google Scholar 

  • Papini A, Mosti S, Milocani E, Tani G, Di Falco P, Brighigna L Megasporogenesis and programmed cell death in Tillandsia (Bromeliaceae). Protoplasma, 2011 Oct; 248(4):651–662

    Google Scholar 

  • Penfield S, Graham S, Graham IA (2005) Storage reserve mobilization in germinating oilseeds: Arabidopsis as a model system. Biochem Soc Trans 33:380–383

    Article  PubMed  CAS  Google Scholar 

  • Poulter NS, Wheeler MJ, Bosch M, Franklin-Tong VE (2010) Self-incompatibility in papaver: identification of the pollen S-determinant PrpS. Biochem Soc Trans 38:588–592

    Article  PubMed  CAS  Google Scholar 

  • Qi Y, Wang H, Zou Y, Liu C, Liu Y, Wang Y, Zhang W (2011) Over-expression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Lett 585:231–239

    Article  PubMed  CAS  Google Scholar 

  • Ravi M, Marimuthu MP, Siddiqi I (2008) Gamete formation without meiosis in Arabidopsis. Nature 451:1121–1124

    Article  PubMed  CAS  Google Scholar 

  • Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59:435–444

    Article  PubMed  CAS  Google Scholar 

  • Riggs DR (2004) Programmed cell death events during reproductive development. In: Gray J (ed) Programmed cell death in plants. Blackwell Publishing, Oxford, pp 71–105

    Google Scholar 

  • Ritchie S, Gilroy S (1998) Calcium-dependent protein phosphorylation may mediate the gibberellic acid response in barley aleurone. Plant Physiol 116:765–776

    Article  PubMed  CAS  Google Scholar 

  • Rodkiewicz B (1970) Callose in cell wall during megasporogenesis in angiosperms. Planta 93:39–47

    Article  Google Scholar 

  • Rogers HJ (2005) Cell death and organ development in plants. Curr Top Dev Biol 71:225–261

    Article  PubMed  CAS  Google Scholar 

  • Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure JE (2003) Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 13:432–436

    Article  PubMed  CAS  Google Scholar 

  • Rotman N, Gourgues M, Guitton AE, Faure JE, Berger F (2008) A dialogue between the SIRENE pathway in synergids and the fertilization independent seed pathway in the central cell controls male gamete release during double fertilization in Arabidopsis. Mol Plant 1:659–666

    Article  PubMed  CAS  Google Scholar 

  • Russell SD (1992) Double fertilization. Int Rev Cytol 140:357–388

    Article  Google Scholar 

  • Sabelli PA, Larkins BA (2009) The development of endosperm in grasses. Plant Physiol 149:14–26

    Article  PubMed  CAS  Google Scholar 

  • Sandaklie-Nikolova L, Palanivelu R, King EJ, Copenhaver GP, Drews GN (2007) Synergid cell death in Arabidopsis is triggered following direct interaction with the pollen tube. Plant Physiol 144:1753–1762

    Article  PubMed  CAS  Google Scholar 

  • Scott RJ, Spielman M, Bailey J, Dickinson HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329–3341

    PubMed  CAS  Google Scholar 

  • Shi DQ, Yang WC (2011) Ovule development in Arabidopsis: progress and challenge. Curr Opin Plant Biol 14:74–80

    Article  PubMed  CAS  Google Scholar 

  • Sorensen AM, Krober S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423

    Article  PubMed  CAS  Google Scholar 

  • Sprunck S, Gross-Hardt R (2011) Nuclear behavior, cell polarity, and cell specification in the female gametophyte. Sex Plant Reprod 24:123–136

    Article  PubMed  Google Scholar 

  • Sreenivasulu N, Radchuk V, Strickert M, Miersch O, Weschke W, Wobus U (2006) Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA-regulated maturation in developing barley seeds. Plant J 47:310–327

    Article  PubMed  CAS  Google Scholar 

  • Sreenivasulu N, Borisjuk L, Junker BH, Mock HP, Rolletschek H, Seiffert U, Weschke W, Wobus U (2010) Barley grain development toward an integrative view. Int Rev Cell Mol Biol 281:49–89

    Article  PubMed  CAS  Google Scholar 

  • Sundstrom JF, Vaculova A, Smertenko AP, Savenkov EI, Golovko A, Minina E, Tiwari BS, Rodriguez-Nieto S, Zamyatnin AA Jr, Valineva T, Saarikettu J, Frilander MJ, Suarez MF, Zavialov A, Stahl U, Hussey PJ, Silvennoinen O, Sundberg E, Zhivotovsky B, Bozhkov PV (2009) Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat Cell Biol 11:1347–1354

    Article  PubMed  CAS  Google Scholar 

  • Suomeng D, Zhengguang Z, Xiaobo Z, Yuanchao W (2008) Mammalian pro-apoptotic bax gene enhances tobacco resistance to pathogens. Plant Cell Rep 27:1559–1569

    Article  PubMed  CAS  Google Scholar 

  • Swanson SJ, Jones RL (1996) Gibberellic acid induces vacuolar acidification in barley aleurone. Plant Cell 8:2211–2221

    PubMed  CAS  Google Scholar 

  • Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467–489

    Article  PubMed  CAS  Google Scholar 

  • Tantikanjana T, Nasrallah ME, Nasrallah JB (2010) Complex networks of self-incompatibility signaling in the brassicaceae. Curr Opin Plant Biol 13:520–526

    Article  PubMed  CAS  Google Scholar 

  • Taylor NL, Tan YF, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteomics 72:367–378

    Article  PubMed  CAS  Google Scholar 

  • Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, Bozhkov PV (2011) Metacaspases. Cell Death Differ 18:1279–1288

    Article  PubMed  CAS  Google Scholar 

  • Turner S, Gallois P, Brown D (2007) Tracheary element differentiation. Annu Rev Plant Biol 58:407–433

    Article  PubMed  CAS  Google Scholar 

  • van Doorn WG, Woltering EJ (2008) Physiology and molecular biology of petal senescence. J Exp Bot 59:453–480

    Article  PubMed  CAS  Google Scholar 

  • van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LA, Petersen M, Smertenko A, Taliansky M, Van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246

    Article  PubMed  CAS  Google Scholar 

  • Vartapetian AB, Tuzhikov AI, Chichkova NV, Taliansky M, Wolpert TJ (2011) A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ 18:1289–1297

    Article  PubMed  CAS  Google Scholar 

  • Vizcay-Barrena G, Wilson ZA (2006) Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. J Exp Bot 57:2709–2717

    Article  PubMed  CAS  Google Scholar 

  • Vuosku J, Sutela S, Tillman-Sutela E, Kauppi A, Jokela A, Sarjala T, Haggman H (2009) Pine embryogenesis: many licences to kill for a new life. Plant Signal Behav 4:928–932

    Article  PubMed  CAS  Google Scholar 

  • Wang M, Oppedijk BJ, Lu X, Van Duijn B, Schilperoort RA (1996) Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol Biol 32:1125–1134

    Article  PubMed  CAS  Google Scholar 

  • Wang M, Oppedijk BJ, Caspers MPM, Lamers GEM, Boot MJ, Geerlings DNG, Bakhuizen B, Meijer AH, van Duijn B (1998) Spatial and temporal regulation of DNA fragmentation in the aleurone of germinating barley. J Exp Bot 49:1293–1301

    CAS  Google Scholar 

  • Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45:884–894

    Article  PubMed  CAS  Google Scholar 

  • Watanabe N, Lam E (2009) Bax inhibitor-1, a conserved cell death suppressor, is a key molecular switch downstream from a variety of biotic and abiotic stress signals in plants. Int J Mol Sci 10:3149–3167

    Article  PubMed  CAS  Google Scholar 

  • Wheeler MJ, de Graaf BH, Hadjiosif N, Perry RM, Poulter NS, Osman K, Vatovec S, Harper A, Franklin FC, Franklin-Tong VE (2009) Identification of the pollen self-incompatibility determinant in papaver rhoeas. Nature 459:992–995

    Article  PubMed  CAS  Google Scholar 

  • Wilkins KA, Bancroft J, Bosch M, Ings J, Smirnoff N, Franklin-Tong VE (2011) Reactive oxygen species and nitric oxide mediate actin reorganization and programmed cell death in the self-incompatibility response of papaver. Plant Physiol 156:404–416

    Article  PubMed  CAS  Google Scholar 

  • Williams B, Dickman M (2008) Plant programmed cell death: can’t live with it; can't live without it. Mol Plant Pathol 9:531–544

    Article  PubMed  CAS  Google Scholar 

  • Williams CE, Grotewold E (1997) Differences between plant and animal Myb domains are fundamental for DNA binding activity, and chimeric Myb domains have novel DNA binding specificities. J Biol Chem 272:563–571

    Article  PubMed  CAS  Google Scholar 

  • Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492

    Article  PubMed  CAS  Google Scholar 

  • Woltering EJ (2010) Death proteases: alive and kicking. Trends Plant Sci 15:185–188

    Article  PubMed  CAS  Google Scholar 

  • Wu M, Huang J, Xu S, Ling T, Xie Y, Shen W (2011) Haem oxygenase delays programmed cell death in wheat aleurone layers by modulation of hydrogen peroxide metabolism. J Exp Bot 62:235–248

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Yang C, Yuan Z, Zhang D, Gondwe MY, Ding Z, Liang W, Wilson ZA (2010) The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. Plant Cell 22:91–107

    Article  PubMed  CAS  Google Scholar 

  • Yamada K, Shimada T, Nishimura M, Hara-Nishimura I (2005) A VPE family supporting various vacuolar functions in plants. Physiol Plant 123:369–375

    Article  CAS  Google Scholar 

  • Yamaguchi S, Kamiya Y, Sun T (2001) Distinct cell-specific expression patterns of early and late gibberellin biosynthetic genes during Arabidopsis seed germination. Plant J 28:443–453

    Article  PubMed  CAS  Google Scholar 

  • Yang WC, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev 13:2108–2117

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Johnston N, Talideh E, Mitchell S, Jeffree C, Goodrich J, Ingram G (2008) The endosperm-specific ZHOUPI gene of Arabidopsis thaliana regulates endosperm breakdown and embryonic epidermal development. Development 135:3501–3509

    Article  PubMed  CAS  Google Scholar 

  • Yang WC, Shi DQ, Chen YH (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61:89–108

    Article  PubMed  CAS  Google Scholar 

  • Young TE, Gallie DR (2000a) Programmed cell death during endosperm development. Plant Mol Biol 44:283–301

    Article  PubMed  CAS  Google Scholar 

  • Young TE, Gallie DR (2000b) Regulation of programmed cell death in maize endosperm by abscisic acid. Plant Mol Biol 42:397–414

    Article  PubMed  CAS  Google Scholar 

  • Young TE, Gallie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol 115:737–751

    PubMed  CAS  Google Scholar 

  • Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095

    Article  PubMed  CAS  Google Scholar 

  • Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1:599–610

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Systems Biology, VIB, Ghent, Belgium

    Yadira Olvera-Carrillo, Yuliya Salanenka & Moritz K. Nowack

  2. Department Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium

    Yadira Olvera-Carrillo, Yuliya Salanenka & Moritz K. Nowack

Authors
  1. Yadira Olvera-Carrillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuliya Salanenka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Moritz K. Nowack
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Moritz K. Nowack .

Editor information

Editors and Affiliations

  1. Telos - Philosophische Praxis, Vogelsangstr. 18c, Bürmoos, 5111, Austria

    Günther Witzany

  2. Inst. Zelluläre und Molekulare, Botanik (IZMB), Universität Bonn, Kirschallee 1, Bonn, 53115, Germany

    František Baluška

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Olvera-Carrillo, Y., Salanenka, Y., Nowack, M.K. (2012). Control of Programmed Cell Death During Plant Reproductive Development. In: Witzany, G., Baluška, F. (eds) Biocommunication of Plants. Signaling and Communication in Plants, vol 14. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-23524-5_10

Download citation

Publish with us

Policies and ethics

Search

Navigation