Abstract
Embryogenesis is a fascinating event during the plant life cycle encompassing several steps whereby the zygote develops into a fully developed embryo which, in angiosperms, is composed of an axis separating the apical meristems, and two cotyledons. Recapitulation of embryogenesis can also occur in vitro through somatic embryogenesis, where somatic cells are induced to form embryos, and androgenesis, in which embryos originate from immature male gametophytes. Besides cell division and differentiation, embryo patterning in vivo and in vitro requires the dismantling and selective elimination of cells and tissues via programmed cell death (PCD). While the manifestation of the death program has long been acknowledged in vivo, especially in relation to the elimination of the suspensor during the late phases of embryo development, PCD during in vitro embryogenesis has only been described in more recent years. Independent studies using the gymnosperm Norway spruce and the angiosperm maize have shown that the death program is crucial for the proper formation and further development of immature somatic embryos. This chapter summarizes the recent advances in the field of PCD during embryogenesis and proposes novel regulatory mechanisms activating the death program in plants.
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Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nuñez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G (2008) Classification of cell death: recommendations of the nomenclature Committee on Cell Death 2009. Cell Death Differ 16:3–11
Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36:2405–2419
Greenberg JT (1996) Programmed cell death: a way of life for plants. Proc Natl Acad Sci U S A 93:12094–12097
Reape T, Molony FM, McCabe MC (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59:435–444
van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:1241–1246
Christofferson DE, Yuan J (2010) Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol 22:263–268
Hara-Nishimura I, Hatsugai N (2011) The role of vacuole in plant cell death. Cell Death Differ 18:1298–1304
Kundu M, Thompson CB (2005) Macroautophagy versus mitochondrial autophagy: a question of fate? Cell Death Differ 12:1484–1489
Gunawardena AH, Pearce MB, Jackson CD, Haves CR, Evans DE (2001) Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize (Zea mays L.) promoted by ethylene. Plant Cell Env 24:1369–1375
Webb J, Jackson MB (1986) A transmission and cryo-scanning electron microscopy study of the formation of aerenchyma (cortical gas-filled space) in adventitious roots of rice (Oryza sativa). J Exp Bot 37:832–841
Arends MJ, Morris RG, Wyllie AH (1990) Apoptosis. the role of the endonuclease. Am J Pathol 136:593–608
Peitsch MC, Polzar B, Stephan H (1993) Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death). EMBO J 12:371–377
Widłak P, Garrard WT (2005) Discovery, regulation, and action of the major apoptotic nucleases DFF40/CAD and endonuclease G. J Cell Biochem 94:1078–1087
Eleftheriou EP (1986) Ultrastructural studies on protophloem sieve elements in Triticum aestivum L. nuclear degeneration. J Ultrast Mol Struct Res 95:47–60
Schussler EE, Longstreth DJ (2000) Changes in cell structure during the formation of root aerenchyma in Sagittaria lancifolia (Alismataceae). Am J Bot 87:12–19
Kermode AR (1990) Regulatory mechanisms involved in the transition from seed development to germination. Crit Rev Plant Sci 2:155–195
Touraev A, Pfosser M, Heberle-Bors E (2001) The microspore: a haploid multipurpose cell. Adv Bot Res 35:53–109
Bozhkov PV, Filonova LH, von Arnold S (2002) A key developmental switch during Norway spruce somatic embryogenesis is induced by withdrawal of growth regulators and associated with cell death and extracellular acidification. Biotechnol Bioeng 77:658–667
Sreenivasulu N, Wobus U (2013) Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol 64:189–217
Raghavan V. (2001) Life and times of the suspensor of angiosperm embryos. Trends Plant Sci Phytomorphology Golden Jubilee Issue, 251–276
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamman T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153
Bozhkov PV, Filonova LH, Suarez MF (2005) Programmed cell death in plant embryogenesis. Curr Topics Dev Biol 67:135–179
Kawashima T, Goldberg RB (2010) The suspensor: not just suspending the embryo. Trends Plant Sci 15:23–30
Lersten NR (1983) Suspensors in Leguminosae. Bot Rev 49:233–257
Lombardi L, Ceccarelli N, Picciarelli P, Lorenzi R (2007) DNA degradation during programmed cell death in Phaseolus coccineus suspensor. Plant Physiol Biochem 45:221–227
Giuliani C, Consonni G, Gavazzi G, Colombo M, Dolfini S (2002) Programmed cell death during embryogenesis in maize. Annals Bot 90:287–292
Marsden MPF, Meinke DW (1985) Abnormal development of the suspensor in an embryo-lethal mutant of Arabidopsis thaliana. Am J Bot 72:1801–1812
Vernon DM, Meinke DW (1994) Embryogenic transformation of the suspensor in twin, a polyembryonic mutant of Arabidopsis. Dev Biol 165:566–573
Håkansson A (1956) Seed development in Picea abies and Pinus silvestris. Med fran Statens Skogsforsk 46:1–23
Filonova LH, Bozhkov PV, von Arnold S (2000) Developmental pathway of somatic embryogenesis in Picea abies as revealed by time-lapse tracking. J Exp Bot 51:249–264
Edo Y (2012) Characterization and systematic implications of the diversity in timing of programmed cell death of the suspensors in Leguminosae. Am J Bot 99:1399–1407
Craig SF, Slobodkin LB, Wray GA, Biermann CH (1997) The ‘paradox’ of polyembryony: a review of the cases and a hypothesis for its evolution. Evol Ecol 11:127–143
Singh H (1978) Embryology of gymnosperms. In: Encyclopedia of Plant Anatomy. Gebru¨der Borntraeger, Berlin
Filonova LH, von Arnold S, Daniel S, Bohzkov P (2002) Programmed cell death eliminates all but one embryo in a polyembryonic plant seed. Cell Death Differ 9:1057–1062
Young TE, Gallie DR (2000) Programmed cell death during endosperm development. Plant Mol Biol 44:283–301
Krutovskii KV, Politov DV (1995) Allozyme evidence for polyzygotic polyembryony in Siberian stone pine (Pinus sibirica Du Tour). Theor App Genet 90:811–818
Yan CH, Chen HM, Dai YR (1999) Induction of programmed cell death by menadione in suspension culture of carrot cells. Shi Yan Sheng Wu Xue Bao 32:197–205
Zhou J, Zhu H, Dai Y (1999) Effect of ethrel on apoptosis in carrot protoplasts. Plant Growth Reg 27:119–123
McCabe PF, Levine A, Meijer PJ, Tapon NA, Pennel R (1997) A programmed cell death pathway activated in carrot cells cultured at low cell density. Plant J 12:267–280
van Zyl L, Bozhkov PV, Chapham D, Sederoff R, von Arnold S (2003) Up, down and up again is a signature global gene expression pattern at the beginning of gymnosperm embryogenesis. Gene Expr Patterns 3:83–91
Stasolla C, Bozhkov PV, Chu T-M, Wolfinger RD, Von Arnold S, Sederoff RR (2004) Variation in transcript abundance during somatic embryogenesis in gymnosperms. Tree Physiol 24:1073–1085
White K, Grether ME, Abrams JM (1994) Genetic control of programmed cell death in Drosophila. Science 264:677–683
Smertenko AP, Bozhkov PV, Filonova LH, von Arnold S, Hussey PJ (2003) Reorganization of the cytoskeleton during developmental programmed cell death in Picea abies embryos. Plant J 33:813–824
Touraev A, Vicente O, Heberle-Borse E (1997) Initiation of embryogenesis by stress. Trends Plant Sci 2:297–302
Sunderland N (1974) Anther culture as a means of haploid induction. In: Kasha KJ (ed) Haploids in higher plants: advances and potential. University of Guelph, Canada, pp 91–122
Raghavan V (1986) Pollen embryogenesis. In: Barlow PW, Green PB, Wylie CC (eds) Embryogenesis in angiosperms. Cambridge University Press, Cambridge, pp 153–189
Varnier AL, Mazeyrat-Gourbeyre F, Sangwan RS (2005) Programmed cell death progressively models the development of anther sporophytic tissues from the tapetum and is triggered in pollen grains during maturation. J Struct Biol 152:118–128
Varnier AL, Jacquard C, Clement C (2009) Programmed cell death and microspore embryogenesis. In: Touraev A, Foster BP, Jain SM (eds) Advances in haploid production in higher plants. Springer, Dordrecht, pp 154–176
Caredda S, Doncoeur C, Devaux P, Sangwan RS, Clement C (2000) Plastid differentiation during androgenesis in albino and non-albino producing cultivars of barley (Hordeum vulgare L.). Sex Plant Reprod 13:95–104
Wang M, Hoekstra S, Van Bergen S, Oppedijk BJ, van der Heijden MW, de Priester W, Schilperoort RA (1999) Apoptosis in developing anthers and the role of ABA in this process during androgenesis in Hordeum vulgare. Plant Mol Biol 39:489–501
Maraschin SF, Caspers M, Potokina E, Wulfert F, Graner A, Spaink HP, Wang M (2006) cDNA array analysis of stress-induced gene expression in barley androgenesis. Physiol Plant 127:535–550
Joosen R, Cordewener J, Supena EDJ, Vorst O, Lammers M, Maliepaard C, Zeilmaker T, Miki B, America T, Custers J, Boutilier K (2007) Combined transcriptome and proteome analysis identifies pathways and markers associated with the establishment of rapeseed microspore-derived embryo development. Plant Physiol 144:155–172
Malik MR, Wang F, Dirpaul JM, Zhou N, Polowick PL, Ferrie AM, Krochko JE (2007) Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus. Plant Physiol 144:134–154
Rodriguez-Serrano M, Barany I, Prem D, Coronado M-S, Risueno MC, Testillano PS (2012) NO, ROS, and cell death associated with caspase-like activity increase in stress-induced microspore embryogenesis of barley. J Exp Bot 63:2007–2014
Maraschin SF, de Priester W, Spaink HP, Wang N (2005) Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56:1711–1726
Watanabe N, Lam E (2004) Recent advance in the study of caspase-like proteases and Bax inhibitor-1 in plants: Their possible roles as regulator of programmed cell death. Mol Plant Pathol 5:65–70
Xu Q, Reed JC (1998) Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell 1:337–346
Coupe SA, Watson LM, Ryan DJ, Pinkney TT, Eason JR (2004) Molecular analysis of programmed cell death during senescence in Arabidopsis thaliana and Brassica oleracea: cloning broccoli LSD1, Bax inhibitor and serine palmitoyltransferase homologues. J Exp Bot 55:59–60
Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5:305–315
Kawai-Yamada M, Ohmori Y, Uchimiya H (2004) Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell 16:21–32
Bolduc N, Brisson LF (2002) Antisense down regulation of NtBI-1 in tobacco BY-2 cells induces accelerated cell death upon carbon starvation. FEBS Lett 532:111–114
Csala M, Banhegyi G, Benedetti A (2006) Endoplasmic reticulum: a metabolic compartment. FEBS Lett 580:2160–2165
Ihara-Ohori Y, Nagano M, Muto S, Uchimiya H, Kawai-Yamanda M (2007) Cell death suppressor Arabidopsis Bax inhibitor-1 is associated with calmodulin binding and ion homeostasis. Plant Physiol 143:650–660
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
Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516
Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1–16
Rai NK, Tripathi K, Sharma D, Shukla VK (2005) Apoptosis: a basic physiologic process in wound healing. Int J Low Extrem Wounds 4:138–144
Uren AG, O’Rourke K, Aravind L, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins one of which plays a key role in MALT lymphoma. Mol Cell 6:961–967
Madeo F, Herker E, Maldener C, Wissing S, Lächelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Fröhlich KU (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917
Suarez MF, Filonova LH, Smertenko EI, Savenkov EI, Clapham DH, von Arnold S, Zhivotovsky B, Bozhkov PV (2004) Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr Biol 14:R339–R340
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 organogenesis. Proc Natl Acad Sci U S A 102:14463–14468
Hill RD (2012) Non-symbiotic haemoglobins - What’s happening beyond nitric oxide scavenging? AoB Plants 2012 doi:10.1093/aobpla/pls004
Brune B (2003) Nitric oxide: NO apoptosis or turning it ON? Cell Death Differ 10:864–869
Hill RD, Huang S, Stasolla C (2013) Hemoglobins, programmed cell death and somatic embryogenesis. Plant Sci 211:35–41
Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inzé D, Delledonne M, Van Breusegem F (2007) Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol Chem 282:1352–1358
Blaise GA, Gauvin D, Gangal M, Authier S (2005) Nitric oxide, cell signaling and cell death. Toxicol 208:177–192
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39
Wang Y, Chen C, Loake GJ, Chu C (2010) Nitric oxide: promoter or suppressor of programmed cell death? Protein Cell 1:133–142
Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ (2000) No way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J 24:667–677
Elhiti M, Hebelstrup K, Wang A, Li C, Cui Y, Hill RD, Stasolla C (2013) Function of the type-2 Arabidopsis hemoglobin in the auxin-mediated formation of embryogenic cells during morphogenesis. Plant J 74:946–958
Huang S, Wally O, Hill RD, Dionisio G, Aylele B, Stasolla C (2014) Hemoglobin control of cell survival/death decision regulates in vitro plant morphogenesis. Plant Physiol 165:810–825
Aravindakumar CT, Ceulemans J, De LM (1999) Nitric oxide induces Zn2+ release from metallothionein by destroying zinc-sulphur clusters without concomitant formation of S-nitrosothiol. Biochem J 344:253–258
Helmersson A, von Arnold S, Bozhkov PV (2008) The level of free intracellular zinc mediates programmed cell death/cell survival decisions in plant embryos. Plant Physiol 147:1158–1167
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Huang, S., Mira, M.M., Stasolla, C. (2016). Dying with Style: Death Decision in Plant Embryogenesis. In: Germana, M., Lambardi, M. (eds) In Vitro Embryogenesis in Higher Plants. Methods in Molecular Biology, vol 1359. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-3061-6_5
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DOI: https://doi.org/10.1007/978-1-4939-3061-6_5
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