Advertisement

Dying with Style: Death Decision in Plant Embryogenesis

  • Shuanglong Huang
  • Mohamed M. Mira
  • Claudio Stasolla
Part of the Methods in Molecular Biology book series (MIMB, volume 1359)

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.

Key words

Androgenesis Embryogenesis Hemoglobins Programmed cell death Somatic embryogenesis 

References

  1. 1.
    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 16:3–11PubMedCentralCrossRefPubMedGoogle Scholar
  2. 2.
    Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36:2405–2419CrossRefPubMedGoogle Scholar
  3. 3.
    Greenberg JT (1996) Programmed cell death: a way of life for plants. Proc Natl Acad Sci U S A 93:12094–12097PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Reape T, Molony FM, McCabe MC (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59:435–444CrossRefPubMedGoogle Scholar
  5. 5.
    van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:1241–1246CrossRefGoogle Scholar
  6. 6.
    Christofferson DE, Yuan J (2010) Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol 22:263–268PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Hara-Nishimura I, Hatsugai N (2011) The role of vacuole in plant cell death. Cell Death Differ 18:1298–1304PubMedCentralCrossRefPubMedGoogle Scholar
  8. 8.
    Kundu M, Thompson CB (2005) Macroautophagy versus mitochondrial autophagy: a question of fate? Cell Death Differ 12:1484–1489CrossRefPubMedGoogle Scholar
  9. 9.
    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 24:1369–1375CrossRefGoogle Scholar
  10. 10.
    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 37:832–841CrossRefGoogle Scholar
  11. 11.
    Arends MJ, Morris RG, Wyllie AH (1990) Apoptosis. the role of the endonuclease. Am J Pathol 136:593–608PubMedCentralPubMedGoogle Scholar
  12. 12.
    Peitsch MC, Polzar B, Stephan H (1993) Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death). EMBO J 12:371–377PubMedCentralPubMedGoogle Scholar
  13. 13.
    Widłak P, Garrard WT (2005) Discovery, regulation, and action of the major apoptotic nucleases DFF40/CAD and endonuclease G. J Cell Biochem 94:1078–1087CrossRefPubMedGoogle Scholar
  14. 14.
    Eleftheriou EP (1986) Ultrastructural studies on protophloem sieve elements in Triticum aestivum L. nuclear degeneration. J Ultrast Mol Struct Res 95:47–60CrossRefGoogle Scholar
  15. 15.
    Schussler EE, Longstreth DJ (2000) Changes in cell structure during the formation of root aerenchyma in Sagittaria lancifolia (Alismataceae). Am J Bot 87:12–19CrossRefPubMedGoogle Scholar
  16. 16.
    Kermode AR (1990) Regulatory mechanisms involved in the transition from seed development to germination. Crit Rev Plant Sci 2:155–195CrossRefGoogle Scholar
  17. 17.
    Touraev A, Pfosser M, Heberle-Bors E (2001) The microspore: a haploid multipurpose cell. Adv Bot Res 35:53–109CrossRefGoogle Scholar
  18. 18.
    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 77:658–667CrossRefPubMedGoogle Scholar
  19. 19.
    Sreenivasulu N, Wobus U (2013) Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol 64:189–217CrossRefPubMedGoogle Scholar
  20. 20.
    Raghavan V. (2001) Life and times of the suspensor of angiosperm embryos. Trends Plant Sci Phytomorphology Golden Jubilee Issue, 251–276Google Scholar
  21. 21.
    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 426:147–153CrossRefPubMedGoogle Scholar
  22. 22.
    Bozhkov PV, Filonova LH, Suarez MF (2005) Programmed cell death in plant embryogenesis. Curr Topics Dev Biol 67:135–179CrossRefGoogle Scholar
  23. 23.
    Kawashima T, Goldberg RB (2010) The suspensor: not just suspending the embryo. Trends Plant Sci 15:23–30CrossRefPubMedGoogle Scholar
  24. 24.
    Lersten NR (1983) Suspensors in Leguminosae. Bot Rev 49:233–257CrossRefGoogle Scholar
  25. 25.
    Lombardi L, Ceccarelli N, Picciarelli P, Lorenzi R (2007) DNA degradation during programmed cell death in Phaseolus coccineus suspensor. Plant Physiol Biochem 45:221–227CrossRefPubMedGoogle Scholar
  26. 26.
    Giuliani C, Consonni G, Gavazzi G, Colombo M, Dolfini S (2002) Programmed cell death during embryogenesis in maize. Annals Bot 90:287–292CrossRefGoogle Scholar
  27. 27.
    Marsden MPF, Meinke DW (1985) Abnormal development of the suspensor in an embryo-lethal mutant of Arabidopsis thaliana. Am J Bot 72:1801–1812CrossRefGoogle Scholar
  28. 28.
    Vernon DM, Meinke DW (1994) Embryogenic transformation of the suspensor in twin, a polyembryonic mutant of Arabidopsis. Dev Biol 165:566–573CrossRefPubMedGoogle Scholar
  29. 29.
    Håkansson A (1956) Seed development in Picea abies and Pinus silvestris. Med fran Statens Skogsforsk 46:1–23Google Scholar
  30. 30.
    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 51:249–264CrossRefPubMedGoogle Scholar
  31. 31.
    Edo Y (2012) Characterization and systematic implications of the diversity in timing of programmed cell death of the suspensors in Leguminosae. Am J Bot 99:1399–1407CrossRefGoogle Scholar
  32. 32.
    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 11:127–143CrossRefGoogle Scholar
  33. 33.
    Singh H (1978) Embryology of gymnosperms. In: Encyclopedia of Plant Anatomy. Gebru¨der Borntraeger, BerlinGoogle Scholar
  34. 34.
    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 9:1057–1062CrossRefPubMedGoogle Scholar
  35. 35.
    Young TE, Gallie DR (2000) Programmed cell death during endosperm development. Plant Mol Biol 44:283–301CrossRefPubMedGoogle Scholar
  36. 36.
    Krutovskii KV, Politov DV (1995) Allozyme evidence for polyzygotic polyembryony in Siberian stone pine (Pinus sibirica Du Tour). Theor App Genet 90:811–818CrossRefGoogle Scholar
  37. 37.
    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 32:197–205PubMedGoogle Scholar
  38. 38.
    Zhou J, Zhu H, Dai Y (1999) Effect of ethrel on apoptosis in carrot protoplasts. Plant Growth Reg 27:119–123CrossRefGoogle Scholar
  39. 39.
    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 12:267–280CrossRefGoogle Scholar
  40. 40.
    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 3:83–91CrossRefPubMedGoogle Scholar
  41. 41.
    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 24:1073–1085CrossRefPubMedGoogle Scholar
  42. 42.
    White K, Grether ME, Abrams JM (1994) Genetic control of programmed cell death in Drosophila. Science 264:677–683CrossRefPubMedGoogle Scholar
  43. 43.
    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 33:813–824CrossRefPubMedGoogle Scholar
  44. 44.
    Touraev A, Vicente O, Heberle-Borse E (1997) Initiation of embryogenesis by stress. Trends Plant Sci 2:297–302CrossRefGoogle Scholar
  45. 45.
    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 91–122Google Scholar
  46. 46.
    Raghavan V (1986) Pollen embryogenesis. In: Barlow PW, Green PB, Wylie CC (eds) Embryogenesis in angiosperms. Cambridge University Press, Cambridge, pp 153–189Google Scholar
  47. 47.
    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 152:118–128CrossRefPubMedGoogle Scholar
  48. 48.
    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 154–176Google Scholar
  49. 49.
    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 13:95–104CrossRefGoogle Scholar
  50. 50.
    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 39:489–501CrossRefPubMedGoogle Scholar
  51. 51.
    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 127:535–550CrossRefGoogle Scholar
  52. 52.
    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 144:155–172PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    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 144:134–154PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    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 63:2007–2014PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    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 56:1711–1726CrossRefPubMedGoogle Scholar
  56. 56.
    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 5:65–70CrossRefPubMedGoogle Scholar
  57. 57.
    Xu Q, Reed JC (1998) Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell 1:337–346CrossRefPubMedGoogle Scholar
  58. 58.
    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 55:59–60CrossRefPubMedGoogle Scholar
  59. 59.
    Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5:305–315CrossRefPubMedGoogle Scholar
  60. 60.
    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 16:21–32PubMedCentralCrossRefPubMedGoogle Scholar
  61. 61.
    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 532:111–114CrossRefPubMedGoogle Scholar
  62. 62.
    Csala M, Banhegyi G, Benedetti A (2006) Endoplasmic reticulum: a metabolic compartment. FEBS Lett 580:2160–2165CrossRefPubMedGoogle Scholar
  63. 63.
    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 143:650–660PubMedCentralCrossRefPubMedGoogle Scholar
  64. 64.
    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 30:1173–1183PubMedCentralCrossRefPubMedGoogle Scholar
  65. 65.
    Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516PubMedCentralCrossRefPubMedGoogle Scholar
  66. 66.
    Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1–16PubMedCentralCrossRefPubMedGoogle Scholar
  67. 67.
    Rai NK, Tripathi K, Sharma D, Shukla VK (2005) Apoptosis: a basic physiologic process in wound healing. Int J Low Extrem Wounds 4:138–144CrossRefPubMedGoogle Scholar
  68. 68.
    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 6:961–967PubMedGoogle Scholar
  69. 69.
    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 9:911–917CrossRefPubMedGoogle Scholar
  70. 70.
    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–R340CrossRefPubMedGoogle Scholar
  71. 71.
    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 102:14463–14468PubMedCentralCrossRefPubMedGoogle Scholar
  72. 72.
    Hill RD (2012) Non-symbiotic haemoglobins - What’s happening beyond nitric oxide scavenging? AoB Plants 2012 doi:10.1093/aobpla/pls004Google Scholar
  73. 73.
    Brune B (2003) Nitric oxide: NO apoptosis or turning it ON? Cell Death Differ 10:864–869CrossRefPubMedGoogle Scholar
  74. 74.
    Hill RD, Huang S, Stasolla C (2013) Hemoglobins, programmed cell death and somatic embryogenesis. Plant Sci 211:35–41CrossRefPubMedGoogle Scholar
  75. 75.
    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 282:1352–1358CrossRefPubMedGoogle Scholar
  76. 76.
    Blaise GA, Gauvin D, Gangal M, Authier S (2005) Nitric oxide, cell signaling and cell death. Toxicol 208:177–192CrossRefGoogle Scholar
  77. 77.
    Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39CrossRefPubMedGoogle Scholar
  78. 78.
    Wang Y, Chen C, Loake GJ, Chu C (2010) Nitric oxide: promoter or suppressor of programmed cell death? Protein Cell 1:133–142CrossRefPubMedGoogle Scholar
  79. 79.
    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 24:667–677CrossRefPubMedGoogle Scholar
  80. 80.
    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 74:946–958CrossRefPubMedGoogle Scholar
  81. 81.
    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 165:810–825PubMedCentralCrossRefPubMedGoogle Scholar
  82. 82.
    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 344:253–258PubMedCentralPubMedGoogle Scholar
  83. 83.
    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 147:1158–1167PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Shuanglong Huang
    • 1
  • Mohamed M. Mira
    • 2
  • Claudio Stasolla
    • 1
  1. 1.Department of Plant ScienceUniversity of ManitobaWinnipegCanada
  2. 2.Department of Botany, Faculty of ScienceTanta UniversityTantaEgypt

Personalised recommendations