Skip to main content
SpringerLink
Log in

Programmed Cell Death during Formation of the Embryo Sac and Seed

  • REVIEWS
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The process of programmed cell death is essential for plant ontogenesis. Seed development reveals the key role of programmed cell death in cell elimination and formation of new structures. Morphological data and biochemical regulators of programmed cell death during formation of the embryo sac and seed are discussed in the review.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. D’Amato, F., Role of polyploidy in reproductive organs and tissues, in Embryology of Angiosperms, Berlin: Springer, 1984.

    Google Scholar 

  2. An, L.H. and You, R.L., Studies on nuclear degeneration during programmed cell death of synergid and antipodal cells in Triticum aestivum,Sex. Plant Reprod., 2004, vol. 17, no. 4, pp. 195–201.

    Article  Google Scholar 

  3. Bartoli, G., Felici, C., and Castiglione, M.R., Female gametophyte and embryo development in Helleborus bocconei Ten. (Ranunculaceae), Protoplasma, 2017, vol. 254, no. 1, pp. 491–504.

    Article  CAS  PubMed  Google Scholar 

  4. Bethke, P.C. et al., Hormonally regulated programmed cell death in barley aleurone cells, Plant Cell, 1999, vol. 11, no. 6, pp. 1033–1045.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bethke, P.C. and Jones, R.L., Cell death of barley aleurone protoplasts is mediated by reactive oxygen species, Plant J., 2001, vol. 25, no. 1, pp. 19–29.

    Article  CAS  PubMed  Google Scholar 

  6. Bozhkov, P.V. et al., Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis, Proc. Natl. Acad. Sci. U. S. A., 2005, vol. 102, no. 40, pp. 14463–14468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Buhtz, A. et al., Xylem sap protein composition is conserved among different plant species, Planta, 2004, vol. 219, no. 4, pp. 610–618.

    Article  CAS  PubMed  Google Scholar 

  8. Cao, L. et al., Arabidopsis ICK/KRP cyclin-dependent kinase inhibitors function to ensure the formation of one megaspore mother cell and one functional megaspore per ovule, PLoS Genet., 2018, vol. 14, no. 3, pp. 1–30.

    Google Scholar 

  9. Chaban, I.A. et al., Antipodal complex development in the embryo sac of wheat, Russ. J. Dev. Biol., 2011, vol. 42, no. 2, pp. 79–91.

    Article  CAS  Google Scholar 

  10. Chaubal, R. and Reger, B.J., The dynamics of calcium distribution in the synergid cells of wheat after pollination, Sex. Plant Reprod., 1992a, vol. 5, no. 3, pp. 206–213.

    Google Scholar 

  11. Chaubal, R. and Reger, B.J., Calcium in the synergid cells and other regions of pearl millet ovaries, Sex. Plant Reprod., 1992b, vol. 5, no. 1, pp. 34–46.

    Article  Google Scholar 

  12. Chaubal, R. and Reger, B.J., Prepollination degeneration in mature synergids of pearl millet: an examination using antimonate fixation to localize calcium, Sex. Plant Reprod., 1993, vol. 6, no. 4, pp. 225–238.

    Article  Google Scholar 

  13. Chen, Y. et al., Programmed cell death in wheat starchy endosperm during kernel development, Afr. J. Agric. Res., 2012, vol. 7, no. 49, pp. 6533–6540.

    Article  Google Scholar 

  14. Cheng, X.X. et al., Reactive oxygen species regulate programmed cell death progress of endosperm in winter wheat (Triticum aestivum L.) under waterlogging, Protoplasma, 2016, vol. 253, no. 2, pp. 311–327.

    Article  CAS  PubMed  Google Scholar 

  15. Chen, F. and Foolad, M.R., Molecular organization of a gene in barley which encodes a protein similar to aspartic protease and its specific expression in nucellar cells during degeneration, Plant. Mol. Biol., 1997, vol. 35, no. 6, pp. 821–831.

    Article  CAS  PubMed  Google Scholar 

  16. Christensen, C.A. et al., Megagametogenesis in Arabidopsis wild type and the Gf mutant, Sex. Plant Reprod., 1997, vol. 10, no. 1, pp. 49–64.

    Article  Google Scholar 

  17. Christensen, C.A. et al., Mitochondrial GFA2 is required for synergid cell death in Arabidopsis,Plant Cell, 2002, vol. 14, no. 9, pp. 2215–2232.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Consonni, G. et al., Analysis of four maize mutants arrested in early embryogenesis reveals an irregular pattern of cell division, Sex. Plant Reprod., 2003, vol. 15, no. 6, pp. 281–290.

    Article  Google Scholar 

  19. Daneva, A. et al., Functions and regulation of programmed cell death in plant development, Annu. Rev. Cell Dev. Biol., 2016, vol. 32, pp. 441–468.

    Article  CAS  PubMed  Google Scholar 

  20. Demesa-Arévalo, E. and Vielle-Calzada, J.P., The classical arabinogalactan protein AGP18 mediates megaspore selection in Arabidopsis,Plant Cell, 2013, vol. 25, no. 4, pp. 1274–1287.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Denay, G. et al., Endosperm breakdown in Arabidopsis requires heterodimers of the basic helix-loop-helix proteins ZHOUPI and INDUCER OF CBP EXPRESSION 1, Development, 2014, vol. 141, no. 6, pp. 1222–1227.

    Article  CAS  PubMed  Google Scholar 

  22. Domínguez, F. and Cejudo, F.J., Germination-related genes encoding proteolytic enzymes are expressed in the nucellus of developing wheat grains, Plant J., 1998, vol. 15, no. 4, pp. 569–574.

    Article  Google Scholar 

  23. Domínguez, F. and Cejudo, F.J., Programmed cell death (PCD): an essential process of cereal seed development and germination, Front. Plant Sci., 2014, vol. 5, p. 366.

    PubMed  PubMed Central  Google Scholar 

  24. Domínguez, F., Moreno, J., and Cejudo, F.J., The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development, Planta, 2001, vol. 213, no. 3, pp. 352–360.

    Article  PubMed  CAS  Google Scholar 

  25. Domínguez, F., Moreno, J., and Cejudo, F.J., A gibberellin-induced nuclease is localized in the nucleus of wheat aleurone cells undergoing programmed cell death, J. Biol. Chem., 2004, vol. 279, no. 12, pp. 11530–11536.

    Article  PubMed  CAS  Google Scholar 

  26. Van Doorn, W.G., Classes of programmed cell death in plants, compared to those in animals, J. Exp. Bot., 2011a, vol. 62, no. 14, pp. 4749–4761.

    Article  CAS  PubMed  Google Scholar 

  27. Van Doorn, W.G., et al., Morphological classification of plant cell deaths, Cell Death Differ., 2011b, vol. 18, no. 8, pp. 1241–1246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Doronina, T.V., Chaban, I.A., and Lazareva, E.M., Structural and functional features of the wheat embryo sac’s antipodal cells during differentiation, Russ. J. Dev. Biol., 2019, vol. 50, no. 4, pp. 1–17.

    Article  Google Scholar 

  29. Dresselhaus, T., Sprunck, S., and Wessel, G.M., Fertilization mechanisms in flowering plants, Curr. Biol., 2016, vol. 26, no. 3, pp. R125–R139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Engell, K., Embryology of barley. IV. Ultrastructure of the antipodal cells of Hordeum vulgare L. cv. Bomi before and after fertilization of the egg cell, Sex. Plant Reprod., 1994, vol. 7, no. 6, pp. 333–346.

    Article  Google Scholar 

  31. Filonova, L.H. et al., Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce, J. Cell Sci., 2000, vol. 113, no. 24, pp. 4399–4411.

    CAS  PubMed  Google Scholar 

  32. Fu, Y. et al., Changes in actin organization in the living egg apparatus of Torenia fournieri during fertilization, Sex. Plant Reprod., 2000, vol. 12, no. 6, pp. 315–322.

    Article  CAS  Google Scholar 

  33. Galluzzi, L. et al., Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018, Cell Death Differ., 2018, vol. 25, no. 3, pp. 486–541.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Gärtner, P.J. and Nagl, W., Acid phosphatase activity in plastids (plastolysomes) of senescing embryo-suspensor cells, Planta, 1980, vol. 149, no. 4, pp. 341–349.

    Article  PubMed  Google Scholar 

  35. Gietl, C. and Schmid, M., Ricinosomes: an organelle for developmentally regulated programmed cell death in senescing plant tissues, Naturwissenschaften, 2001, vol. 88, no. 2, pp. 49–58.

    Article  CAS  PubMed  Google Scholar 

  36. Giuliani, C. et al., Programmed cell death during embryogenesis in maize, Ann. Bot., 2002, vol. 90, no. 2, pp. 287–292.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Greenwood, J.S., Helm, M., and Gietl, C., Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development, Proc. Natl. Acad. Sci. U. S. A., 2005, vol. 102, no. 6, pp. 2238–2243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hamamura, Y., Nagahara, S., and Higashiyama, T., Double fertilization on the move, Curr. Opin. Plant Biol., 2012, vol. 15, no. 1, pp. 70–77.

    Article  PubMed  Google Scholar 

  39. Hatsugai, N. et al., Vacuolar processing enzyme in plant programmed cell death, Front. Plant Sci., 2015, vol. 6, p. 234.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Van Hautegem, T. et al., Only in dying, life: programmed cell death during plant development, Trends PlantSci., 2015, vol. 20, no. 2, pp. 102–113.

    Article  CAS  PubMed  Google Scholar 

  41. Heydlauff, J. and Groß-Hardt, R., Love is a battlefield: programmed cell death during fertilization, J. Exp. Bot., 2014, vol. 65, no. 5, pp. 1323–1330.

    Article  CAS  PubMed  Google Scholar 

  42. Higashiyama, T. and Takeuchi, H., The mechanism and key molecules involved in pollen tube guidance, Ann. Rev. Plant Biol., 2015, vol. 66, pp. 393–413.

    Article  CAS  Google Scholar 

  43. Hiratsuka, R., Yamada, Y., and Terasaka, O., Programmed cell death of Pinus nucellus in response to pollen tube penetration, J. Plant Res., 2002, vol. 115, no. 2, pp. 0141–0148.

  44. Hofius, D. et al., Role of autophagy in disease resistance and hypersensitive response-associated cell death, Cell Death Differ., 2011, vol. 18, no. 8, pp. 1257–1262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Huang, B.Q. and Russell, S.D., Fertilization in Nicotiana tabacum: cytoskeletal modifications in the embryo sac during synergid degeneration, Planta, 1994, vol. 194, no. 2, pp. 200–214.

    Article  CAS  Google Scholar 

  46. Hunt, D.J.L. and McCabe, P.F., Death and rebirth: programmed cell death during plant sexual reproduction, Mol. Cell Biol. Growth Differ. Plant Cells, 2017, pp. 340–361.

    Google Scholar 

  47. Johri, B.M., Ambegaokar, K.B., and Srivastava, P.S., Comparative Embryology of Angiosperms, Springer Science and Business Media, 2013, vol. 1.

    Google Scholar 

  48. Kacprzyk, J., Daly, C.T., and McCabe, P.F., The botanical dance of death: programmed cell death in plants, Adv. Bot. Res., Academic Press, 2011, vol. 60, pp. 169–261.

  49. Kägi, C. et al., The gametic central cell of Arabidopsis determines the lifespan of adjacent accessory cells, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 51, pp. 22350–22355.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Kawashima, T. and Goldberg, R.B., The suspensor: not just suspending the embryo, Trends Plant Sci., 2010, vol. 15, no. 1, pp. 23–30.

    Article  CAS  PubMed  Google Scholar 

  51. Kessler, S.A. et al., Conserved molecular components for pollen tube reception and fungal invasion, Science, 2010, vol. 330, no. 6006, pp. 968–971.

    Article  CAS  PubMed  Google Scholar 

  52. Kuo, A. et al., Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells, Plant Cell, 1996, vol. 8, no. 2, pp. 259–269.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Leydon, A.R. et al., Pollen tube discharge completes the process of synergid degeneration that is initiated by pollen tube-synergid interaction in Arabidopsis,Plant Physiol., 2015, vol. 169, no. 1, pp. 485–496.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Linnestad, C. et al., Nucellain, a barley homolog of the dicot vacuolar-processing protease, is localized in nucellar cell walls, Plant Physiol., 1998, vol. 118, no. 4, pp. 1169–1180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Locascio, A. et al., Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin, Front. Plant Sci., 2014, vol. 5, p. 412.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Lombardi, L. et al., DNA degradation during programmed cell death in Phaseolus coccineus suspensor, Plant Physiol. Biochem., 2007a, vol. 45, nos. 3–4, pp. 221–227.

    Article  CAS  PubMed  Google Scholar 

  57. Lombardi, L. et al., Programmed cell death of the nucellus during Sechium edule Sw. seed development is associated with activation of caspase-like proteases, J. Exp. Bot., 2007b, vol. 58, no. 11, pp. 2949–2958.

    Article  CAS  PubMed  Google Scholar 

  58. Lombardi, L. et al., Ethylene produced by the endosperm is involved in the regulation of nucellus programmed cell death in Sechium edule Sw, Plant Sci., 2012, vol. 187, pp. 31–38.

    Article  CAS  PubMed  Google Scholar 

  59. López-Fernández, M.P. and Maldonado, S., Ricinosomes provide an early indicator of suspensor and endosperm cells destined to die during late seed development in quinoa (Chenopodium quinoa), Ann. Bot., 2013, vol. 112, no. 7, pp. 1253–1262.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Lu, J. and Magnani, E., Seed tissue and nutrient partitioning, a case for the nucellus, Plant Reprod., 2018, vol. 31, no. 3, pp. 309–317.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Maeda, E. and Miyake, H., Ultrastructure of antipodal cells of rice (Oryza sativa) after anthesis, as related to nutrient transport in embryo sac, Jpn. J. Crop Sci., 1996, vol. 65, no. 2, pp. 340–351.

  62. Maizel, A., A view to a kill: markers for developmentally regulated cell death in plants, Plant Physiol., 2015, vol. 169, no. 4, pp. 2341–2341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Minina, E.A. et al., Autophagy and metacaspase determine the mode of cell death in plants, J. Cell Biol., 2013, vol. 203, no. 6, pp. 917–927.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Mogensen, H.L., Pollen tube–synergid interactions in Proboscidea louisianica (Martineaceae), Am. J. Bot., 1978, vol. 65, no. 9, pp. 953–964.

    Article  Google Scholar 

  65. Nagl, W., The Phaseolus suspensor and its polytene chromosomes, Z. Pflanzenphysiol., 1974, vol. 73, no. 1, pp. 1–44.

    Article  Google Scholar 

  66. Nagl, W., “Plastolysomes”—plastids involved in the autolysis of the embryo-suspensor in Phaseolus,Z. Pflanzenphysiol., 1977, vol. 85, no. 1, pp. 45–51.

    Article  Google Scholar 

  67. Nakaune, S. et al., A vacuolar processing enzyme, δVPE, is involved in seed coat formation at the early stage of seed development, Plant Cell, 2005, vol. 17, no. 3, pp. 876–887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ngo, Q.A. et al., A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery, Dev. Cell, 2014, vol. 29, no. 4, pp. 491–500.

    Article  CAS  PubMed  Google Scholar 

  69. Nogueira, F.C.S. et al., Proteomic profile of the nucellus of castor bean (Ricinus communis L.) seeds during development, J. Proteomics, 2012, vol. 75, no. 6, pp. 1933–1939.

    Article  CAS  PubMed  Google Scholar 

  70. Olsen, O.A., Nuclear endosperm development in cereals and Arabidopsis thaliana,Plant Cell, 2004, vol. 16, pp. S214–S227.

    Article  Google Scholar 

  71. Olvera-Carrillo, Y. et al., A conserved core of programmed cell death indicator genes discriminates developmentally and environmentally induced programmed cell death in plants, Plant Physiol., 2015, vol. 169, no. 4, pp. 2684–2699.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Ondzighi, C.A. et al., Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds, Plant Cell, 2008, vol. 20, no. 8, pp. 2205–2220.

    Article  CAS  Google Scholar 

  73. Papini, A. et al., Megasporogenesis and programmed cell death in Tillandsia (Bromeliaceae), Protoplasma, 2011, vol. 248, no. 4, pp. 651–662.

    Article  PubMed  Google Scholar 

  74. Peng, X. and Sun, M.X., The suspensor as a model system to study the mechanism of cell fate specification during early embryogenesis, Plant Reprod., 2018, vol. 31, no. 1, pp. 59–65.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Pereira, A.M. et al., “Love is strong, and you’re so sweet”: JAGGER is essential for persistent synergid degeneration and polytubey block in Arabidopsis thaliana,Mol. Plant, 2016, vol. 9, no. 4, pp. 601–614.

    Article  CAS  PubMed  Google Scholar 

  76. Petrussa, E. et al., Mitochondrial bioenergetics linked to the manifestation of programmed cell death during somatic embryogenesis of Abies alba,Planta, 2009, vol. 231, no. 1, pp. 93–107.

    Article  CAS  PubMed  Google Scholar 

  77. Qiu, Y.L. et al., Calcium changes during megasporogenesis and megaspore degeneration in lettuce (Lactuca sativa L.), Sex. Plant Reprod., 2008, vol. 21, no. 3, pp. 197–204.

    Article  CAS  Google Scholar 

  78. Radchuk, V.V. et al., Spatiotemporal profiling of starch biosynthesis and degradation in the developing barley grain, Plant Physiol., 2009, vol. 150, no. 1, pp. 190–204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Reape, T.J. and McCabe, P.F., Apoptotic-like programmed cell death in plants, New Phytol., 2008, vol. 180, no. 1, pp. 13–26.

    Article  CAS  PubMed  Google Scholar 

  80. Reape, T.J. and McCabe, P.F., Commentary: the cellular condensation of dying plant cells: programmed retraction or necrotic collapse?, Plant Sci., 2013, vol. 207, pp. 135–139.

    Article  CAS  PubMed  Google Scholar 

  81. Rocha, A.J. et al., Differential expression of cysteine peptidase genes in the inner integument and endosperm of developing seeds of Jatropha curcas L. (Euphorbiaceae), Plant Sci., 2013, vol. 213, pp. 30–37.

    Article  CAS  PubMed  Google Scholar 

  82. Rocha, A.J., Pohl, S., and Fonteles, C.S.R., Cloning and gene expression analysis of two cDNA of cysteine proteinase genes involved in programmed cell death in the inner integument from developing seeds of Jatropha curcas L., Gene Expr. Patterns, 2018, vol. 27, pp. 122–127.

    Article  CAS  PubMed  Google Scholar 

  83. Russell, S.D., Fine structure of megagametophyte development in Zea mays,Can. J. Bot., 1979, vol. 57, no. 10, pp. 1093–1110.

    Article  Google Scholar 

  84. Schmid, M., Simpson, D., and Gietl, C., Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes, Proc. Natl. Acad. Sci. U. S. A., 1999, vol. 96, no. 24, pp. 14159–14164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Schmid, M. et al., The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum, Proc. Natl. Acad. Sci. U. S. A., 2001, vol. 98, no. 9, pp. 5353–5358.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Shah, M. et al., Deep proteome analysis of gerontoplasts from the inner integument of developing seeds of Jatropha curcas,J. Proteomics, 2016, vol. 143, pp. 346–352.

    Article  CAS  PubMed  Google Scholar 

  87. Smertenko, A.P. et al., Re-organisation of the cytoskeleton during developmental programmed cell death in Picea abies embryos, Plant J., 2003, vol. 33, no. 5, pp. 813–824.

    Article  CAS  PubMed  Google Scholar 

  88. Tian, H.Q. and Russell, S.D., Calcium distribution in fertilized and unfertilized ovules and embryo sacs of Nicotiana tabacum L., Planta, 1997, vol. 202, no. 1, pp. 93–105.

    Article  CAS  Google Scholar 

  89. Üstün, S., Hafren, A., and Hofius, D., Autophagy as a mediator of life and death in plants, Curr. Opin. Plant Biol., 2017, vol. 40, pp. 122–130.

    Article  PubMed  CAS  Google Scholar 

  90. Völz, R. et al., Ethylene signaling is required for synergid degeneration and the establishment of a pollen tube block, Dev. Cell, 2013, vol. 25, no. 3, pp. 310–316.

    Article  PubMed  CAS  Google Scholar 

  91. Wan, L. et al., Early stages of seed development in Brassica napus: a seed coat-specific cysteine proteinase associated with programmed cell death of the inner integument, Plant J., 2002, vol. 30, no. 1, pp. 1–10.

    Article  CAS  PubMed  Google Scholar 

  92. Wang, M. et al., Apoptosis in barley aleurone during germination and its inhibition by abscisic acid, Plant. Mol. Biol., 1996, vol. 32, no. 6, pp. 1125–1134.

    Article  CAS  PubMed  Google Scholar 

  93. Wang, P., Mugume, Y., and Bassham, D.C., New advances in autophagy in plants: regulation, selectivity and function, Semin. Cell Dev. Biol., Academic Press, 2018, vol. 80, pp. 113–122.

    Google Scholar 

  94. Wredle, U., Walles, B., and Hakman, I., DNA fragmentation and nuclear degradation during programmed cell death in the suspensor and endosperm of Vicia faba,Int. J. Plant Sci., 2001, vol. 162, no. 5, pp. 1053–1063.

    Article  Google Scholar 

  95. Wu, J.J. et al., Mitochondrial gcd1 dysfunction reveals reciprocal cell-to-cell signaling during the maturation of Arabidopsis female gametes, Dev. Cell, 2012, vol. 23, no. 5, pp. 1043–1058.

    Article  CAS  PubMed  Google Scholar 

  96. Xu, W. et al., Endosperm and nucellus develop antagonistically in Arabidopsis seeds, Plant Cell, 2016, vol. 28, no. 6, pp. 1343–1360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Yadegari, R. and Drews, G.N., Female gametophyte development, Plant Cell, 2004, vol. 16, pp. 133–141.

    Article  Google Scholar 

  98. Yang, X. et al., Live and let die-the Bsister MADS-box gene OsMADS29 controls the degeneration of cells in maternal tissues during seed development of rice (Oryza sativa), PLoS One, 2012, vol. 7, no. 12. e51435.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Young, T.E. and Gallie, D.R., Programmed cell death during endosperm development, in Programmed Cell Death in Higher Plants, Dordrecht: Springer, 2000.

    Google Scholar 

  100. Zhao, P. et al., A bipartite molecular module controls cell death activation in the basal cell lineage of plant embryos, PLoS Biol., 2013, vol. 11, no. 9. e1001655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Zhimulev, I.F., Morphology and structure of polytene chromosomes, in Advances in Genetics, Academic Press, 1996, vol. 34, pp. 1–490.

    Google Scholar 

  102. Zhuang, X. et al., ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis,Proc. Natl. Acad. Sci. U. S. A., vol. 114, no. 3, pp. E426–E435.

Download references

Author information

Authors and Affiliations

  1. Biology Faculty, Moscow State University, 119234, Moscow, Russia

    T. V. Doronina, E. V. Sheval & E. M. Lazareva

  2. Belozersky Institute of Physicochemical Biology, Moscow State University, 119234, Moscow, Russia

    E. V. Sheval

Authors
  1. T. V. Doronina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. V. Sheval
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. M. Lazareva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. V. Doronina.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by M. Shulskaya

Abbreviations: ROS—reactive oxygen species; PCD—programmed cell death; ER—endoplasmic reticulum.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Doronina, T.V., Sheval, E.V. & Lazareva, E.M. Programmed Cell Death during Formation of the Embryo Sac and Seed. Russ J Dev Biol 51, 135–147 (2020). https://doi.org/10.1134/S1062360420030029

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360420030029

Keywords:

Search

Navigation