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Embryo of Flowering Plants at the Critical Stage of Embryogenesis Relative Autonomy (by Example of Cereals)

Abstract

Autonomy is a special structural and functional state of an embryo, reflecting its ability for self-regulation and independence from the adjacent tissues. Full autonomy is the ability to accomplish normal embryogenesis outside the maternal organism. In this regard, relative autonomy is of special interest. This is one of the critical stages of embryogenesis, when an immature embryo becomes independent of some physiological factors, in particular, hormones (mainly auxins, cytokinins, and ABA) of a maternal organism. The review surveys the literary and authors’ original data on this phenomenon by examples of cereals as compared with other families of flowering plants. Identification of the relative embryonic autonomy as a critical stage in embryo culture in vitro, along with morphological, histological, and physiological statuses of the relatively autonomous embryos, is considered. Prospects of solving basic problems of autonomy of plants embryogenesis and and its biotechnological application autonomy are discussed.

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REFERENCES

  1. Allagulova, Ch.R., Gimalov, F.R., Shakirova, F.M., and Vakhitov, V.A., The plant dehydrins: structure and putative functions, Biochemistry (Moscow), 2003, vol. 68, no. 9, pp. 945–951.

    CAS  PubMed  Google Scholar 

  2. Altamura, M.M., Della Rovere, F., Fattorini, L., D’Angeli, S., and Falaska, G., Recent advances on genetic and physiological bases of in vitro somatic embryo formation, in In vitro Embryogenesis in Higher Plants, German, M.A. and Lambardi, M., Eds., New York: Springer, 2016, pp. 47–85.

    Google Scholar 

  3. An, Y.-Q. and Lin, L., Transcriptional regulatory programs underlying barley germination and regulatory functions of gibberellin and abscisic acid, BMC Plant Biol., 2011, vol. 11, p. 24.https://doi.org/10.1186/1471-2229-11-105

    CAS  Article  Google Scholar 

  4. Bakos, F., Darko, E., Ponya, Z., and Barnabas, B., Regeneration of fertile wheat plants from isolated zygotes using wheat microspore culture as nurse cells, Plant Cell Tiss. Organ Cult., 2003, vol. 74, pp. 243–247.

    Article  CAS  Google Scholar 

  5. Bannikova, V.P. and Khvedynich, O.A., Osnovy embriologii rastenii (Fundamentals of Plant Embryology), Kiev: Naukova Dumka, 1982.

  6. Banowetz, G.M., Ammar, K., and Chen, D.D., Temperature effects on cytokinin accumulation and kernel mass in a dwarf wheat, Ann. Bot., 1999, vol. 83, pp. 303–307.

    Article  CAS  Google Scholar 

  7. Barrero, J.M., Talbot, M.J., White, R.G., Jacobsen, J.V., and Gubler, F., Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley, Plant Physiol., 2009, vol. 150, pp. 1006–1021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Batygin, N.F., Ontogenez vysshikh rastenii (Ontogenesis of Higher Plants), Moscow: Agropromizdat, 1986.

  9. Batygin, N.F., Physiology of ontogenesis, in Fiziologicheskie osnovy selektsii rastenii (Physiological Basics of Plant Breeding), Udovenko, G.V. and Shevelukhi, V.P., Eds., St. Petersburg: VIR, 1995, pp. 14–92.

  10. Batygin, N.F., The systems approach in biology and agronomy, in Nikolai Fedorovich Batygin: zhizn’ i tvorchestvo (Nikolai Fedorovich Batygin: Life and Creative Work), Batygina, T.B., Ed., St. Petersburg: Professional, 2007, pp. 151–196.

  11. Batygina, T.B., On the possibility of distinguishing a new type of embryogenesis in Angiospermae, Dokl. Akad. Nauk SSSR, 1968a, vol. 186, no. 6, pp. 1499–1502.

    Google Scholar 

  12. Batygina, T.B., Embryogenesis in the genus Triticum (with regard to the issues of monocotyledony and distant hybridization in cereals), Bot. Zh., 1968b, vol. 53, no. 4, pp. 480–490.

    Google Scholar 

  13. Batygina, T.B., Embriologiya pshenitsy (Wheat Embryology), Leningrad: Kolos, 1974.

  14. Batygina, T.B., Khlebnoe zerno (Bread Grain), Leningrad: Nauka, 1987.

  15. Batygina, T.B., Graminad-type of embryogenesis, in Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 2: Semya (Seed), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 1997a, pp. 520–526.

  16. Batygina, T.B., Embryogenesis of cereals, in Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 2: Semya (Seed), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 1997b, pp. 528–538.

  17. Batygina, T.B., Critical periods used to embryonal structures, in XVII Congr. on Sexual Plant Reproduction, Abstracts of Papers, Lublin, 2002, p. 33.

  18. Batygina, T.B., Integrity and reliability system in ontogenesis and evolution, Int. J. Plant Reprod. Biol., 2012, vol. 4, pp. 107–120.

    Google Scholar 

  19. Batygina, T.B., Biologiya razvitiya rastenii. Simfoniya zhizni (Developmental Biology of Plants: A Symphony of Life), St. Petersburg: DEAN, 2014.

  20. Batygina, T.B. and Vasilyeva, V.E., The expediency of a systemic approach to the problem of embryo differentiation in angiosperms, Ontogenez, 1983, vol. 14, no. 3, pp. 304–311.

    Google Scholar 

  21. Batygina, T.B. and Vasilyeva, V.E., Some aspects of embryo-culture (autonomy of embryo) of flowering plants, Phytomorphology, 1987a, vol. 37, pp. 283–288.

    Google Scholar 

  22. Batygina, T.B. and Vasilyeva, V.E., Applied aspects of embryology. Autonomy of embryo and the embryonic culture of flowering plants, Bot. Zh., 1987b, vol. 72, no. 2, pp. 155–161.

    Google Scholar 

  23. Batygina, T.B. and Vasilyeva, V.E., Some aspects of autonomy of embryo in flowering plants, Phytomorphology, 1988, vol. 38, pp. 293–297.

    Google Scholar 

  24. Batygina, T.B. and Vasilyeva, V.E., Razmnozhenie rastenii (Plant Reproduction), St. Petersburg: S.-Peterb. Univ., 2002.

    Google Scholar 

  25. Belefant-Miller, H., Fong, F., and Smith, D., Abscisic acid biosynthesis during corn embryos development, Planta, 1994, vol. 195, pp. 17–21.

    Article  CAS  Google Scholar 

  26. Benkova, E., Michniewicz, M., Sauer, M., Tichmann, T., Seifertova, D., Jurgens, G., and Friml, J., Local, efflux-dependent auxin gradients as a common module for plant organ formation, Cell, 2003, vol. 115, pp. 591–602.

    Article  CAS  PubMed  Google Scholar 

  27. Bouamama, B., Salem, A.B., Youssef, F.B., Chaieb, S., Jaafoura, M.-H., Mliki, A., and Ghorbel, A., Somatic embryogenesis and organogenesis from mature caryopses of North African barley accession “Kerkena” (Hordeum vulgare L.), In Vitro Cell. Dev. Biol. Plant, 2011, vol. 47, pp. 321–327.

    Article  Google Scholar 

  28. Bychkova, O.V., Evaluation of the effectiveness of morphogenesis and regeneration of spring durum wheat in culture in vitro, Acta Biol. Sib., 2016, no. 2 (1), pp. 139–149.

  29. Capron, A., Chatfield, S., Provart, N., and Berleth, T., Embryogenesis: pattern formation from a single cell, in The Arabidopsis Book, Rockville, MD: The American Society of Plant Biologists, 2009, pp. 1–28.

    Google Scholar 

  30. Carciofi, M., Blennow, A., Nielsen, M.M., Holm, P.B., and Hebelstrup, K.H., Barley callus: a model system for bioengineering of starch in cereals, Plant Methods, 2012, vol. 8. https://doi.org/10.1186/1746-4811-8-36

  31. Chaumont, F. and Tyerman, S.D., Aquaporins: highly regulated channels controlling plant water relations, Plant Physiol., 2014, vol. 164, pp. 1600–1618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Cheng, Z.J., Wang, L., Sun, W., et al., Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3, Plant Physiol., 2013, vol. 161, pp. 240–251.

    Article  CAS  PubMed  Google Scholar 

  33. Davoyan, E.I. and Smetanin, A.P., Poluchenie kallusa i regeneratsiya rastenii risa, Fiziol. Rast., 1979, vol. 26, no. 2, pp. 323–328.

    CAS  Google Scholar 

  34. Delporte, F., Pretova, A., Jardin, P., and Watillon, B., Morpho-histology and genotype dependence of in vitro morphogenesis in mature embryo cultures of wheat, Protoplasma, 2014, vol. 251, pp. 1455–1470.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Devaux, P., The Hordeum bulbosum (L.) method, in Doubled Haploid Production in Crop Plants, Maluszynski, M., Kasha, K.J., Foster, B.P., and Szareiko, I., Eds., Jan: Springer Science + Business Media, LLC, 2003, pp. 15–19.

  36. Du, H., Wu, N., Fu, J., Wang, S., Li, X., Xiao, J., and Xiong, L., A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice, J. Exp. Bot., 2012, vol. 63, pp. 6467–6480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Elhiti, M. and Stasolla, C., The use of zygotic embryos as explants for in vitro propagation: an overview, in Plant Embryo Culture: Methods in Molecular Biology (Methods and Protocols), Thorpe, T.A. and Yeung, E.C., Eds., New York: Humana Press, 2011, vol. 170, pp. 229–255.

    Google Scholar 

  38. Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 2: Semya (Seed), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 1997.

    Google Scholar 

  39. Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 3: Sistemy reproduktsii (Reproduction Systems), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 2000.

  40. Fan, G.-Q., Liu, F., Shao, Q.-Q., and Ren, W.-J., Relations among wheat (Triticum aestivum L.) protein, starch contents and endogenous hormone contents during kernel development, Plant Physiol. Commun., 2007, vol. 43, pp. 36–40.

    Google Scholar 

  41. Finkelstein, R.R., The role of hormones during seed development and germination, in Plant Hormones Biosynthesis, Signal Transduction, Action, Davies, P.J., Ed., Dordrecht: Springer, 2010, pp. 549–573.

    Google Scholar 

  42. Fischer, C. and Neuhaus, G., Influence of auxin on the establishment of bilateral symmetry in monocots, Plant J., 1996, vol. 9, pp. 659–669.

    Article  CAS  Google Scholar 

  43. Fischer, C., Speth, V., Fleig-Eberenz, S., and Neuhaus, G., Induction of zygotic polyembryos in wheat: influence of auxin polar transport, Plant Cell, 1997, vol. 9, pp. 1767–1780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Fischer-Iglesias, C., Sundberg, B., Neuhaus, G., and Jones, A.M., Auxin distribution and transport during embryonic pattern formation in wheat, Plant J., 2001, vol. 26, pp. 115–129.

    Article  CAS  PubMed  Google Scholar 

  45. Forestan, C., Meda, S., and Varotto, S., ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development, Plant Physiol., 2010, vol. 152, pp. 1373–1390.

    Article  PubMed  Google Scholar 

  46. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwartz, H., Hamann, T., Offringa, R., and Jurgens, G., Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis,Nature, 2003, vol. 426, pp. 147–153.

    Article  CAS  PubMed  Google Scholar 

  47. Galin, I.R., Zaitsev, D.Yu., Seldimirova, O.A., and Kruglova, N.N., Involvement of cytokinin in the early stages of embryoidogenesis in vitro in wheat germ calli, Biomika, 2018, vol. 10, no. 2, pp. 141–145.

    Google Scholar 

  48. Goldberg, R., de Paiva, G., and Yadegari, R., Plant embryogenesis: zygote to seed, Science, 1994, vol. 266, pp. 605–614.

    Article  CAS  PubMed  Google Scholar 

  49. Goleva, G.G., Batluk, Yu.A., Vashchenko, T.G., Cherkasova, N.N., and Golev, A.D., Obtaining of regenerated plants of winter wheat (Triticum aestivum L.) in culture in vitro, Vestn. Voronezh. Gos. Agr. Univ., Ser. S.-kh. Nauki, 2014, no. 3 (42), pp. 17–22.

  50. Grigor’eva, L.P. and Shletser, I.A., Screening wheat cultivars for morphogenesis ability in in vitro culture of immature embryos, Izv. Altaisk. Gos. Univ., Ser. Biol., 2006, no. 3 (41), pp. 64–66.

  51. Gusakovskaya, M.A., Blintsov, A.N., and Lebedeva, A.F., Comparative analysis of the spatiotemporal distribution of endogenous hormones in the ovaries of wheat and dandelion in the period of ovule activity, Moscow Univ. Biol. Sci. Bull., 2008, vol. 63, no. 3, pp. 99–108.

    Article  Google Scholar 

  52. Hamann, T., The role of auxin in apical-basal pattern formation during Arabidopsis embryogenesis, Plant Growth Regul., 2001, vol. 20, pp. 292–299.

    Article  CAS  Google Scholar 

  53. Hamann, T., Benkova, E., Baurle, I., Kientz, M., and Jurgens, G., The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo pattering, Genes Dev., 2002, vol. 16, pp. 1610–1615.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Harada, J.J., Belmonte, M.F., and Kwong, R.W., Plant Embryogenesis (Zygotic and Somatic), Chichester: Wiley, 2010. https://doi.org/10.1002/9780470015902.a0002042.pub2

    Book  Google Scholar 

  55. Hess, J.R., Carman, J.G., and Banowetz, G.M., Hormones in wheat kernels during embryony, Plant Physiol., 2002, vol. 159, pp. 379–386.

    Article  CAS  Google Scholar 

  56. Horstman, A., Bemer, M., and Boutilier, K., A transcriptional view on somatic embryogenesis, Regeneration, 2017, vol. 4, pp. 201–216.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Huang, W.-L., Lee, Ch.-H., and Chen, Y.-R., Levels of endogenous abscisic acid and indole-3-acetic acid influence shoot organogenesis in callus cultures of rice subjected to osmotic stress, Plant. Cell, Tiss. Org. Cult., 2012, vol. 108, pp. 257–263.

    Article  CAS  Google Scholar 

  58. Hussain, A., Qarshi, I.A., Nazir, H., and Ullah, I., Plant tissue culture: current status and opportunities, in Recent Advances in Plant in vitro Culture, Intech, 2012, pp. 1–21. https://doi.org/10.5772/50568

  59. Ignatova, S.A., Kletochnye tekhnologii v rastenievodstve, genetike i selektsii vozdelyvaemykh rastenii: zadachi, vozmozhnosti, razrabotki sistem in vitro (Cell Technologies in Plant Growing, Genetics, and Breeding of Cultivated Plants: Challenges, Opportunities, and Development of in Vitro Systems), Odessa: Astroprint, 2011.

  60. Jenik, P.D. and Barton, M.K., Surge and destroy: the role of auxin in plant embryogenesis, Development, 2005, vol. 132, pp. 3577–3585.

    Article  CAS  PubMed  Google Scholar 

  61. Jiang, H., Chen, J., Gao, X.L., Wan, J., Wang, P.R., Wang, X.D., and Xu, Z.J., Effect of ABA on rice callus and development of somatic embryo and plant regeneration, Acta Agron. Sin., 2006, vol. 32, pp. 1379–1383.

    CAS  Google Scholar 

  62. Jimenez, V.M., Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis, Plant Growth Regul., 2005, vol. 47, pp. 91–110.

    Article  CAS  Google Scholar 

  63. Jimenez, V.M. and Bangerth, F., Hormonal status of maize initial explants and the embryogenic and non-embryogenic callus cultures derived from them as related to morphogenesis in vitro, Plant Sci., 2001, vol. 160, pp. 247–257.

    Article  CAS  PubMed  Google Scholar 

  64. Kalinin, F.L., Physiological and biochemical features of embryonic development of plants, Extended Abstract of Doctoral (Biol.) Dissertation, Moscow, 1956.

  65. Kawakami, N., Miyake, Y., and Noda, K., ABA insensitivity and low ABA levels during seed development of non-dormant wheat mutants, J. Exp. Bot., 1997, vol. 48, pp. 1415–1421.

    Article  CAS  Google Scholar 

  66. Korochkin, L.I., Biologiya individual’nogo razvitiya (geneticheskii aspekt) (The Biology of Individual Development (Genetic Aspect)), Moscow: Mosk. Gos. Univ., 2002.

  67. Kruglova, N.N., Optimization of biotechnology of obtaining wheat plants in culture in vitro, Izv. Ufim. Nauchn. Tsentra Ross. Akad. Nauk, 2012a, no. 3, pp. 57–61.

  68. Kruglova, N.N., Evaluation of collection of spring wheat genotypes by the resistance of autonomous embryos on selective media in vitro simulating drought, Izv. Samarsk. Nauchn. Tsentra Ross. Akad. Nauk, 2012b, vol. 14, no. 1 (9), pp. 2243–2245.

  69. Kruglova, N.N., Periodization of the development of wheat germ as a methodological aspect of biotechnological developments, Izv. Ufim. Nauchn. Tsentra Ross. Akad. Nauk, 2012c, no. 2, pp. 21–24.

  70. Kruglova, N.N., Determination of the critical stage of wheat embryo autonomy in in vitro culture, Izv. Ufim. Nauchn. Tsentra Ross. Akad. Nauk, 2013a, no. 1, pp. 42–45.

  71. Kruglova, N.N., Periodization of wheat embryo structure development on the basis of anatomical and morphological criteria, Modern Phytomorphol., 2013b, vol. 4, pp. 181–183.

    Google Scholar 

  72. Kruglova, N.N., Detection of the wheat embryo autonomy as a stage of elaboration of rapid diagnostical biotechnology for obtaining drought-resistant samples, Perm. Agrarn. Vestn., 2014, no. 1 (5), pp. 38–43.

  73. Kruglova, N.N., Organogenesis of cereals at the early stages of ontogenesis in vivo as a structural basis of experimental studies in vitro, Ekobiotekh, 2019, vol. 2, no. 1, pp. 36–50.

    Google Scholar 

  74. Kruglova, N.N. and Katasonova, A.A., Immature wheat embryo as a morphogenetically competent explant, Fiziol. Biokhim. Kul’t. Rast., 2009, vol. 41, no. 2, pp. 124–131.

    Google Scholar 

  75. Kruglova, N.N. and Seldimirova, O.A., Regeneratsiya pshenitsy in vitro i ex vitro (Wheat Regeneration in vitro and ex vitro), Ufa: Gilem, 2011.

  76. Kruglova, N.N., Seldimirova, O.A., Zinatullina, A.E., and Veselov, D.S., Abscisic acid in in vitro explant culture systems, Izv. Ufim. Nauchn. Tsentra Ross. Akad. Nauk, 2018a, no. 2, pp. 55–60.

  77. Kruglova, N.N., Seldimirova, O.A., Zinatullina, A.E., and Veselov, D.S., The critical stage of wheat embryo autonomy in planta, Biomika, 2018b, vol. 10, no. 1, pp. 1–6.

    Google Scholar 

  78. Kruglova, N.N., Seldimirova, O.A., Zinatullina, A.E., and Veselov, D.S., Involvement of abscisic acid in stimulation of somatic embryogenesis in plants, Usp. Sovrem. Biol., 2018c, vol. 138, no. 5, pp. 516–528.

    Google Scholar 

  79. Kruglova, N.N., Seldimirova, O.A., Zinatullina, A.E., and Nikonov, V.I., Detection of relative autonomy of spring wheat zygotic embryos in planta to optimize biotechnological research, Izv. Ufim. Nauchn. Tsentra Ross. Akad. Nauk, 2018d, no. 3, pp. 28–33.

  80. Kruglova, N.N., Seldimirova, O.A., and Zinatullina, A.E., The histological status of wheat embryo at the stage of organogenesis in vivo optimal for obtaining morphogenic callus in vitro, Izv. Ufim. Nauchn. Tsentra Ross. Akad. Nauk, 2019a, no. 1, pp. 25–29.

  81. Kruglova, N.N., Seldimirova, O.A., and Zinatullina, A.E., Structural features and hormonal regulation of zygotic embryogenesis in cereals, Usp. Sovr. Biol., 2019b, vol. 139, no. 4, pp. 326–337.

  82. Kumari, P. and Thaneshwari Rahul, Embryo resque in horticular crops, Int. J. Curr. Microbiol. Appl. Sci., 2018, vol. 7, pp. 3350–3358.

    Article  CAS  Google Scholar 

  83. Kusnetsov, V.V., Chloroplasts: structure and expression of the plastid genome, Russ. J. Plant Physiol., 2018, vol. 65, no. 4, pp. 465–476.

    Article  CAS  Google Scholar 

  84. Laurie, D.A. and Bennet, M.D., Wheat × maize hybridization, Can. J. Genet. Cytol., 1986, vol. 28, pp. 313–316.

    Article  Google Scholar 

  85. Luk’yanyuk, S.F., The development of in vitro methods to obtain haploid barley and triticale, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow, 1983.

  86. Luk’yanyuk, S.F. and Ignatova, S.A., Metody kul’tury tkanei i organov v selektsii rastenii (Methods for Tissue and Organ Culture in Plant Breeding), Odessa, 1980.

    Google Scholar 

  87. Lykova, N.A., Effekt prevegetatsii: ekologicheskie posledstviya (Prevegetation Effect: Environmental Consequences), St. Petersburg: Nauka, 2009.

  88. Mahdavi-Darvari, F., Noor, N., and Ismanizan, I., Epigenetic regulation and gene markers as signals of early somatic embryogenesis, Plant Cell Tiss. Org. Cult., 2015, vol. 120, pp. 407–422.

    Article  CAS  Google Scholar 

  89. Medvedev, S.S. and Sharova, E.I., Biologiya razvitiya rastenii (Developmental Biology of Plants), in 2 vols., vol. 1: Nachala biologii razvitiya rastenii. Fitogormony (Basics of Developmental Biology of Plants: Phytohormones), St. Petersburg: S.-Peterb. Univ., 2011.

  90. Meinke, D.W., Seed development in Arabidopsis thaliana, in Arabidopsis, Meyerowith, E.M. and Somerwille, C.R., Eds., Cold Spring Harber, New York: Cold Spring Harber Laboratory Press, 1994, pp. 253–295.

    Google Scholar 

  91. Meinke, D.W., Molecular genetics of plant embryogenesis, Ann. Rev. Plant Physiol. Plant Mol. Biol., 1995, vol. 46, pp. 369–394.

    Article  CAS  Google Scholar 

  92. Miransaria, M. and Smithc, D.L., Plant hormones and seed germination, Env. Exp. Bot., 2014, vol. 99, pp. 110–121.

    Article  CAS  Google Scholar 

  93. Mitić, N., Dodig, D., Nikolić, R., Nikonović, S., Vinterkhalter, D., and Vinterkhalter, B., Effects of donor plant environmental conditions on immature embryo cultures derived from worldwide origin wheat genotypes, Russ. J. Plant Physiol., 2009, vol. 56, no. 4, pp. 540–545.

    Article  CAS  Google Scholar 

  94. Methods in Molecular Biology, vol. 427: Plant Embryogenesis, Suarez, M.E. and Bozhkov, P.V., Eds., Totowa, New York: Humana Press, 2008.

  95. Möller, B. and Weijers, D., Auxin control of embryo patterning, Cold Spring Harb. Perspect. Biol., 2009, vol. 1. https://doi.org/10.1101/cshperspect.a001545

  96. Muller, B. and Sheen, J., Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis, Nature, 2008, vol. 453, pp. 1094–1097.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Müller, K., Tintelnot, S., and Leubner-Metzger, G., Endosperm limited brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana,Plant Cell Physiol., 2006, vol. 47, pp. 864–877.

    Article  CAS  PubMed  Google Scholar 

  98. Nambara, E., Okamoto, M., Tatematsu, K., Yano, R., Seo, M., and Kamiya, Y., Abscisic acid and the control of seed dormancy and germination, Seed Sci. Res., 2010, vol. 20, pp. 55–67.

    Article  CAS  Google Scholar 

  99. Nikitina, E.D. and Khlebova, L.P., Effect of temperature and light on the direct germination of immature embryos of Triticum aestivum L. in culture in vitro, Izv. Altaisk. Gos. Univ., Ser. Biol. Nauki, 2014, vol. 3, no. 1 (83), pp. 46–50.

  100. Nikolaeva, M.G., Lyanguzova, I.V., and Pozdova, L.M., Biologiya semyan (Seed Biology), St. Petersburg, 1999.

    Google Scholar 

  101. Noga, A., Skrzypek, E., Warchoł, M., Czyczylo-Mysza, I., Dziurka, K., Marcinska, I., Juzon, K., Warzecha, T., Sutkowska, A., Nita, Z., and Werwinska, K., Conversion of oat (Avena sativa L.) haploid embryos into plants in relation to embryo developmental stage and regeneration media, In Vitro Cell Dev. Biol. Plant, 2016, vol. 52, pp. 590–597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Obroucheva, N.V., Transition from hormonal to nonhormonal regulation as exemplified by seed dormancy release and germination triggering, Russ. J. Plant Physiol., 2012, vol. 59, no. 4, pp. 546–555.

    Article  CAS  Google Scholar 

  103. Obroucheva, N.V., Hormonal regulation during plant fruit development, Russ. J. Dev. Biol., 2014, vol. 45, no. 1, pp. 11–21.

    Article  CAS  Google Scholar 

  104. Obrucheva, N.V. and Antipova, O.V., Morphology and physiology of seed germination, in Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 2: Semya (Seed), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 1997, pp. 667–680.

  105. Osnovy embriogeneza zlakov (Fundamentals of Embryogenesis of Cereals), Bannikova, V.P., Khvedynich, O.A., Kravets, E.A., Tarasenko, L.V., Shulaev, V.K., Il’chenko, K.V., Maistrov, P.D., and Barabanova, E.A., Eds., Kiev: Naukova Dumka, 1991.

  106. Paiva, R. and Kriz, A.L., Effect of abscisic acid on embryo-specific gene expression during normal and precocious germination in normal and viviparous maize (Zea mays) embryos, Planta, 1994, vol. 192, pp. 332–339.

    Article  CAS  Google Scholar 

  107. Plant Embryo Culture: Methods and Protocols, Thorpe, T.A. and Yeung, E.C., Eds., New York: Springer, 2011.

    Google Scholar 

  108. Plant Embryogenesis, Thorpe, T.A., Ed., Dordrecht: Kluwer, 1995.

    Google Scholar 

  109. Plant Hormones: Biosynthesis, Signal Transduction, Action, Davies, P.J., Ed., Dordrecht: Springer, 2010.

  110. Poddubnaya-Arnol’di, V.A., Tsitoembriologiya pokrytosemennykh rastenii. Osnovy i perspektivy (Cytoembryology of Angiosperms: Fundamentals and Prospects), Moscow: Nauka, 1976.

  111. Poddubnaya-Arnol’di, V.A., Cytoembryological characteristics of the family Gramineae, Byull. Gl. Botan. Sada AN SSSR, 1978, no. 109, pp. 57–60.

  112. Poddubnaya-Arnol’di, V.A., Kharakteristika semeistv pokrytosemennykh rastenii po tsitoembriologicheskim priznakam (Characteristics of Angiosperm Families by Cytoembryological Traits), Moscow: Nauka, 1982.

  113. Przetakiewicz, A., Orczyk, W., and Nadolska-Orczyk, A., The effect of auxin on plant regeneration of wheat, barley and triticale, Plant Cell Tiss. Org. Cult., 2003, vol. 73, pp. 245–256.

    Article  CAS  Google Scholar 

  114. Puthur, J.T., Shackira, A.M., Saradhi, P.P., and Bartels, D., Chloroembryos: a unique photosynthesis system, J. Plant Physiol., 2013, vol. 170, pp. 1131–1138.

    Article  CAS  PubMed  Google Scholar 

  115. Rademacher, E.H., Lokerse, A.S., Schlereth, A., Llavata-Peris, C.I., Bayer, M., Kientz, M., Rios, A.F., Borst, J.W., Lukowitz, W., and Jurgens, G., Different auxin response machineries control distinct cell fates in the early plant embryo, Dev. Cell, 2012, vol. 22, pp. 211–222.

    Article  CAS  PubMed  Google Scholar 

  116. Raghavan, V., Experimental Embryogenesis in Vascular Plants, London: Academic, 1976.

    Google Scholar 

  117. Raghavan, V., Molecular Embryology of Flowering Plants, Cambridge: Cambridge Univ. Press, 1997.

    Book  Google Scholar 

  118. Raghavan, V., One hundred years of zygotic embryo culture investigations, In Vitro Cell Dev. Biol. Plant, 2003, vol. 39, pp. 437–442.

    Article  Google Scholar 

  119. Rai, M.K., Shekhawat, N.S., Gupta, A.K., et al., The role of abscisic acid in plant tissue culture: a review of recent progress, Plant Cell Tiss. Org. Cult., 2011, vol. 106, pp. 179–190.

    Article  CAS  Google Scholar 

  120. Reynolds, Th., Plant embryogenesis, Plant. Mol. Biol., 1997, vol. 33, pp. 1–10.

    Article  CAS  PubMed  Google Scholar 

  121. Robert Boisivon, H., Crhak Khaitova, L., Mroue, S., and Frimova, E., The importance of localized auxin production for morphogenesis of reproductive organs and embryos in Arabidopsis,J. Exp. Bot., 2015, vol. 66, pp. 5029–5042.

    Article  CAS  Google Scholar 

  122. Rostami, H., Giri, A., Nejad, A.S.M., and Moslem, A., Optimization of multiple shoot induction and plant regeneration in Indian barley (Hordeum vulgare) cultivars using mature embryos, Saudi J. Biol. Sci., 2013, vol. 20, pp. 251–255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Rusmussen, R.D., Hole, D., and Carman, J.G., Wheat kernel dormancy and +abscisic acid level following exposure to fluridone, J. Plant Physiol., 1997, vol. 150, pp. 440–445.

    Article  Google Scholar 

  124. De Rybel, B., Abidi, M., Breda, A., Wendrich, J., Smit, M., Novak, O., Yamaguchi, N., Yoshida, S., Isterdael, G., Palovaara, J., Nijsse, B., Boekschoten, M.V., Hooiveld, G., Beeckman, T., Wagner, D., Ljunq, K., Fleck, C., and Weijers, D., Plant development. integration of growth and pattering during vascular tissue formation in Arabidopsis, Science, 2014, vol. 345, p. 1255215. https://doi.org/10.1126/science.1255215

    CAS  Article  PubMed  Google Scholar 

  125. Sauer, M. and Friml, J., Visualization of auxin gradients in embryogenesis, Methods Mol. Biol., 2008, vol. 427, pp. 137–144.

    Article  CAS  PubMed  Google Scholar 

  126. Schaller, G.E., Bishopp, A., and Kieberc, J.J., The Yin-Yang of hormones: cytokinin and auxin interactions in plant development, Plant Cell, 2015, vol. 27, pp. 44–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Seldimirova, O.A., Titova, G.E., and Kruglova, N.N., A complex morpho-histological approach to the in vitro study of morphogenic structures in a wheat anther culture, Biol. Bull. (Moscow), 2016a, vol. 43, no. 2, pp. 121–126.

    Article  Google Scholar 

  128. Seldimirova, O.A., Kudoyarova, G.R., Kruglova, N.N., Zaytsev, D.Yu., and Veselov, S.Yu., Changes in distribution of cytokinins and auxins in cell during callus induction and organogenesis in vitro in immature embryo culture of wheat, In Vitro Cell Dev. Biol. Plant, 2016b, vol. 52, pp. 251–264.

    Article  CAS  Google Scholar 

  129. Seldimirova, O.A., Galin, I.R., Kruglova, N.N., and Veselov, D.S., Distribution of IAA and ABA in developing wheat embryos in vivo, Izv. Ufim. Nauchn. Tsentra Ross. Akad. Nauk, 2017a, no. 3 (1), pp. 114–118.

  130. Seldimirova, O.A., Kruglova, N.N., Titova, G.E., and Batygina, T.B., Comparative ultrastructural analysis of the in vitro microspore embryoids and in vivo zygotic embryos of wheat as a basis for understanding of cytophysiological aspects of their development, Russ. J. Dev. Biol., 2017b, vol. 48, no. 3, pp. 185–197.

    Article  Google Scholar 

  131. Seldimirova, O.A., Galin, I.R., Kudoyarova, G.R., Kruglova, N.N., and Veselov, D.S., Effect of ABA on maturation of barley embryos in vivo: results of the study of the ABA-deficient mutant AZ34, Ekobiotekh, 2018a, vol. 1, no. 4, pp. 203–211.

    Google Scholar 

  132. Seldimirova, O.A., Kruglova, N.N., Galin, I.R., and Veselov, D.S., Comparative evaluation of the level of IAA, ABA, and cytokinin in in vivo embryogenesis of barley cultivar Steptoe and ABA-deficient mutant AZ34, Ekobiotekh, 2018b, vol. 1, no. 3, pp. 134–142.

    Google Scholar 

  133. Seldimirova, O.A., Kudoyarova, G.R., Kruglova, N.N., Galin, I.R., and Veselov, D.S., Somatic embryogenesis in wheat and barley calli in vitro is determined by the level of indoleacetic and abscisic acids, Russ. J. Dev. Biol., 2019, vol. 50, no. 3, pp. 124–135.

    Article  CAS  Google Scholar 

  134. Shamrov, I.I., Ovule of flowering plants: principles of organization and typing, Doctoral (Biol.) Dissertation, St. Petersburg: Botanical Institute, Ross. Akad. Nauk, 1995.

  135. Shamrov, I.I., Embryogeny, in Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 2: Semya (Seed), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 1997, pp. 297–307.

  136. Shamrov, I.I., Semyazachatok tsvetkovykh rastenii: stroenie, funktsii, proiskhozhdenie (Ovule of Flowering Plants: Structure, Functions, and Origin), Batygina, T.B., Ed., Moscow: Tov. Nauchn. Izd. KMK, 2008.

    Google Scholar 

  137. Shamrov, I.I. and Anisimova, G.M., Features of the transformation of ovule to seed in Luzula pedemontana (Juncaceae), Bot. Zh., 1993, vol. 78, no. 12, pp. 24–44.

    Google Scholar 

  138. Shamrov, I.I. and Anisimova, G.M., Critical stages of ovule and seed development, Acta Biol. Cracov. Ser. Bot., 2003, vol. 45, pp. 167–172.

    Google Scholar 

  139. Shamrov, I.I. and Nikiticheva, Z.I., Morphogenesis of ovule and seed in Gymnadenia conopsea (Orchidaceae): structural and histochemical study, Bot. Zh., 1992, vol. 77, no. 4, pp. 45–60.

    Google Scholar 

  140. Sharma, H.C. and Gill, B.C., Effect of embryo age and culture media on plant growth and vernalization response in winter wheat, Euphytica, 1982, vol. 31, pp. 629–634.

    Article  Google Scholar 

  141. Schmalhausen, I.I., Faktory evolyutsii (teoriya stabiliziruyushchego otbora) (Factors of Evolution (the Theory of Stabilizing Selection)), Berg, R.L., Makhotin, A.A., and Yablokov, A.V., Eds., 2nd ed. (revised and extended), Moscow: Nauka, 1968.

  142. Sieburth, L., Muday, G., King, E., Benton, G., Kim, S., Metcalf, K., Meyers, L., Seamen, E., and Norman, J., SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein pattering in Arabidopsis,Plant Cell, 2006, vol. 18, pp. 1396–1411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Skazkin, F.D., Kriticheskii period u rastenii po otnosheniyu k nedostatku vody v pochve (The Critical Period in Plants in Relation to the Lack of Water in the Soil), Leningrad: Nauka, 1971.

  144. Slesak, H., Goralski, G., Pawłowska, H., Skucińska, B., Popielarska-Konieczna, M., and Joachimiak, A.J., The effect of genotype on a barley scutella culture. Histological aspects, Cent. Eur. J. Biol., 2013, vol. 8, pp. 30–37.

    CAS  Google Scholar 

  145. De Smet, I., Lau, S., Mayer, U., and Jurgens, G., Embryogenesis—the humble beginnings of plant life, Plant J., 2010, vol. 61, pp. 959–970.

    Article  CAS  PubMed  Google Scholar 

  146. Smet, W., Sevilem, I., de Luis, BalaguerM.A., Wybouw, B., Mor, E., Miyashima, S., Blob, B., Roszak, P., Jacobs, T.B., Boekschoten, M., Hooiveld, G., Sozzani, R., Helariutta, Y., and de Rybel, B., DOF2.1 controls cytokinin-dependent vascular cell proliferation downstream of TMO5/LHW, Curr. Biol., 2019, vol. 29, pp. 520–529.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Snape, J.W., Chapman, V., Moss, L., Blanchard, C.F., and Miller, T.E., The crossabilities of wheat varieties with Hordeum bulbosum,Heredity, 1979, vol. 42, pp. 291–298.

    Article  Google Scholar 

  148. Spivak, V.A., Minlikaeva, K.I., Evseeva, N.V., Tkachenko, O.V., and Lobachev, Yu.V., Properties of morphogenesis of structural elements of immature embryos of wheat lines cultured in vitro, Byull. Bot. Sada Sarat. Univ., 2014, no. 12, pp. 188–197.

  149. Sravnitel’naya embriologiya tsvetkovykh rastenii. Odnodol’nye: Butomaceae–Lemnaceae (Comparative Embryology of Flowering Plants. Monocots: Butomaceae–Lemnaceae), Batygina, T.B. and Yakovlev, M.S., Eds., Leningrad: Nauka, 1990.

  150. Suzuki, T., Matsuura, T., Kawakami, N., and Noda, K., Accumulation and leakage of abscisic acid during embryo development and seed dormancy in wheat, Plant Growth Regul., 2000, vol. 30, pp. 253–260.

    Article  CAS  Google Scholar 

  151. Svetlov, P.G., The theory of critical periods of development and its importance for understanding the principles of environmental influence on ontogenesis, in Voprosy tsitologii i obshchei fiziologii (Problems of Cytology and General Physiology), Moscow: Akad. Nauk SSSR, 1960, pp. 263–285.

  152. Symons, S.J., Angold, R.E., Black, M.A., and Chapman, J.M., Changes in the growth capacity of the developing wheat embryo, J. Exp. Bot., 1983, vol. 34, pp. 1541–1550.

    Article  Google Scholar 

  153. Takhtadzhyan, A.L., Sistema i filogeniya tsvetkovykh rastenii (System and Phylogeny of Flowering Plants), Moscow: Nauka, 1966.

  154. Terekhin, E.S., Semya i semennoe razmnozhenie (Seed and Seed Reproduction), St. Petersburg: Mir i Sem’ya, 1996.

  155. Terletskaya, N.V., Nespetsificheskie reaktsii zernovykh zlakov na abioticheskie stressy in vivo i in vitro (Nonspecific Responses of Cereals to Abiotic Stress in vivo and in vitro), Almaty: IBBR KN MON RK, 2012.

  156. Titova, G.E., Seldimirova, O.A., Kruglova, N.N., Galin, I.R., and Batygina, T.B., Phenomenon of “Siamese embryos” in cereals in vivo and in vitro: cleavage polyembryony and fasciations, Russ. J. Dev. Biol., 2016, vol. 47, no. 3, pp. 122–137.

    Article  Google Scholar 

  157. Tsinger, N.V., Semya, ego razvitie i fiziologicheskie svoistva (Seed, Its Development and Physiological Properties), Moscow: Akad. Nauk SSSR, 1958.

  158. Tvorogova, V.E. and Lutova, L.A., Genetic regulation of zygotic embryogenesis in angiosperm plants, Russ. J. Plant Physiol., 2018, vol. 65, no. 1, pp. 1–14.

    Article  CAS  Google Scholar 

  159. Vasilyeva, V.E. and Batygina, T.B., Cultivation in vitro of lotus embryos and ovules isolated at different stages of development, Fiziol. Rast., 1981, vol. 28, no. 2, pp. 319–327.

    Google Scholar 

  160. Vasilyeva, V.E. and Batygina, T.B., Autonomy of the embryo, in Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 2: Semya (Seed), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 1997, pp. 579–588.

  161. Vasilyeva, V.E. and Batygina, T.B., Autonomy of the embryo, in Embryology of Flowering Plants. Terminology and Concepts, vol. 2: Seed, Batygina, T.B., Ed., Enfield, NH, USA: Science Publishers, Inc., 2006, pp. 375–382.

  162. Vasilyeva, V.E., Batygina, T.B., and Titova, G.E., Morpho-physiological correlations in the development of the reproductive structures of Nelumbo nucifera Gaertn, Phytomorphology, 1987, vol. 37, pp. 349–358.

    Google Scholar 

  163. Veselov, D.S., Kudoyarova, G.R., Kudryakova, N.V., and Kuznetsov, V.V., Role of cytokinins in stress resistance of plants, Russ. J. Plant Physiol., 2017, vol. 64, no. 1, pp. 15–27.

    Article  CAS  Google Scholar 

  164. Wareing, F.P. and Phillips, I.D.J., Growth and Differentiation in Plants, Oxford: Pergamon Press, 1981.

    Google Scholar 

  165. Wendrich, J.R., Möller, B.K., Uddin, B., Radoeva, T., Lokerse, A.S., Rybel, B.D., and Weijer, D., A set of domain-specific markers in the Arabidopsis embryo, Plant Reprod., 2015, vol. 28, pp. 153–160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. White, C.N., Proebsting, W.M., Hedden, P., and Rivin, C.J., Gibberellins and seed development in maize. I. Evidence that gibberellin/abscisic acid balance governs germination versus maturation pathways, Plant Physiol., 2000, vol. 122, pp. 1081–1088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Willige, B.C., Isono, E., Richter, R., Zourelidou, M., and Schwechheimer, C., Gibberellin regulates PIN-FORMED abundance and is required for auxin-transport growth and development in Arabidopsis thaliana,Plant Cell, 2011. https://doi.org/10.1105/tpc.111.086355

  168. Wilson, I., Barker, G., Lu, C., Coghill, J., Beswick, R., Lenton, J., and Edwards, K., Alteration of the embryo transcriptome of hexaploid winter wheat (Triticum aestivum cv. Mercia) during maturation and germination, Funct. Integr. Genomics, 2005, vol. 5, pp. 144–154.

    Article  PubMed  Google Scholar 

  169. Wu, K., Wang, J., Kong, Z., and Ma, Z.-Q., Characterization of a single recessive yield trait mutant with elevated endogenous ABA concentration and deformed grains, spikelets and leaves, Plant Sci., 2011, vol. 180, pp. 306–312.

    Article  CAS  PubMed  Google Scholar 

  170. Xu, Y., Zhang, W., Gao, Y., Zhao, Y., Guo, L., and Wang, J., Proteomic analysis of embryo development in rice (Oryza sativa), Planta, 2011. https://doi.org/10.1007/s00425-011-1535-4

  171. Zhang, W., Wang, X., Fan, R., Yin, G., Wang, K., Du, L., Xiao, L., and Ye, X., Effects of inter-culture, arabinogalactan proteins, and hydrogen peroxide on the plant regeneration of wheat immature embryos, J. Integr. Agricult., 2015, vol. 14, pp. 11–19.

    Article  CAS  Google Scholar 

  172. Zhao, J., Zhou, C., and Yang, H.Y., Isolation and in vitro culture of zygotes and central cells of Oryza sativa L, Plant Cell Rep., 2000, vol. 19, pp. 321–326.

    Article  CAS  PubMed  Google Scholar 

  173. Zhao, S., Jiang, Q., Ma, J., et al., Characterization and expression analysis of WOX5 genes from wheat and its relatives, Gene, 2014, vol. 537, pp. 63–69.

    Article  CAS  PubMed  Google Scholar 

  174. Zhao, S., Jiang, Q.-T., Ma, J., Wang, J.-R., Liu, Y.-X., Chen, G.-Y., Qi, P.-F., Pu, Z.-E., Lu, Z.-X., Zheng, Y.-L., and Wei, Y.-M., Characterization and expression analysis of WOX2 homeodomain transcription factor in Eegilops tauschii,Genet. Mol. Biol., 2015, vol. 38, pp. 79–85.

    Article  CAS  PubMed  Google Scholar 

  175. Zhukova, G.Ya., Endosperm, in Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 2: Semya (Seed), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 1997, pp. 212–218.

  176. Zhukova, G.Ya., The presence of chlorophyll in the embryo as a trait of classification of flowering plants, in Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants: Terminology and Concepts), vol. 2: Semya (Seed), Batygina, T.B., Ed., St. Petersburg: Mir i Sem’ya, 1997, pp. 461–470.

  177. Zocchi, G. and de Nisi, P., Physiological and biochemical mechanisms involved in the response to abscisic acid in maize coleoptiles, Plant Cell Physiol., 1996, vol. 37, pp. 840–846.

    Article  CAS  Google Scholar 

  178. Zuraida, A.R., Naziah, B., Zamri, Z., and Sreeramanan, S., Efficient plant regeneration of Malaysian indica rice MR 219 and 232 via somatic embryogenesis system, Acta Physiol. Plant., 2011, vol. 33, pp. 1913–1921.

    Article  CAS  Google Scholar 

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Funding

The work was carried out through an association agreement between Ufa Federal Research Center and Komarov Botanical Institute for 2018–2023 by the project no. AAAA-A18-118022190099-6 (Laboratory of Plant Physiology, Ufa Federal Research Center, State Task of Ministry of Science and Higher Education of the Russian Federation no. 075-00326-19-00) and no. AAAA-A18-118051590112-8 (Laboratory of Embryology and Reproductive Biology, Komarov Botanical Institute) and was partially supported by the Russian Foundation for Basic Research, grant no. 17-04-01477.

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Kruglova, N.N., Titova, G.E., Seldimirova, O.A. et al. Embryo of Flowering Plants at the Critical Stage of Embryogenesis Relative Autonomy (by Example of Cereals). Russ J Dev Biol 51, 1–15 (2020). https://doi.org/10.1134/S1062360420010026

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Keywords:

  • embryo
  • embryogenesis
  • embryo autonomy (full and relative)
  • cereals