Skip to main content
SpringerLink
Log in

Cytophysiological Features of the Cereal-Based Experimental System “Embryo In Vivo–Callus In Vitro”

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

Abstract

The most important problem in studying plant calluses in vitro is the relationship between endogenous and exogenous factors that affect the formation of callus (“callus formation”) and their development in an induction medium (“callusogenesis”). Such an endogenous factor as the cytophysiological status of explants in vivo and of calluses in the dynamics of in vitro cultivation attracts the particular attention of the scientific community. In this review, considering the example of cereals, the literature and the authors’ own data on the identification of histological and hormonal features of initial callus cells in explants, immature embryos in vivo, and morphogenic calluses formed from them during in vitro development have been analyzed. The answers to some controversial questions related to the induction of morphogenetic competence and reprogramming of the development of initial callus cells presented in the literature are considered. The comparison of callus formation and callusogenesis in vitro with some similar events in vivo confirms the validity of the principle of universality of morphogenesis processes in vivo and in vitro (Batygina, 2014 and earlier). The prospects applying an integrated experimental system “embryo in vivo–callus in vitro” as a model for studying plant morphogenesis, one of the most complex biological phenomena, is discussed.

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.

Similar content being viewed by others

REFERENCES

  1. Alejandri-Ramirez, N.D., Chavez-Hernandez, E.C., Contreras-Guerra, J.L., et al., Small RNA differential expression and regulation in Tuxpeno maize embryogenic callus induction and establishment, Plant Physiol. Biochem., 2018, vol. 122, pp. 78–89.

    Article  CAS  PubMed  Google Scholar 

  2. Ali, F., Ahsan, M., Saeed, N.A., et al., Establishment and optimization of callus-to-plant regeneration system using mature and immature embryos of maize (Zea mays), Int. J. Agric. Biol., 2014, vol. 16, pp. 111–117.

    CAS  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. https://doi.org/10.1186/1471-2229-11-105

  4. Andronova E.V. Protoderma, in Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants. Terminology and Concepts), St. Petersburg: Mir i sem’ya, 1997, vol. 2, pp. 346–352.

  5. Awan, M.F., Iqbal, M., Sharis, M.N., et al., Evaluation of genotypic and hormone mediated callus induction and regeneration in sugarcane (Saccharum officinarum L.), Int. J. Bot. Stud., 2019, vol. 4, pp. 70–76.

    Google Scholar 

  6. Basile, A., Fambrini, M., and Pugliesti, C., The vascular plants: open system of growth, Dev. Genes Evol., 2017, vol. 227, pp. 129–157.

    Article  CAS  PubMed  Google Scholar 

  7. Batygina, T.B., Biologiya razvitiya rastenii (Plant Developmental Biology), St. Petersburg: DEAN, 2014.

  8. Batygina, T.B., Kruglova, N.N., Gorbunova, V.Yu., et al., Ot mikrospory – k sortu (From Microspore to Cultivar), Moscow: Nauka, 2010.

  9. Batygina, T.B. and Vasilyeva, V.E., Periodization of development of reproductive structures. Critical periods, Acta Biol. Cracov. Ser. Bot., 2003, vol. 45, pp. 27–36.

    Google Scholar 

  10. Butenko, R.G., Biologiya kletok vysshikh rastenii in vitro i biotekhnologii na ikh osnove (Biology of Cells of Higher Plants in Vitro and Biotechnology Based on Them), Moscow: FEK-PRESS, 1999.

  11. Butenko, R.G., Dzhardemaliev, Zh.K., and Gavrilova, N.F., Callus-forming ability of explatates from different organs of different varieties of winter wheat, Fiziol. Rast., 1986, vol. 33, no. 2, pp. 350–355.

    CAS  Google Scholar 

  12. Bychkova, O.V., Ereshchenko, D.V., and Rozova, M.A., Comparative assessment of the use of mature and immature embryos of spring durum wheat in culture, Acta Biol. Sib., 2016, vol. 2, no. 2, pp. 76–80.

    Google Scholar 

  13. Bykova, E.A., Сhergintsev, D.A., Vlasova, T.A., et al., Effect of the auxin polar transport inhibitor on the morphogenesis of leaves and generative structures during fasciation in Arabidopsis thaliana (L.) Heynh., Russ. J. Dev. Biol., 2016, vol. 47, pp. 207–215.

    Article  CAS  Google Scholar 

  14. Bystrova, E.I., Zhukovskaya, N.V., Rakitin, V.J., et al., Role of ethylene in activation of cell division in quiescent center of exised maize roots, Russ. J. Dev. Biol., 2015, vol. 46, pp. 60–64.

    Article  CAS  Google Scholar 

  15. Chavez-Hernandez, E.C., Alehandri-Ramirez, N.D., Contreras-Guerra, L.L., et al., Maize mirna and target regulation in response to hormone depletion and light exposure during somatic embryogenesis, Front. Plant Sci., 2015, vol. 6, pp. 78–89. https://doi.org/10.3389/fpls.2015.00555

    Article  Google Scholar 

  16. Chen, J., Lausser, A., and Dresselhaus, T., Hormonal responses during early embryogenesis in maize, Biochem. Soc. Trans., 2014, vol. 42, pp. 325–331.

    Article  PubMed  CAS  Google Scholar 

  17. Chen, L., Tong, J., Xiao, L., et al., YUCCA-mediated auxin biogenesis is required for cell fate transition occurring during de novo root organogenesis in Arabidopsis, J. Exp. Bot., 2016, vol. 67, pp. 4273–4284.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cheng, Y., Liu, H., Cao, L., et al., Down-regulation of multiple CDK inhibitor ICK/KRP genes promotes cell proliferation, callus induction and plant regeneration in Arabidopsis, Front. Plant Sci., 2015. https://doi.org/10.3389/fpls.2015.00825

  19. Chernov, V.E. and Pendinen, G.I., Comparative assessment of callusogenesis and regeneration in different types of barley, S.-Kh. Biol., 2011, no. 1, pp. 44–53.

  20. Chu, Z., Chen, J., Xu, H., et al., Identification and comparative analysis of microRNA in wheat (Triticum aestivum L.) callus derived from mature and immature embryos during in vitro cultures, Front. Plant Sci., 2016, vol. 7. https://doi.org/10.3389/fpls.2016.01302

  21. Chub, V.V., Rol’ pozitsionnoi informatsii v regulyatsii razvitiya organov tsvetka i listovykh serii pobegov (Role of Positional Information in the Regulation of the Development of Flower Organs and Leaf Series of Shoots), Moscow: Binom, 2010.

  22. Czajkowska, B.I., Finlay, C.M., Jones, G., et al., Diversity of a cytokinin dehydrogenase gene in wild and cultivated barley, PLoS One, 2019, vol. 14. https://doi.org/10.1371/journal.pone.0225899

  23. Dagustu, N., Comparison of callus formation and plantlet regeneration capacity from immature embryo culture of wheat (Triticum aestivum L.) genotypes, Biotech. Biotechnol. Equip., 2014. https://doi.org/10.1080/13102818.2008.10817552

  24. Dakshayini, K., Vaman, R.C., Karun, A., et al., High-frequency plant regeneration and histological analysis of callus in Cichorium intybus: an important medicinal plant, J. Phytol., 2016, vol. 8, pp. 7–12.

    Article  CAS  Google Scholar 

  25. Dodueva, I.E., Gancheva, M.S., Osipova, M.A., et al., Lateral meristems of higher plants: phytohormonal and genetic control, Russ. J. Plant Physiol., 2014, vol. 61, no. 5, pp. 571–589.

    Article  CAS  Google Scholar 

  26. Doll, N.M., Depege-Fargeix, N., Rogowsky, P.M., et al., Signaling in early maize kernel development, Mol. Plant, 2017, vol. 10, pp. 375–388.

    Article  CAS  PubMed  Google Scholar 

  27. Du, H., Wu, N., Fu, J., et al., 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 

  28. Duarte-Ake, F., Nic-Can, G., and De-la-Peca, C., Somatic embryogenesis: polycomb complexes control cell-to-embryo transition, in Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications, Springer Nature Switzerland AG, 2019, Ch. 13, pp. 339–354.

  29. Dziurka, K., Dziurka, M., Warchol., M., et al., Endogenous phytohormone profile during oat (Avena sativa L.) haploid embryo development, In Vitro Cell Dev. Biol. Plant, 2019, vol. 55, pp. 221–229.

    Article  CAS  Google Scholar 

  30. Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Embryology of Flowering Plants. Terminology and Concepts), vol. 2: Semya (Seed), St. Petersburg: Mir i sem’ya, 1997.

  31. Embriologiya tsvetkovykh rastenii. Terminologiya i kontseptsii (Reproduction systems), vol. 3: Sistemy reproduktsii (Embryology of Flowering Plants. Terminology and Concepts), St. Petersburg: Mir i sem’ya, 2000.

  32. Evseeva, N.V., Tkachenko, O.V., Lobachev, Yu.V., et al., Biochemical evaluation of the morphogenetic potential of wheat callus cells in vitro, Russ. J. Plant Physiol., 2007, vol. 54, no. 2, pp. 273–277.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  34. Feher, A., Callus, dedifferentiation, totipotency, somatic embryogenesis: what these terms mean in the era of molecular plant biology?, Front. Plant Sci., 2019. https://doi.org/10.3389/fpls.2019.00536

  35. 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  CAS  PubMed  Google Scholar 

  36. Gaillochet, C. and Lohmann, J.U., The never-ending story: from pluripotency to plant developmental plasticity, Development, 2015, vol. 142, pp. 2237–2249.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Gaillochet, C., Daum, G., and Lohmann, J.U., O cell, where art thou? The mechanisms of shoot meristem pattering, Curr. Opin. Plant Biol., 2015, vol. 23, pp. 91–97.

    Article  PubMed  Google Scholar 

  38. Galin, I.R., Zaitsev, D.Yu., Seldimirova, O.A., et al., Participation of cytokinins in the initial stages of in vitro embryoidogenesis in wheat germ calli, Biomika, 2018, vol. 10, no. 2, pp. 141–145.

    Google Scholar 

  39. Galvan-Ampudia, C.S., Chaumeret, A.M., Godin, C., et al., Phyllotaxis: from patterns of organogenesis at the meristem to shoot architecture, Wiley Interdiscip. Rev. Dev. Biol., 2016, vol. 5, pp. 460–473.

    Article  PubMed  Google Scholar 

  40. Godel-Jedrychowska, K., Kulinska-Lukaszek, K., Horstman, A., et al., Symplasmic isolation marks cell fate changes during somatic embryogenesis, J. Exp. Bot., 2020. https://doi.org/10.1093/jxb/eraa041

  41. Guo, H., Fan, Y., Guo, H., et al., Somatic embryogenesis critical initiation stage-specific m CHH hypomethylation reveals epigenetic basis underlying embryogenic redifferentiation in cotton, Plant Biotechnol. J., 2020, vol. 18, pp. 1648–1650.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hajheidari, M., Koncz, C., and Bucker, M., Chromatin evolution-key innovations underpinning morphological complexity, Front. Plant Sci., 2019. https://doi.org/10.3389/fpls.2019.00454

  43. 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 

  44. Hisano, H., Matsuura, T., Mori, I.C., et al., Endogenous hormone levels affect the regeneration ability of callus derived from different organs in barley, Plant Physiol. Biochem., 2016, vol. 99, pp. 66–72.

    Article  CAS  PubMed  Google Scholar 

  45. Hong, J.K., Park, K.J., Lee, G.-S., et al., Callus induction and plant regeneration from immature zygotic embryos of various maize genotypes (Zea mays L.), J. Plant Biotechnol., 2017, vol. 44, pp. 49–55.

    Article  Google Scholar 

  46. Iida, H., Yoshida, A., and Takada, S., ATML1 activity is restricted to the outermost cells of the embryo through post-transcriptional repressions, Development, 2019, vol. 146. https://doi.org/10.1242/dev.169300

  47. Ijaz, B., Sudiro, C., Hyder, M.Z., et al., Histo-morphological analysis of rice callus cultures reveals differential regeneration response with varying media combinations, In Vitro Cell Dev. Biol. Plant, 2019. https://doi.org/10.1007/s11627-019-09974-6

  48. Ikeuchi, M., Sugimoto, K., and Iwase, A., Plant callus: mechanisms of induction and repression, Plant Cell, 2013, vol. 25, pp. 3159–3173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ikeuchi, M., Iwase, A., and Sugimoto, K., Control of plant cell differentiation by histone modification and DNA methylation, Curr. Opin. Plant Biol., 2015, vol. 28, pp. 60–67.

    Article  CAS  PubMed  Google Scholar 

  50. Ikeuchi, M., Ogawa, Y., Iwase, A., et al., Plant regeneration: cellular origins and molecular mechanisms, Development, 2016, vol. 143, pp. 1442–1453.

    Article  CAS  PubMed  Google Scholar 

  51. Ikeuchi, M., Shibata, M., Rymen, B., et al., A gene regulatory network for cellular reprogramming in plant regeneration, Plant Cell Physiol., 2018, vol. 59, pp. 770–782.

    Article  CAS  PubMed Central  Google Scholar 

  52. Ikeuchi, M., Favero, D.S., Sakamoto, Y., et al., Molecular mechanisms of plant regeneration, Ann. Rev. Plant Biol., 2019, vol. 70, pp. 377–406.

    Article  CAS  Google Scholar 

  53. Iwase, A., Mita, K., Nonaka, S., et al., WIND1-based acquisition of regeneration competency in arabidopsis and rapeseed, J. Plant Res., 2015, vol. 128, pp. 389–397.

    Article  CAS  PubMed  Google Scholar 

  54. Jaeger, J., Irons, D., and Monk, N., Regulative feedback in pattern formation: towards a general relativistic theory of positional information, Development, 2008, vol. 135, pp. 3175–3183.

    Article  CAS  PubMed  Google Scholar 

  55. Janocha, D. and Lohmann, J.U., From signals to stem cells and back again, Curr. Opin. Plant Biol., 2018, vol. 45, pp. 136–142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Jogawat, A. and Yadav, B., Chhaya et al. crosstalk between phytohormones and secondary metabolites in the drought stress tolerance of crop plants: a review, Physiol. Plant., 2021. https://doi.org/10.1111/ppl.13328

  57. Joshi, R. and Kumar, P., Regulation of somatic embryogenesis in crops: a review, Agr. Rev., 2013, vol. 34, pp. 1–20.

    Google Scholar 

  58. Juarez-Gonzalez, V., Lopez-Ruiz, B.A., Baldrich, P., et al., The explant developmental stage profoundly impacts small RNA-mediated regulation at the dedifferentiation step of maize somatic embryogenesis, Sci. Rep., 2019, vol. 9. https://doi.org/10.1038/s41598-019-50962-y

  59. Kawochar, M.A., Ahmed, N.U., Hossain, M.I., et al., Role of the explants and NAA on callus induction of potato (Solanum tuberosum), Am. J. Life Sci., 2017, vol. 5, pp. 140–144.

    CAS  Google Scholar 

  60. Khaliluev, M.R., Bogoutdinova, L.R., Baranova, G.B., et al., Influence of genotype, explant type, and component of culture medium on in vitro callus induction and shoot organogenesis of tomato (Solanum lycopersicum L.), Biol. Bull. (Moscow), 2014, vol. 41, no. 6, pp. 512–521.

    Article  CAS  Google Scholar 

  61. Khlebova, L.P. and Nikitina, E.D., Morphogenetic responses of wheat immature embryo culture depending on growing conditions of donor plants, Acta Biol. Sib., 2016, vol. 2, pp. 68–75.

    Google Scholar 

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

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

    Google Scholar 

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

  65. Kruglova, N.N. and Seldimirova, O.A., Potentially morphogenic callus of wheat in culture in vitro, Izv. Ufimsk. Nauchn. Tsentra Ross. Akad. Nauk, 2018, no. 2, pp. 61–65.

  66. Kruglova, N.N., Batygina, T.B., Gorbunova, V.Yu., et al., Embriologicheskie osnovy androklinii pshenitsy (Embryological Bases of Wheat Androclinia), Moscow: Nauka, 2005.

  67. Kruglova, N.N., Titova, G.E., and Seldimirova, O.A., Callusogenesis as an in vitro morphogenesiss pathway in cereals, Russ. J. Dev. Biol., 2018a, vol. 49, pp. 245–259.

    Article  Google Scholar 

  68. Kruglova, N.N., Seldimirova, O.A., and Zinatulina, A.E., In vitro callus as a model system for the study of plant stress-resistance to abiotic factors (on the example of cereals), Biol. Bull. Rev., 2018b, vol. 8, pp. 518–526.

    Article  Google Scholar 

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

  70. Kruglova, N.N., Seldimirova, O.A., and Zinatullina, A.E., Callus in vitro as a model system for studying plant organogenesis, Izv. Ufimsk. Nauchn. Tsentra Ross. Akad. Nauk, 2019b, no. 2, pp. 44–54.

  71. Kruglova, N.N., Seldimirova, O.A., and Zinatulina, A.E., Structural features and hormonal regulation of the zygotic embryogenesis in cereals, Biol. Bull. Rev., 2020a, vol. 10, pp. 115–126.

    Article  Google Scholar 

  72. 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., 2020b, vol. 51, pp. 1–15.

    Article  Google Scholar 

  73. Lafon-Placette, C. and Kohler, C., Embryo and endosperm, partners in seed development, Curr. Opin. Plant Biol., 2014, vol. 17, pp. 64–69.

    Article  PubMed  Google Scholar 

  74. Lee, K. and Seo, P.J., Dynamic epigenetic changes during plant regeneration, Trends Plant Sci., 2018, vol. 23, pp. 235–247.

    Article  CAS  PubMed  Google Scholar 

  75. Li, K., Wang, J., Liu, C., et al., Expression of AtLEC2 and AtIPTs promotes embryogenic callus formation and shoot regeneration in tobacco, BMC Plant Biol., 2019, vol. 19.https://doi.org/10.1186/s12870-019-1907-7

  76. Liu, J., Sheng, L., Xu, Y., et al., WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis, Plant Cell, 2014, vol. 26, pp. 1081–1093.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Lopez-Ruiz, B.A., Juarez-Gonzalez, V.T., Sandoval-Zapotitla, E., et al., Development-related miRNA expression and target regulation during staggered in vitro plant regeneration of Tuxpeno VS-535 maize cultivar, Int. J. Mol. Sci., 2019, vol. 20. https://doi.org/10.3390/ijms20092079

  78. Lowe, K., La Rota, M., Hoerster, G., et al., Rapid genotype “independent” Zea mays L. (maize) transformation via direct somatic embryogenesis, In Vitro Cell Dev. Biol. Plant, 2018, vol. 28, pp. 1998–2015.

    Google Scholar 

  79. Mashkina, O.S. and Tabatskaya, T.M., Morphogenesis of a dissected birch leaf in vitro culture, Russ. J. Dev. Biol., 2020, vol. 51, no. 6, pp. 397–409.

    Article  CAS  Google Scholar 

  80. Maury, S., Sow, M.D., Le Gac, A.-L., et al., Phytohormone and chromatin crosstalk: the missing link for developmental plasticity?, Front. Plant Sci., 2019. https://doi.org/10.3389/fpls.2019.00395

  81. Medvedev, S.S. and Sharova, E.I., Biologiya razvitiya rastenii (Plant Developmental Biology), vol. 2: Rost i morfogenez (Growth and Morphogenesis), Nizhnevartovsk: Nizhnevart. Univ., 2014, pp. 26–30.

  82. Mendez-Hernandez, H.A., Ledezma-Rodriguez, M., Avilez-Montalvo, R.N., et al., Signaling overview of plant somatic embryogenesis, Front. Plant Sci., 2019, vol. 10. https://doi.org/10.3389/fpls.2019.00077

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

    Article  CAS  Google Scholar 

  84. Miroshnichenko, D.N., Sokolov, R.N., Alikina, O.V., et al., Screening of the regeneration potential of di-, tetra- and hexaploid cultivars and species of wheat in in vitro culture, Biotekhnologiya, 2014, no. 1, pp. 38–51.

  85. Miroshnichenko, D., Chaban, I., Chernobrovkina, M., et al., Protocol for efficient regulation of in vitro morphogenesis in einkorn (Triticum monococcum L.), a recalcitrant diploid wheat species, PLoS One, 2017. https://doi.org/10.1371/journal.pone.0173533

  86. Motte, H., Vereecke, D., Geelen, D., et al., The molecular path to in vitro shoot regeneration, Biotechnol. Adv., 2014, vol. 32, pp. 107–121.

    Article  CAS  PubMed  Google Scholar 

  87. Moubayidin, L., Perilli, S., Dello, IoioR., et al., The rate of cell differentiation controls the Arabidopsis root meristem growth phase, Curr. Biol., 2010, vol. 20, pp. 1138–1143.

    Article  CAS  PubMed  Google Scholar 

  88. Nikitina, E.D., Formative processes in the culture of immature embryos of Triticum aestivum L. and their relationship, Vestn. Altaisk. Gos. Agrarn. Univ., 2014, no. 4, pp. 48–52.

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

    Google Scholar 

  90. Nosov, A.M., Cell culture of higher plants—a unique system, model, tool, Russ. J. Plant Physiol., 1999, vol. 46, no. 6, pp. 837–844.

    Google Scholar 

  91. Ojolo, S.P., Cao, S., Priyadarshani, S., et al., Regulation of plant growth and development: a review from a chromatin remodeling perspective, Front. Plant Sci., 2018. https://doi.org/10.3389/fpls.2018.01232

  92. Oliveira, E.J., Koehler, A.D., Rocha, D.I., et al., Morpho-histological, histochemical, and molecular evidences related to cellular reprogramming during somatic embryogenesis of the model grass Brachypodium distachyon, Protoplasma, 2017, vol. 254, pp. 2017–2034.

    Article  CAS  PubMed  Google Scholar 

  93. Osborne, D. and McManus, M., Hormones, Signals and Target Cells in Plant Development, Cambridge: Cambridge Univ. Press, 2009.

    Google Scholar 

  94. Pasternak, T. and Dudits, D., Epigenetic clues to better understanding of the asexual embryogenesis in vivo and in vitro, Front. Plant Sci., 2019. https://doi.org/10.3389/fpls.2019.00778

  95. Perilli, S., Di Mambro, R., and Sabatini, S., Growth and development of the root apical meristem, Curr. Opin. Plant Biol., 2012, vol. 15, pp. 17–23.

    Article  CAS  PubMed  Google Scholar 

  96. Popielarska-Konieczna, M., Sala, K., Abdullah, M., et al., Extracellular matrix and wall composition are diverse in the organogenic and non-organogenic calli of Actinidia arguta, Plant Cell Rep., 2020. https://doi.org/10.1007/s00299-020-02530-2

  97. Pykalo, S.V. and Dubrovna, O.V., Variability of the triticale genome in vitro, Cytol. Genet., 2018, vol. 52, pp. 385–393.

    Article  Google Scholar 

  98. Radoeva, T., Lokerse, A.S., Llavata-Peris, C.I., et al., A robust auxin response network controls embryo and suspensor development through a basic helix–loop–helix transcriptional module, Plant Cell, 2019, vol. 31, pp. 52–67.

    Article  CAS  PubMed  Google Scholar 

  99. Radoeva, T., Albrecht, C., Piepers, M., et al., Suspensor-derived somatic embryogenesis in Arabidopsis, Development, 2020, vol. 147. https://doi.org/10.1242/dev.188912

  100. Rahni, R., Efroni, I., and Birnbaum, K.D., A case for distributed control of local stem cell behavior in plants, Dev. Cell, 2016, vol. 38, pp. 635–642.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Raizada, M.N., Goron, T.L., Bannerjee, O., et al., Loss of developmental pluripotency occurs in two stages during leaf aging in Arabidopsis thaliana, In Vitro Cell Dev. Biol. Plant, 2017, vol. 53, pp. 178–187.

    Article  CAS  Google Scholar 

  102. Rakshit, S., Rashid, Z., Sekhar, J.C., et al., Callus induction and whole plant regeneration in elite Indian maize (Zea mays L.) inbreds, Plant Cell Tiss. Organ Cult., 2010, vol. 100, pp. 31–37.

    Article  Google Scholar 

  103. Rober-Kleber, N., Albrechtova, J.T.P., Fleig, S., et al., Plasma membrane H+-ATPase is involved in auxin-mediated cell elongation during wheat embryo development, J. Plant Physiol., 2003, vol. 131, pp. 1302–1312.

    Article  CAS  Google Scholar 

  104. Rocha, D.I., Vieira, L.M., Koehler, A.D., et al., Cellular and morpho-histological foundations of in vitro plant regeneration, in Plant Cell Culture Protocols, Methods in Molecular Biology, New York, N.Y.: Humana Press, 2018, vol. 1815, pp. 47–68.

  105. Romanenko, K.O., Babenko, L.M., Vasheka, O.V., et al., In vitro phytohormonal regulation of fern gametophytes growth and development, Russ. J. Dev. Biol., 2020, vol. 51, pp. 71–83.

    Article  CAS  Google Scholar 

  106. Sahoo, S.A., Jha, Z., Verulkar, S.B., et al., High-throughput cell analysis based protocol for ploidy determination in anther-derived rice callus, Plant Cell Tiss. Organ Cult., 2019. https://doi.org/10.1007/s11240-019-01561-2

  107. Schuster, C., Gaillochet, C., Medzihradszky, A., et al., A regulatory framework for shoot stem cell control integrating metabolic, transcriptional, and phytohormone signals, Dev. Cell, 2014, vol. 28, pp. 438–449.

    Article  CAS  PubMed  Google Scholar 

  108. Seldimirova, O.A. and Kruglova, N.N., Properties of the initial stages of embryoidogenesis in vitro in wheat calli of various origin, Biol. Bull. (Moscow), 2013, vol. 40, no. 5, pp. 447–454.

    Article  Google Scholar 

  109. Seldimirova, O.A. and Kruglova, N.N., Balance of endogenous and exogenous hormones and pathways of morphogenesis in androclinic calluses of wheat in vitro, Izv. Ufimsk. Nauchn. Tsentra Ross. Akad. Nauk, 2015, vol. 1, pp. 33–39.

    Google Scholar 

  110. 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 

  111. Seldimirova, O.A., Kudoyarova, G.R., Kruglova, N.N., et al., 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 

  112. Seldimirova, O.A., Galin, I.R., Kruglova, N.N., et al., Distribution of IAA and ABA in developing wheat germ in vivo, Izv. Ufimsk. Nauchn. Tsentra Ross. Akad. Nauk, 2017a, no. 3, pp. 114–118.

  113. Seldimirova, O.A., Kruglova, N.N., Titova, G.E., et al., Comparative ultrastuctural 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, pp. 185–197.

    Article  Google Scholar 

  114. Seldimirova, O.A., Galin, I.R., Kudoyarova, G.R., et al., The effect of ABA on the maturation of barley embryos in vivo: the results of studying the ABA-deficient AZ34 mutant, Ekobiotekhnologiya, 2018a, vol. 1, no. 4, pp. 203–211.

    Google Scholar 

  115. Seldimirova, O.A., Kruglova, N.N., Galin, I.R., et al., Comparative assessment of IAA, ABA and cytokinin levels in in vivo embryogenesis of Steptoe barley and its ABA-deficient mutant AZ34, Ekobiotekhnologiya, 2018b, vol. 1, no. 3, pp. 134–142.

    Google Scholar 

  116. Seldimirova, O.A., Kudoyarova, G.R., Katsuhara, M., et al., Dynamics of the contents and distribution of ABA, auxins and aquaporins in developing caryopses of ABA-deficient barley mutant and its parental cultivar, Seed Sci. Res., 2019a, vol. 29, pp. 1–9.

    Article  CAS  Google Scholar 

  117. Seldimirova, O.A., Kudoyarova, G.R., Kruglova, N.N., et al., Somatic embryogenesis in wheat and barley callus in vitro is determined by the local of indoleacetic and abscisic acids, Russ. J. Dev. Biol., 2019b, vol. 50, pp. 124–135.

    Article  CAS  Google Scholar 

  118. Shamrov, I.I., Semyazachatok tsvetkovykh rastenii: stroenie, funktsii, proiskhozhdenie (The Ovule of Flowering Plants: Structure, Functions, and Origin), Moscow: KMK, 2008.

  119. Shen, Y., Jiang, Z., Yao, X., et al., Genome expression profile analysis of the immature maize embryo during dedifferentiation, PLoS One, 2012, vol. 7. https://doi.org/10.1371/journal.pone.0032237

  120. Shin, J. and Seo, P.J., Varying auxin levels induce distinct pluripotent states in callus cells, Front. Plant Sci., 2018. https://doi.org/10.3389/fpls.2018.01653

  121. Short, E., Leighton, M., Imriz, G., et al., Epidermal expression of a sterol biosynthesis gene regulates root growth by a non-cell-autonomous mechanism in Arabidopsis, Development, 2018, vol. 145. https://doi.org/10.1242/dev.160572

  122. Singh, A., Gautam, V., Singh, S., et al., Plant small RNAs: advancement in the understanding of biogenesis and role in plant development, Planta, 2018, vol. 248, pp. 545–558.

    Article  CAS  PubMed  Google Scholar 

  123. Skoog, F. and Miller, C.O., Chemical regulation of growth and organ formation in plant tissues cultured in vitro, Symp. Soc. Exp. Biol.: Proceed., 1957, vol. 11, pp. 118–130.

    CAS  Google Scholar 

  124. Slesak, H., Goralski, G., Pawłowska, H., et al., The effect of genotype on a barley scutella culture. Histological aspects, Cent. Eur. J. Biol., 2013, vol. 8, pp. 30–37.

    CAS  Google Scholar 

  125. Smit, M.E., Llavata-Peris, C.I., Roosjen, M., et al., Specification and regulation of vascular tissue identity in the Arabidopsis embryo, Development, 2020, vol. 147. https://doi.org/10.1242/dev.186130

  126. Su, Y.H., Liu, Y.B., and Zhang, X.S., Auxin-cytokinin interaction regulates meristem development, Mol. Plant, 2011, vol. 4, pp. 616–625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Sugimoto, K., Jiao, I., and Meyerowith, E.M., Arabidopsis regeneration from multiple tissues occurs via root development pathway, Dev. Cell, 2010, vol. 18, pp. 463–471.

    Article  CAS  PubMed  Google Scholar 

  128. Sugimoto, K., Gordon, S.P., and Meyerowitz, E.M., Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation?, Trends Cell Biol., 2011, vol. 21, pp. 212–218.

    Article  CAS  PubMed  Google Scholar 

  129. Sugiyama, M., Historical review of research on plant cell dedifferentiation, J. Plant Res., 2015, vol. 128, pp. 349–359.

    Article  CAS  PubMed  Google Scholar 

  130. Sun, L., Wu, Y., Zou, H., et al., Comparative proteomic analysis of the H99 inbred maize (Zea mays L.) line in embryogenic and non-embryogenic callus during somatic embryogenesis, Plant Cell Tiss. Organ Cult., 2013, vol. 113, pp. 103–119.

    Article  CAS  Google Scholar 

  131. Sun, R.Z., Zuo, E.H., Qi, J.F., et al., A role of age-dependent DNA methylation reprogramming in regulating the regeneration capacity of Boea hygrometrica leaves, Funct. Integr. Genomics, 2019. https://doi.org/10.1007/s10142-019-00701-3

  132. Tian, R., Paul, P., Joshi, S., et al., Genetic activity during early plant embryogenesis, Biochem. J., 2020, vol. 477, pp. 3743–3767.

    Article  CAS  PubMed  Google Scholar 

  133. Titova, G.E., Seldimirova, O.A., Kruglova, N.N., et al., Phenomenon of “siamese embryos” in cereals in vivo and in vitro: cleavage polyembryony and fasciations, Russ. J. Dev. Biol., 2016, vol. 47, pp. 122–137.

    Article  Google Scholar 

  134. Tuskan, G.A., Mewalal, R., Gunter, L.E., et al., Defining the genetic components of callus formation: a GWAS approach, PLoS One, 2018, vol. 17. https://doi.org/10.1371/journal.pone.0202519

  135. 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 

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

    Article  CAS  Google Scholar 

  137. De Vries, S.C. and Weijers, D., Plant embryogenesis, Curr. Biol., 2017, vol. 27, pp. 870–873.

    Article  CAS  Google Scholar 

  138. Wang, C., Wang, G., Gao, Y., et al., A cytokinin-activation enzyme-like gene improves grain yield under various field conditions in rice, Plant. Mol. Biol., 2019. https://doi.org/10.1007/s11103-019-00952-5

  139. Wendrich, J.R., Möller, B.K., Uddin, B., et al., 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 

  140. Wolpert, L., Positional information and pattern formation, Curr. Top. Dev. Biol., 2016, vol. 117, pp. 597–608.

    Article  PubMed  Google Scholar 

  141. Wu, K., Wang, J., Kong, Z., et al., 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 

  142. Xu, Y., Zhang, W., Gao, Y., et al., Proteomic analysis of embryo development in rice (Oryza sativa), Planta, 2011. https://doi.org/10.1007/s00425-011-1535-4

  143. Xu, C., Cao, H., Zhang, Q., et al., Control of auxin-induced callus formation by bZIP59–LBD complex in Arabidopsis regeneration, Nat. Plants, 2018, vol. 4, pp. 108–115.

    Article  CAS  PubMed  Google Scholar 

  144. Yu, J., Liu, W., Liu, J., et al., Auxin control of root organogenesis from callus in tissue culture, Front. Plant Sci., 2017, vol. 8. https://doi.org/10.3389/fpls.2017.01385

  145. Yu, Y., Qin, W., Li, Y., et al., Red light promotes cotton embryogenic callus formation by influencing endogenous hormones, polyamines and antioxidative enzyme activities, Plant Growth Regul., 2019, vol. 87, pp. 187–199.

    Article  CAS  Google Scholar 

  146. Zhang, W., Wang, X., Fan, R., et al., 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 

  147. Zhang, W., Cao, Z., Zhou, Q., et al., Grain filling characteristics and their relations with endogenous hormones in large- and small-grain mutants of rice, PLoS One, 2016, vol. 11. https://doi.org/10.1371/journal.pone.0165321

  148. 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 

  149. 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 

  150. Zhao, S., Jiang, Q.-T., Ma, J., et al., Characterization and expression analysis of WOX2 homeodomain transcription factor in Aegilops tauschii, Genet. Mol. Biol., 2015, vol. 38, pp. 79–85.

    Article  CAS  PubMed  Google Scholar 

  151. Zhao, J., Yu, N., Ju, M., et al., ABC transporter OsABCG18 controls the shootward transport of cytokinins and grain yield in rice, J. Exp. Bot., 2019. https://doi.org/10.1093/jxb/erz382

  152. Zhuravlev, Yu.N. and Omel’ko, A.M., Morphogenesis in plants in vitro, Russ. J. Plant Physiol., 2008, vol. 55, no. 5, pp. 643–664.

    Article  CAS  Google Scholar 

  153. Zinatullina, A.E., Cytophysiological features of contrast types of calli in vitro, Usp. Sovrem. Biol., 2020, vol. 140, no. 1, pp. 183–194.

    Google Scholar 

  154. Zur, I., Dubas, E., Krzewska, M., et al., Current insights into hormonal regulation of microspore embryogenesis, Front. Plant Sci., 2016, pp. 110–109.

Download references

Funding

The article was prepared in the course of the implementation of the topics no. АААА-А18-118022190099-6 (Ufa Institute of Biology, Ufa Federal Research Center, Russian Academy of Sciences, State Assignment of the Ministry of Science and Higher Education of the Russian Federation no. 075-00326-19-00) and no. АААА-А18-118051590112-8 (Komarov Botanical Institute, Russian Academy of Sciences) within the framework of the agreement on creative cooperation between the institutes.

Author information

Authors and Affiliations

  1. Ufa Institute of Biology, Ufa Federal Research Center, Russian Academy of Sciences, 450054, Ufa, Russia

    N. N. Kruglova, O. A. Seldimirova & A. E. Zinatullina

  2. Komarov Botanical Institute, Russian Academy of Sciences, 197376, St. Petersburg, Russia

    G. E. Titova

Authors
  1. N. N. Kruglova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. E. Titova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. A. Seldimirova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. E. Zinatullina
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N.N. Kruglova, O.A. Seldimirova, and A.E. Zinatullina prepared the initial version of the review text using the literature and original data. G.E. Titova analyzed the main statements of the article and made valuable additions. All the authors participated in the discussion of the final version of the article.

Corresponding author

Correspondence to N. N. Kruglova.

Ethics declarations

The authors declare that they have no conflict of interests.

This article does not contain any studies involving human participants or laboratory animals as experimental models performed by the authors.

Additional information

Translated by A. Ermakov

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kruglova, N.N., Titova, G.E., Seldimirova, O.A. et al. Cytophysiological Features of the Cereal-Based Experimental System “Embryo In Vivo–Callus In Vitro”. Russ J Dev Biol 52, 199–214 (2021). https://doi.org/10.1134/S1062360421040044

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360421040044

Keywords:

Search

Navigation