Skip to main content
SpringerLink
Log in

Callusogenesis as an in vitro Morphogenesis Pathway in Cereals

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

Abstract

Callus is an integrated system formed both exogenously (as a result of proliferation of surface cells of different plant tissues) and endogenously (deep in tissues). Initially, callus consists of homogeneous cells gradually transforming into a system of groups of heterogeneous cells with species-specific morphogenetic potencies, which are realized via various pathways of morphogenesis. In this review, issues associated with studying the formation of calli in in vitro cultures of immature anthers and embryos of cultivated cereals are analyzed. Distinguishing the critical stages of callusogenesis is proposed. The features of hemmorhizogenesis in vitro as a type of organogenesis in calli are considered. The concept of the versatility of the processes of plant morphogenesis in vivo, in situ, and in vitro proposed by T.B. Batygina (1987, 1999, 2012, 2014) is confirmed. The prospects of the approach to calli as model systems for studying various problems of plant developmental biology are 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

Similar content being viewed by others

References

  • De Almeida, W.A.B., de Mourao, F.F., Mendes, B.M.J., et al., Histological characterization of in vitro adventitious organogenesis in citrus sinensis, Biol. Plant., 2006, vol. 50, no. 3, pp. 321–325.

    Article  Google Scholar 

  • Ashapkin, V.V., Kutueva, L.I., and Vanyushin, B.F., Epigenetic variability in plants: heritability, adaptability, evolutionary significance, Russ. J. Plant Physiol., 2016, vol. 63, no. 2, pp. 181–192.

    Article  CAS  Google Scholar 

  • Barlou, P.U., Cell division in the meristems and the significance of this process for organogenesis and morphogenesis in plants, Ontogenez, 1994, vol. 25, no. 5, pp. 5–27.

    Google Scholar 

  • Batygina, T.B., Khlebnoe zerno: atlas (Bread Grain: An Atlas), Leningrad: Nauka, 1987.

    Google Scholar 

  • Batygina, T.B., Embryogenesis and morphogenesis of zygotic and somatic embryos, Russ. J. Plant Physiol., 1999, vol. 46, no. 6, pp. 774–778.

    CAS  Google Scholar 

  • Batygina, T.B., Reproduction, propagation, and renewal of plants, in 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, pp. 35–39.

    Google Scholar 

  • Batygina, T.B., Sexual and asexual processes in reproductive systems of flowering plants, Acta Biol. Cracov. Ser. Bot., 2005, vol. 47, no. 1, pp. 51–60.

    Google Scholar 

  • Batygina, T.B., Stem cells and morphogenetic developmental programs in plants, Stem Cell Res. J., 2011, vol. 3, nos. 1–2, pp. 45–120.

    Google Scholar 

  • Batygina, T.B., Integrity and reliability system in ontogenesis and evolution, Int. J. Plant Reprod. Biol., 2012, vol. 4, no. 2, pp. 107–120.

    Google Scholar 

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

    Google Scholar 

  • Batygina, T.B. and Osadchii, Ya.V., Detection of the homology of the cellular elements of reproductive and morphogenetic structures, Usp. Sovrem. Biol., 2015, vol. 135, no. 4, pp. 337–345.

    Google Scholar 

  • Batygina, T.B. and Rudskii, I.V., Role of stem cells in plant morphogenesis, Dokl. Biol. Sci., 2006, vol. 410, pp. 400–402.

    Article  PubMed  CAS  Google Scholar 

  • Batygina, T.B. and Vasilyeva, V.E., Periodization of development of reproductive structures. Critical periods, Acta Biol. Cracov. Ser. Bot., 2003, vol. 45, no. 1, pp. 27–36.

    Google Scholar 

  • Batygina, T.B., Vasil’eva, V.E., and Mamet’eva, T.B., Problems of morphogenesis in vivo and in vitro (embryogenesis in angiosperms), Bot. Zh., 1978, vol. 63, no. 1, pp. 87–111.

    Google Scholar 

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

    Google Scholar 

  • Beloussov, L.V., Biologicheskii morfogenez (Biological Morphogenesis), Moscow: Mosk. Gos. Univ., 1987.

    Google Scholar 

  • Beloussov, L.V., On the origin of novelty in the evolution and ontogeny, Zh. Obshch. Biol., 1990, vol. 51, no. 1, pp. 107–115.

    Google Scholar 

  • Bertalanfi, L., General systems theory: a critical review, in Issledovaniya po obshchei teorii sistem (Research on the General Systems Theory), Moscow: Progress, 1969, pp. 23–82.

    Google Scholar 

  • Bevitori, R., Popielarska-Konieczna, M., dos Santos, E.M., et al., Morpho-anatomical characterization of mature embryo-derived callus of rice (Oryza sativa L.) suitable for transformation, Protoplasma, 2014, vol. 251, no. 5, pp. 545–554.

    PubMed  CAS  Google Scholar 

  • Bishimbaeva, N.K., Cytophysiological bases of biotechnology of continuous regeneration of plants in cereal tissue culture, Extended Abstract of Doctoral (Biol.) Dissertation, Almaty, 2007.

    Google Scholar 

  • Butenko, R.G., Kul’tura izolirovannykh tkanei i fiziologiya morfogeneza rastenii (Isolated Tissue Culture and Plant Morphogenesis Physiology), Moscow: Nauka, 1964.

    Google Scholar 

  • Butenko, R.G., Cellular and molecular aspects of plant morphogenesis in vitro, in I Chailakhyanovskie chteniya (I Chailakhyan Lectures), Pushchino: Pushch. Nauchn. Tsentr, 1994, pp. 7–26.

    Google Scholar 

  • Bykova, E.A., Chergintsev, D.A., Vlasova, T.A., and Chub, V.V., 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, no. 4, pp. 207–215.

    Article  CAS  Google Scholar 

  • Bystrova, E.I., Zhukovskaya, N.V., Rakitin, V.Yu., and Ivanov, V.B., Role of ethylene in activation of cell division in quiescent center of excised maize roots, Russ. J. Dev. Biol., 2015, vol. 46, no. 2, pp. 60–64.

    Article  CAS  Google Scholar 

  • Chaum, S., Srianan, B., Pichakum, A., et al., An efficient procedure for embryogenic callus induction and double haploid plant regeneration through anther culture of Thai aromatic rice (Oryza sativa L. subsp. indica), InVitro Cell Dev. Biol. Plant., 2009, vol. 45, pp. 171–179.

    Article  Google Scholar 

  • Che, P., Lall, S., Nettleton, D., and Howell, S.H., Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture, Plant Physiol., 2006, vol. 141, no. 2, pp. 620–637.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, no. 1, pp. 240–251.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Choob, V.V. and Sinyushin, A.A., Flower and shoot fasciation: from phenomenology to the construction of models of apical meristem transformations, Russ. J. Plant Physiol., 2012, vol. 59, no. 4, pp. 530–545.

    Article  CAS  Google Scholar 

  • Colebrook, E.H., Thomas, S.G., Phillips, A.L., et al., The role of gibberellin signalling in plant responses to abiotic stress, J. Exp. Biol., 2014, vol. 217, pp. 67–75.

    Article  PubMed  CAS  Google Scholar 

  • Delporte, F., Pretova, A., du Jardin, P., et al., Morpho-histology and genotype dependence of in vitro morphogenesis in mature embryo cultures of wheat, Protoplasma, 2014, vol. 251, no. 6, pp. 1455–1470.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dodueva, I.E., Tvorogova, V.E., Azarakhsh, M., et al., Plant stem cells: the unity and diversity, Vavilov. Zh. Genet. Selekts., 2016, vol. 20, no. 4, pp. 441–458.

    Google Scholar 

  • Doubled Haploidy in Model and Recalcitrant Species, Segui-Simarro, J.M., Ed., Lausanne: Frontiers Media, 2016.

  • Dubrovna, O.V. and Bavol, A.V., Variability of the wheat genome during in vitro culture, Cytol. Genet., 2011, vol. 45, no. 5, pp. 333–340.

    Article  Google Scholar 

  • Ebrahimie, E., Naghavi, M.R., Hosseinzadeh, A., et al., Induction and comparison of different in vitro morphogenesis pathways using embryo of cumin (Cuminum cyminum L.) as a model material, Plant Cell, Tiss. Org. Cult., 2007, vol. 90, no. 3, pp. 293–311.

    Article  Google Scholar 

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

    Google Scholar 

  • Ellis, M., Egelund, J., Schultz, C.J., and Bacic, A., Arabinogalactan-proteins: key regulators at the cell surface?, Plant Physiol., 2010, vol. 153, no. 2, pp. 403–419.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ermakov, I.P. and Matveeva, N.P., Pollen dimorphism and androgenesis in antheral and microspore culture, Vestn. Mosk. Univ., Ser. 16: Biol., 1986, no. 3, pp. 28–40.

    Google Scholar 

  • 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. 273–286.

    Article  CAS  Google Scholar 

  • Ezhova, T.A., Genetic control of morphogenesis and plant tolerance to stressors, Extended Abstract of Doctoral (Biol.) Dissertation, Moscow, 2003.

    Google Scholar 

  • Gilbert, S.F., Developmental Biology, Sunderland, MA: Sinauer Associates, 1988, vol. 3, 2nd ed.

    Google Scholar 

  • Gorbunova, V.Yu., Kruglova, N.N., and Abramov, S.N., The induction of androgenesis in vitro in spring soft wheat. Balance of exogenous and endogenous phytohormones, Biol. Bull. (Moscow), 2001, vol. 28, no. 1, pp. 25–30.

    Article  CAS  Google Scholar 

  • Gutierrez, R.A., Shasha, D.E., and Coruzzi, G.M., Systems biology for the virtual plant, Plant Physiol., 2005, vol. 138, pp. 550–554.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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, no. 2, pp. 257–263.

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Isaeva, V.V., Kletki v morfogeneze (Cells in Morphogenesis), Moscow: Nauka, 1994.

    Google Scholar 

  • Isaeva, V.V., Self-organization in biological systems, Biol. Bull. (Moscow), 2012, vol. 39, no. 2, pp. 110–118.

    Article  Google Scholar 

  • Ivanov, V.B., The problem of stem cells in plants, Russ. J. Dev. Biol., 2003, vol. 34, no. 4, pp. 205–212.

    Article  Google Scholar 

  • Ivanov, V.B., Stem cells in the root and the problem of stem cells in plants, Russ. J. Dev. Biol., 2007, vol. 38, no. 6, pp. 338–349.

    Article  Google Scholar 

  • Ivanov, V.B., Kletochnye mekhanizmy rosta rastenii (Cellular Mechanisms of Plant Growth), Moscow: Nauka, 2011.

    Google Scholar 

  • Jaeger, J., Irons, D., and Monk, N., Regulative feedback in pattern formation: towards a general relativistic theory of positional information, Development, 2008, vol. 135, no. 19, pp. 3175–3183.

    Article  PubMed  CAS  Google Scholar 

  • Jaligot, E., Rival, A., Beule, T., et al., Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis, Plant Cell Rep., 2000, vol. 19, pp. 684–690.

    Article  CAS  Google Scholar 

  • Konieczny, R., Swierczynska, J., Czaplicki, A.Z., and Bohdanowicz, J., Distribution of pectin and arabinogalactan protein epitopes during organogenesis from androgenic callus of wheat, Plant Cell Rep., 2007, vol. 26, no. 3, pp. 355–363.

    Article  PubMed  CAS  Google Scholar 

  • Korochkin, L.I., Biologiya individual’nogo razvitiya (Biology of Individual Development), Moscow: Mosk. Gos. Univ., 2002.

    Google Scholar 

  • Kruglova, N.N., Cereal microspore as a model system to study pathways of morphogenesis, Extended Abstract of Doctoral (Biol.) Dissertation, St. Petersburg, 2002.

    Google Scholar 

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

    Google Scholar 

  • Kruglova, N.N. and Batygina, T.B., Stress as a factor inducing androcliny in cereals: a competent object of stress, Usp. Sovrem. Biol., 2001, vol. 121, no. 1, pp. 67–78.

    Google Scholar 

  • 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 

  • Kruglova, N.N. and Seldimirova, O.A., Morphogenesis in androcline calli of cereals: cytohistological features, Usp. Sovrem. Biol., 2010, vol. 130, no. 3, pp. 247–257.

    Google Scholar 

  • Kruglova, N.N. and Seldimirova, O.A., Regeneratsiya pshenitsy in vitro i ex vitro: tsito-gistologicheskie aspekty (Wheat Regeneration in vitro and ex vitro: Cytohistological Aspects), Ufa: Gilem, 2011.

    Google Scholar 

  • Kruglova, N.N. and Seldimirova, O.A., In vitro morphogenesis pathways of wheat androcline callus cells, Fiziol. Rast. Genet., 2013, vol. 45, no. 5, pp. 382–389.

    Google Scholar 

  • Kruglova, N.N., Gorbunova, V.Yu., Abramov, S.N., et al., Wheat androgenic embryoids and calli: data of scanning electron microscopy, Biol. Bull. (Moscow), 2001, vol. 28, no. 2, pp. 150–156.

    Article  Google Scholar 

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

    Google Scholar 

  • Kumar, V., Systems biology approaches towards the prediction of prospective novel plant system-derived products or services, Biol. Syst. Open Access, 2013, vol. 2, no. 4, p. 119. doi 10.4172/2329-6577.100011.

    Article  Google Scholar 

  • Kunakh, V.A., Plant genome variation in the course of in vitro dedifferentiation and callus formation, Russ. J. Plant Physiol., 1999, vol. 46, no. 6, pp. 808–817.

    CAS  Google Scholar 

  • Kurdyukov, S., Song, Y., Sheahan, M.B., et al., Transcriptional regulation of early embryo development in the model legume Medicago truncatula, Plant Cell Rep., 2014, vol. 33, no. 2, pp. 349–362.

    Article  PubMed  CAS  Google Scholar 

  • Lee, S.-T. and Huang, W.-L., Cytokinin, auxin, and abscisic acid affects sucrose metabolism conduce to de novo shoot organogenesis in rice (Oryza sativa L.) callus, Bot. Stud., 2013, vol. 54, no. 5. http://www.asbotanicalstudies. com/content/54/1/5.

    Google Scholar 

  • Lutova, L.A., Ezhova, T.A., Dodueva, I.E., and Osipova, M.A., Genetika razvitiya rastenii (Plant Developmental Genetics), Inge-Vechtomov, S.G., Ed., St. Petersburg: Izd. N-L, 2010.

    Google Scholar 

  • Marchenko, A.O., Realization of the morphogenetic potential of plants, Usp. Sovrem. Biol., 1996, vol. 116, no. 3, pp. 306–319.

    Google Scholar 

  • Marzec, M. and Kurczynska, E., Importance of symplasmic communication in cell differentiation, Plant Signal. Behav., 2014, vol. 9. e27931. http://dx.doi.org/10.4161/psb.27931tt.

    Google Scholar 

  • Medvedev, S.S., Mechanisms and physiological role of polarity in plants, Russ. J. Plant Physiol., 2012, vol. 59, no. 4, pp. 502–514.

    Article  CAS  Google Scholar 

  • Medvedev, S.S., Systems biology of plants, in Materialy V mezhdunarodnoi shkoly dlya molodykh uchenykh, posvyashchennoi pamyati T.B. Batyginoi (Proc. V Int. School for Young Scientists in Memory of T.B. Batygina), St. Petersburg, 2016, p. 130.

    Google Scholar 

  • Medvedev, S.S. and Sharova, E.I., Genetic and epigenetic regulation of plant development (a review), Zh. Sib. Fed. Univ., Ser. Biol., 2010, no. 3, pp. 109–129.

    Google Scholar 

  • Meristematic Tissues in Plant Growth and Development, McManus, M.T. and Veit, B., Eds., Sheffield: Sheffield Acad. Press, 2002.

  • Merks, R.M.H. and Guravage, M.A., Building simulation models of developing plant organs, in Plant Organogenesis: Methods and Protocols, De Smet, I., Ed., Methods in Molecular Biology, New York: Springer Science + Business Media, 2013, vol. 959, pp. 333–352.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Mohd Din, A.R.J., Ahmad, F.I., Wagiran, A., et al., Improvement of efficient in vitro regeneration potential of mature callus induced from Malaysian upland rice seed (Oryza sativa cv. Panderas), Saudi J. Biol. Sci., 2016, vol. 23, no. 1 (suppl.), pp. 69–77.

    Google Scholar 

  • Narciso, J.O. and Hattori, K., Genotypic differences in morphology and ultrastructures of callus derived from selected rice varieties, Philippine Sci. Lett., 2010, vol. 3, no. 1, pp. 59–65.

    Google Scholar 

  • Nosov, A.M., Plant cell culture: unique system, model, and tool, Russ. J. Plant Physiol., 1999, vol. 46, no. 6, pp. 731–738.

    CAS  Google Scholar 

  • Oliveira, E.J., Koehler, A.D., Rocha, D.I., et al., Morphohistological, histochemical, and molecular evidences related to cellular reprogramming during somatic embryogenesis of the model grass Brachypodium distachyon, Protoplasma, 2017, vol. 254, no. 5, pp. 2017–2034.

    Article  PubMed  CAS  Google Scholar 

  • Parra-Vega, V., Renau-Morata, B., Sifres, A., et al., Stress treatments and in vitro culture conditions influence microspore embryogenesis and growth of callus from anther walls of sweet pepper (Capsicum annuum L.), Plant Cell Tiss. Org. Cult., 2013, vol. 112, no. 3, pp. 353–360.

    Article  CAS  Google Scholar 

  • Patwari, P. and Lee, R.T., Mechanical control of tissue morphogenesis, Circ. Res., 2008, vol. 103, no. 3, pp. 234–243.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rębilas, K. and Rębilas, A., Auxin concentration control of the average DNA content in cells of in vitro cultures: a theoretical model and comparison to experimental data for Allium cepa and Alium sativum, Plant Cell, Tiss. Org. Cult., 2008, vol. 95, no. 1, pp. 89–99.

    Article  CAS  Google Scholar 

  • Savona, M., Mattioli, R., Nigro, S., et al., Two SERK genes are markers of pluripotency in Cyclamen persicum Mill., J. Exp. Bot., 2012, vol. 63, no. 1, pp. 471–488.

    Article  PubMed  CAS  Google Scholar 

  • Segui-Simarro, J.M., Androgenesis revisited, Bot. Rev., 2010, vol. 76, pp. 377–404.

    Article  Google Scholar 

  • 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 

  • Seldimirova, O.A. and Kruglova, N.N., Androcline embryogenesis in vitro in cereals, Usp. Sovrem. Biol., 2014, vol. 134, no. 5, pp. 476–487.

    Google Scholar 

  • Seldimirova, O.A. and Kruglova, N.N., The balance of endogenous and exogenous hormones and the pathways of morphogenesis in wheat androcline calli in vitro, Izv. Ufimsk. Nauchn. Tsentra, Ross. Akad. Nauk, 2015, no. 1, pp. 33–39.

    Google Scholar 

  • Seldimirova, O.A., Katasonova, A.A., and Kruglova, N.N., Morphogenetic focus formation as the initial stage of in vitro morphogenesis in wheat calli of various origin, Fiziol. Biokhim. Kul’t. Rast., 2011, vol. 43, no. 4, pp. 297–306.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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, no. 3, pp. 251–264.

    Google Scholar 

  • 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. Ufimsk. Nauchn. Tsentra, Ross. Akad. Nauk, 2017a, no. 3 (1), pp. 114–118.

    Google Scholar 

  • Seldimirova, O.A., Kruglova, N.N., Titova, G.E., et al., 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, vol. 3, pp. 185–197.

    Article  Google Scholar 

  • Sinnot, E., Morfogenez rastenii (Morphogenesis of Plants), Moscow: Izd. Inostr. Lit-ry, 1963.

    Google Scholar 

  • 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, no. 1, pp. 30–37.

    CAS  Google Scholar 

  • Spivak, V.A., Minlikaeva, K.I., Evseeva, N.V., et al., 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.

    Google Scholar 

  • Sugiyama, M., Historical review of research on plant cell dedifferentiation, J. Plant Res., 2015, vol. 128, no. 5, pp. 349–359.

    Article  PubMed  CAS  Google Scholar 

  • 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. Org. Cult., 2013, vol. 113, pp. 103–119.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • 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, no. 3, pp. 122–137.

    Article  Google Scholar 

  • Tyagi, N., Dahleen, L.S., and Bregitzer, P., Candidate genes within tissue culture regeneration QTL revisited with a linkage map based on transcript-derived markers, Crop Sci., 2010, vol. 50, no. 5, pp. 1697–1707.

    Article  CAS  Google Scholar 

  • Urmantsev, Yu.A., Systems approach to the problem of tolerance of plants, Fiziol. Rast, 1979, vol. 26, no. 4, pp. 762–777.

    CAS  Google Scholar 

  • Waddington, K., Morfogenez i genetika (Morphogenesis and Genetics), Moscow: Mir, 1964.

    Google Scholar 

  • Wang, X., Nolan, K.E., Irwanto, R.R., et al., Ontogeny of embryogenic callus in Medicago truncatula: the fate of the pluripotent and totipotent stem cells, Ann. Bot., 2011, vol. 107, pp. 599–609.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wendrich, J.R., Moller, 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  PubMed  PubMed Central  CAS  Google Scholar 

  • Wolfe, N.W. and Clark, N.L., ERC analysis: web-based inference of gene function via evolutionary rate covariation, Bioinformatics, 2015, vol. 31, no. 23, pp. 3835–3837.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wolpert, L., Positional information and the spatial pattern of cellular differentiation, J. Theor. Biol., 1969, vol. 25, no. 1, pp. 1–47.

    Article  PubMed  CAS  Google Scholar 

  • Zhuravlev, Yu.N. and Omel’ko, A.M., Plant morphogenesis in vitro, Russ. J. Plant Physiol., 2008, vol. 55, no. 5, pp. 579–596.

    Article  CAS  Google Scholar 

  • Zur, I., Dubas, E., Krzewska, M., et al., Current insights into hormonal regulation of microspore embryogenesis. Doubled haploidy in model and recalcitrant species, Front. Plant Sci., 2016, pp. 110–109.

    Google Scholar 

  • Zuraida, A.R., Naziah, B., Zamri, Z., et al., 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 

Download references

Author information

Authors and Affiliations

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

    N. N. Kruglova & O. A. Seldimirova

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

    G. E. Titova

  3. St. Petersburg State University, St. Petersburg, 199034, 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

Corresponding author

Correspondence to N. N. Kruglova.

Additional information

Original Russian Text © N.N. Kruglova, G.E. Titova, O.A. Seldimirova, 2018, published in Ontogenez, 2018, Vol. 49, No. 5, pp. 273–288.

In blessed memory of Corresponding Member of the Russian Academy of Sciences Tatyana Borisovna Batygina

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. Callusogenesis as an in vitro Morphogenesis Pathway in Cereals. Russ J Dev Biol 49, 245–259 (2018). https://doi.org/10.1134/S106236041805003X

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S106236041805003X

Keywords

Search

Navigation