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Origination of asexual plantlets in three species of Crassulaceae

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Abstract

During asexual plant reproduction, cells from different organs can be reprogrammed to produce new individuals, a process that requires the coordination of cell cycle reactivation with the acquisition of other cellular morphological characteristics. However, the factors that influence the variety of asexual reproduction have not yet been determined. Here, we report on plantlet formation in Kalanchoe daigremontiana, Graptopetalum paraguayense, and Crassula portulacea (Crassulaceae) and analyse the effect of initiating cells on asexual reproduction in these three species. Additionally, the roles of WUSCHEL (WUS) and CUP-SHAPED COTYLEDON 1 (CUC1) in the asexual reproduction of these species were analysed through qRT-PCR. Our results indicated that pre-existing stem cell-like cells at the sites of asexual reproduction were responsible for the formation of plantlets. These cells were arrested in different phases of the cell cycle and showed different cell morphological characteristics and cell counts. The accumulation of auxin and cytokinin at the sites of asexual plantlet formation indicated their important functions, particularly for cell cycle reactivation. These differences may influence the pattern and complexity of asexual reproduction in these Crassulaceae species. Additionally, the dynamic expression levels of CUC1 and WUS may indicate that CUC1 functions in the formation of callus and shoot meristems; whereas, WUS was only associated with shoot induction.

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References

  • Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc'h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57:626–644

    Article  CAS  PubMed  Google Scholar 

  • Barbara B, Lieven DV (2009) Transcriptional control of the cell cycle. Curr Opin Plant Biol 12:599–605

    Article  Google Scholar 

  • Cary AJ, Che P, Howell SH (2002) Developmental events and shoot apical meristem gene expression patterns during shoot development in Arabidopsis thaliana. Plant J 32:867–877

    Article  CAS  PubMed  Google Scholar 

  • Charuvi D, Kiss V, Nevo R, Shimoni E, Adam Z, Reich Z (2012) Gain and loss of photosynthetic membranes during plastid differentiation in the shoot apex of Arabidopsis. Plant Cell 24:1143–1157

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Che P, Lall S, Howell SH (2007) Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture. Planta 226:1183–1194

    Article  CAS  PubMed  Google Scholar 

  • Daimon Y, Takabe K, Tasaka M (2003) The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant Cell Physiol 44:113–121

    Article  CAS  PubMed  Google Scholar 

  • Den BG, Murray JA (2000) Triggering the cell cycle in plants. Trends Cell Biol 10:245–250

    Article  Google Scholar 

  • Dubrovsky JG, Doerner PW, Colon-Carmona A, Rost TL (2000) Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol 124:1648–1657

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fleming A (2006a) Metabolic aspects of organogenesis in the shoot apical meristem. J Exp Bot 57:1863–1870

    Article  CAS  PubMed  Google Scholar 

  • Fleming A (2006b) The co-ordination of cell division, differentiation and morphogenesis in the shoot apical meristem: a perspective. J Exp Bot 57:25–32

    Article  CAS  PubMed  Google Scholar 

  • Garcês HM, Champagne CE, Townsley BT, Park S, Malhó R, Pedroso MC, Harada JJ, Sinha NR (2007) Evolution of asexual reproduction in leaves of the genus Kalanchoe. Proc Natl Acad Sci U S A 104:15578–15583

    Article  PubMed Central  PubMed  Google Scholar 

  • Gau RJ (2003) Plant tissue culture: the history, In: Plant Tissue Culture: 100 Years since Gottlieb Haberlandt, Springer Wien

  • Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134:3539–3548

    Article  CAS  PubMed  Google Scholar 

  • Haywood V, Kragler F, Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14:S303–S325

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kaoru S, Sean PG, Elliot MM (2011) Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol 21:212–218

    Article  Google Scholar 

  • Kenneth DB, Alejandro SA (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697–710

    Article  Google Scholar 

  • Koroleva OA, Tomlinson M, Parinyapong P, Sakvarelidze L, Leader D, Shaw P (2004) CycD1, a putative G1 cyclin from Antirrhinum majus, accelerates the cell cycle in cultured tobacco BY-2 cells by enhancing both G1/S entry and progression through S and G2 phases. Plant Cell 16:2364–2379

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kurata T, Okada K, Wada T (2005) Intercellular movement of transcription factors. Curr Opin Plant Biol 8:600–605

    Article  CAS  PubMed  Google Scholar 

  • Laux T (2003) The stem cell concept in plants: a matter of debate. Cell 113:281–283

    Article  CAS  PubMed  Google Scholar 

  • Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7(8):e1002243

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lieven DV, Jerome J, Dirk I (2003) Plant cell cycle transitions. Curr Opin Plant Biol 6:536–543

    Article  Google Scholar 

  • Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035

    CAS  PubMed  Google Scholar 

  • Lopez-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49:557–577

    Article  CAS  PubMed  Google Scholar 

  • Marcel M, James AH (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4:44–49

    Article  Google Scholar 

  • Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815

    Article  CAS  PubMed  Google Scholar 

  • Planchais S, Glab N, Inze D, Bergounioux C (2000) Chemical inhibitors: a tool for plant cell cycle studies. FEBS Lett 476:78–83

    Article  CAS  PubMed  Google Scholar 

  • Quelo AH, Bryant JA, Verbelen JP (2002) Endoreduplication is not inhibited but induced by aphidicolin in cultured cells of tobacco. J Exp Bot 53:669–675

    Article  CAS  PubMed  Google Scholar 

  • Richard GK (2006) Cytokinins inhibit epiphyllous plantlet development on leaves of Bryophyllum (Kalanchoe) marnierianum. J Exp Bot 57:4089–4098

    Article  Google Scholar 

  • Richard GK (2008) Hormonal control of root development on epiphyllous plantlets of Bryophyllum (Kalanchoe) marnierianum: role of auxin and ethylene. J Exp Bot 59:2361–2370

    Article  Google Scholar 

  • Sablowski R (2004) Plant and animal stem cells: conceptually similar, molecularly distinct? Trends Cell Biol 14:605–611

    Article  CAS  PubMed  Google Scholar 

  • Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644

    Article  CAS  PubMed  Google Scholar 

  • Schween G, Gorr G, Hohe A, Reski R (2003) Unique tissue specific cell cycle in Physcomitrella. Plant Biol 5:50–58

    Article  Google Scholar 

  • Singh MB, Bhalla PL (2006) Plant stem cells carve their own niche. Trends Plant Sci 11:241–246

    Article  CAS  PubMed  Google Scholar 

  • Skoog F (1950) Chemical control of growth and organ formation in plant tissues. Annee Biol 54:545–562

    CAS  PubMed  Google Scholar 

  • Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 54:118–130

    Google Scholar 

  • Slaby K, Sebanek J (1984) Content of endogenous cytokinins in intact and transversally cut leaf blades of Bryophyllum crenatum. Plant Growth Regul 2:111–116

    Article  CAS  Google Scholar 

  • Slaby K, Sebanek J, Psota V (1990) The release of primordial of marginal buds on Bryophyllum crenatum leaves from growth inhibition in relationship to the level of endogenous IAA. Biol Plant 32:352–356

    Article  CAS  Google Scholar 

  • Street HE (1977) Plant tissue and cell culture. Blackwell Scientific Publications

  • Su YH, Zhao XY, Liu YB, Zhang CL, O'Neill SD, Zhang XS (2009) Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J 59:448–460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471

    Article  CAS  PubMed  Google Scholar 

  • Tatyana B (2004) Polymorphism of sexual and somatic embryos as manifestation of their developmental parallelism under natural conditions and in tissue culture. Plant Biotechnology and Molecular Markers, Anamaya Publications. 43–59

  • Tatyana B (2005) Sexual and asexual processes in reproductive systems of flowering plants. Acta Biol Cracov Ser Bot 47:51–60

    Google Scholar 

  • Ueki S, Citovsky V (2005) Control improves with age: intercellular transport in plant embryos and adults. Proc Natl Acad Sci U S A 102:1817–1818

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Verdeil JL, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:245–252

    Article  CAS  PubMed  Google Scholar 

  • Weigel D, Jurgens G (2002) Stem cells that make stems. Nature 415:751–754

    Article  CAS  PubMed  Google Scholar 

  • Williams L, Fletcher JC (2005) Stem cell regulation in the Arabidopsis shoot apical meristem. Curr Opin Plant Biol 8:582–586

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Feng Z, Wang G, Li F, Du X, Zhu J (2010) Initiation of dedifferentiation and structural changes in in vitro cultured petiole of Arabidopsis thaliana. Protoplasma 241:75–81

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Sciences Foundation of China (nos. 31370214, 31301058), the Major State Basic Research Development Program (973 Program) of China (No. 2012CB966903), and the Key Programme for Basic Research of the Science and Technology Commission of Shanghai (13JC1407102).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Molecular and Cell Biology, School of Life Science and Technology, Tongji University, Shanghai, 200092, China

    Jiansheng Guo, Yangyang He, Xianghuan Cui, Xiling Du & Jian Zhu

  2. Translational Center for Stem Cell Research, Tongji University School of Medicine, Tongji Hospital, Shanghai, 200065, China

    Hailiang Liu

  3. College of Life Science of Shihezi University, Shihezi, Xinjiang, 832003, China

    Hailiang Liu

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  1. Jiansheng Guo
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  2. Hailiang Liu
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  3. Yangyang He
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  4. Xianghuan Cui
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  5. Xiling Du
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  6. Jian Zhu
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Correspondence to Jian Zhu.

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Handling Editor: Liwen Jiang

Jiansheng Guo and Hailiang Liu contributed equally to this work

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Guo, J., Liu, H., He, Y. et al. Origination of asexual plantlets in three species of Crassulaceae . Protoplasma 252, 591–603 (2015). https://doi.org/10.1007/s00709-014-0704-2

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