Insights into the regenerative property of plant cells and their receptivity to transgenesis

From a holistic perspective, the discovery of cellular plasticity, a very interesting property of totipotency, underlies many topical issues in biology with important medical applications, while transgenesis is a core research tool in biology. Partially known, some basic mechanisms involved in the regenerative property of cells and in their receptivity to transgenesis are common to plant and animal cells and highlight the principle of the unity of life. Transgenesis provides an important investigative instrument in plant physiology and is regarded as a valuable tool for crop improvement. The economic, social, cultural and scientific importance of cereals has led to a rich stream of research into their genetics, biology and evolution. Sustained efforts to achieve the results obtained in the fields of genetic engineering and applied biotechnology reflect this deep interest. Difficulties encountered in creating genetically modified cereals, especially wheat, highlighted the central notions of tissue culture regeneration and transformation competencies. From the perspective of combining or encountering these competencies in the same cell lineage, this reputedly recalcitrant species provides a stimulating biological system in which to explore the physiological and genetic complexity of both competencies. The former involves two phases, dedifferentiation and redifferentiation. Cells undergo development switches regulated by extrinsic and intrinsic factors. The re-entry into the cell division cycle progressively culminates in the development of organized structures. This is achieved by global chromatin reorganization associated with the reprogramming of the gene expression pattern. The latter is linked with surveillance mechanisms and DNA repair, aimed at maintaining genome integrity before cells move into mitosis, and with those mechanisms aimed at genome expression control and regulation. In order to clarify the biological basis of these two physiological properties and their interconnectedness, we look at both competencies at the core of defense/adaptive mechanisms and survival, between undifferentiated cell proliferation and organization, constituting a transition phase between two different dynamic regimes, a typical feature of critical dynamic systems. Opting for a candidate-gene strategy, several gene families could be proposed as relevant targets for investigating this hypothesis at the molecular level.

[1]  P. Cockerill Structure and function of active chromatin and DNase I hypersensitive sites , 2011, The FEBS journal.

[2]  Z. Herceg,et al.  Histone acetylation by Trrap–Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks , 2006, Nature Cell Biology.

[3]  P. Khurana,et al.  Analysis of expression profile of selected genes expressed during auxin-induced somatic embryogenesis in leaf base system of wheat (Triticum aestivum) and their possible interactions , 2007, Plant Molecular Biology.

[4]  S. Gelvin Plant proteins involved in Agrobacterium-mediated genetic transformation. , 2010, Annual review of phytopathology.

[5]  G. Grafi The complexity of cellular dedifferentiation: implications for regenerative medicine. , 2009, Trends in biotechnology.

[6]  Ian McFarlane,et al.  The role of transgenic crops in sustainable development. , 2011, Plant biotechnology journal.

[7]  A. Fehér Why somatic plant cells start to form embryos , 2005 .

[8]  M. Greer,et al.  Ammonium nitrate improves direct somatic embryogenesis and biolistic transformation of Triticum aestivum. , 2009, New biotechnology.

[9]  A. Fehér,et al.  The involvement of reactive oxygen species (ROS) in the cell cycle activation (G0-to-G1 transition) of plant cells , 2008, Plant signaling & behavior.

[10]  M. .. Alvarez,et al.  Epigenetic control of plant immunity. , 2010, Molecular plant pathology.

[11]  K. Toriyama,et al.  Transgenic plant production mediated by Agrobacterium in Indica rice , 1996, Plant Cell Reports.

[12]  H. Hirt,et al.  New insights into an old story: Agrobacterium‐induced tumour formation in plants by plant transformation , 2010, The EMBO journal.

[13]  V. Chalifa-Caspi,et al.  Plant response to stress meets dedifferentiation , 2011, Planta.

[14]  S. Krauss,et al.  Cellular responses to targeted genomic sequence modification using single-stranded oligonucleotides and zinc-finger nucleases. , 2009, DNA repair.

[15]  I. Vasil The story of transgenic cereals: The challenge, the debate, and the solution—A historical perspective , 2005, In Vitro Cellular & Developmental Biology - Plant.

[16]  A. Shrawat,et al.  Agrobacterium-mediated transformation of cereals: a promising approach crossing barriers. , 2006, Plant biotechnology journal.

[17]  F. Kempken,et al.  Genetic Modification of Plants , 2010 .

[18]  G. N. Amzallag Maturation of integrated functions during development. I. Modifications of the regulatory network during transition periods in Sorghum bicolor , 2001 .

[19]  J. Sainis,et al.  Histone octamer trans-transfer: a signature mechanism of ATP-dependent chromatin remodelling unravelled in wheat nuclear extract. , 2011, Annals of botany.

[20]  Agrobacterium-mediated transformation of indica rice cv. ADT 43 , 2012, Plant Cell, Tissue and Organ Culture (PCTOC).

[21]  A. Fehér,et al.  Linked activation of cell division and oxidative stress defense in alfalfa leaf protoplast-derived cells is dependent on exogenous auxin , 2007, Plant Growth Regulation.

[22]  P. Sharp,et al.  Oligonucleotide-directed gene repair in wheat using a transient plasmid gene repair assay system , 2006, Plant Cell Reports.

[23]  I. Potrykus,et al.  Genetically Engineered Fertile Indica-Rice Recovered from Protoplasts , 1990, Bio/Technology.

[24]  S. Kauffman,et al.  Critical Dynamics in Genetic Regulatory Networks: Examples from Four Kingdoms , 2008, PloS one.

[25]  C. Clément,et al.  Microspore embryogenesis in barley: anther pre-treatment stimulates plant defence gene expression , 2008, Planta.

[26]  A. Kohli,et al.  The Quest to Understand the Basis and Mechanisms that Control Expression of Introduced Transgenes in Crop Plants , 2006, Plant signaling & behavior.

[27]  M. Doutriaux,et al.  RAD51 loss of function abolishes gene targeting and de-represses illegitimate integration in the moss Physcomitrella patens. , 2010, DNA repair.

[28]  C. Foyer,et al.  Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. , 2009, Antioxidants & redox signaling.

[29]  H. Leung,et al.  A Germin-Like Protein Gene Family Functions as a Complex Quantitative Trait Locus Conferring Broad-Spectrum Disease Resistance in Rice1[W][OA] , 2008, Plant Physiology.

[30]  M. Caliskan Germin, an Oxalate Oxidase, Has a Function in Many Aspects of Plant Life , 2000 .

[31]  Z. Chen,et al.  Roles of dynamic and reversible histone acetylation in plant development and polyploidy. , 2007, Biochimica et biophysica acta.

[32]  E. Kmiec,et al.  Regulation of targeted gene repair by intrinsic cellular processes , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[33]  K. Ozawa Establishment of a high efficiency Agrobacterium-mediated transformation system of rice (Oryza sativa L.). , 2009, Plant science : an international journal of experimental plant biology.

[34]  P. Khurana,et al.  Effect of water stress and heavy metals on induction of somatic embryogenesis in wheat leaf base cultures. , 2005, Indian journal of experimental biology.

[35]  T. Mahmood,et al.  Germin and Germin-like Proteins: Evolution, Structure, and Function , 2008 .

[36]  B. Arnholdt‐Schmitt Stress-Induced Cell Reprogramming. A Role for Global Genome Regulation? , 2004, Plant Physiology.

[37]  T. Fujimura,et al.  Efficient gene introduction into rice by electroporation and analysis of transgenic plants: use of electroporation buffer lacking chloride ions , 1990, Theoretical and Applied Genetics.

[38]  P. Shewry,et al.  Silencing of γ-gliadins by RNA interference (RNAi) in bread wheat , 2008 .

[39]  Colin Norman,et al.  What Don't We Know? , 2005, Science.

[40]  Youzhi Ma,et al.  GM wheat development in China: current status and challenges to commercialization. , 2012, Journal of experimental botany.

[41]  G. Hensel,et al.  Genetic transformation technology in the Triticeae , 2009 .

[42]  Daniel J. Hoeppner,et al.  Global transcription in pluripotent embryonic stem cells. , 2008, Cell stem cell.

[43]  B. Lane Oxalate, germin, and the extracellular matrix of higher plants , 1994, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[44]  M. Kemal Germin , an Oxalate Oxidase , Has a Function in Many Aspects of Plant Life , 2000 .

[45]  H. de Jong,et al.  From nucleosome to chromosome: a dynamic organization of genetic information. , 2011, The Plant journal : for cell and molecular biology.

[46]  Kazuki Saito,et al.  Application of Gene Targeting to Designed Mutation Breeding of High-Tryptophan Rice1[W][OA] , 2011, Plant Physiology.

[47]  P. Schweizer,et al.  The Multigene Family Encoding Germin-Like Proteins of Barley. Regulation and Function in Basal Host Resistance1[W][OA] , 2006, Plant Physiology.

[48]  A. Cuming,et al.  Temporal and Spatial Determination of Germin Biosynthesis in Wheat Tissues , 2000 .

[49]  G. Grafi How cells dedifferentiate: a lesson from plants. , 2004, Developmental biology.

[50]  T. Nishio,et al.  Low glutelin content1: A Dominant Mutation That Suppresses the Glutelin Multigene Family via RNA Silencing in Rice Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011452. , 2003, The Plant Cell Online.

[51]  Dean P. Jones,et al.  Extracellular redox state: refining the definition of oxidative stress in aging. , 2006, Rejuvenation research.

[52]  M. Matzke,et al.  Planting the Seeds of a New Paradigm , 2004, PLoS biology.

[53]  P. Bozhkov,et al.  Developmental pathways of somatic embryogenesis , 2002, Plant Cell, Tissue and Organ Culture.

[54]  V. Citovsky,et al.  Epigenetic control of Agrobacterium T-DNA integration. , 2011, Biochimica et biophysica acta.

[55]  R. Hell,et al.  Glutathione homeostasis and redox-regulation by sulfhydryl groups , 2005, Photosynthesis Research.

[56]  B. Lane,et al.  Oxalate, Germins, and Higher‐Plant Pathogens , 2002, IUBMB life.

[57]  N. Eckardt Grass Genome Evolution , 2008, The Plant Cell Online.

[58]  R. Hromas,et al.  More forks on the road to replication stress recovery. , 2011, Journal of molecular cell biology.

[59]  Y. Guisez,et al.  Different stresses, similar morphogenic responses: integrating a plethora of pathways. , 2009, Plant, cell & environment.

[60]  Tiegang Lu,et al.  Large-scale production of enhancer trapping lines for rice functional genomics , 2004 .

[61]  N. L. Innes Global Status of Commercialized Biotech/GM Crops: 2005. ISAAA Briefs No. 34. By C. James. Ithaca, NY, USA: ISAAA (2005), pp. 46, US$50.00. ISBN 1-892456-38-9 , 2006, Experimental Agriculture.

[62]  Ranjit G Gurav,et al.  Role of RNA interference in plant improvement , 2011, Naturwissenschaften.

[63]  M. Warburton,et al.  Identification of highly transformable wheat genotypes for mass production of fertile transgenic plants. , 2002, Genome.

[64]  A. Fehér The initiation phase of somatic embryogenesis: what we know and what we don't , 2008 .

[65]  M. Tasaka,et al.  Intersections between immune responses and morphological regulation in plants. , 2010, Journal of experimental botany.

[66]  C. Stasolla,et al.  Glutathione modulation of in vitro development , 2005, In Vitro Cellular & Developmental Biology - Plant.

[67]  M. Morell,et al.  High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[68]  K. Ozawa A high-efficiency Agrobacterium-mediated transformation system of rice (Oryza sativa L.). , 2012, Methods in molecular biology.

[69]  Gretchen Vogel,et al.  How Does a Single Somatic Cell Become a Whole Plant? , 2005, Science.

[70]  S. Henikoff,et al.  Gene regulation: A chromatin thermostat , 2010, Nature.

[71]  J. Gago,et al.  1 Agrobacterium-Mediated Transformation of Wheat : General Overview and New Approaches to Model and Identify the Key Factors Involved , 2012 .

[72]  S. Iida,et al.  A large-scale Agrobacterium-mediated transformation procedure with a strong positive-negative selection for gene targeting in rice (Oryza sativa L.) , 2004, Plant Cell Reports.

[73]  T. Tzfira,et al.  Biological systems of the host cell involved in Agrobacterium infection , 2007, Cellular microbiology.

[74]  Dirk Inzé,et al.  The ins and outs of the plant cell cycle , 2007, Nature Reviews Molecular Cell Biology.

[75]  Steven Henikoff,et al.  Capturing the dynamic epigenome , 2010, Genome Biology.

[76]  S. Toki,et al.  Towards a Highly Efficient Gene Targeting System in Higher Plants , 2009 .

[77]  W. Harwood Advances and remaining challenges in the transformation of barley and wheat. , 2012, Journal of experimental botany.

[78]  J. Ray,et al.  Germin, a protein marker of early plant development, is an oxalate oxidase. , 1993, The Journal of biological chemistry.

[79]  A. Cuming,et al.  Spatial specificity of H2O2-generating oxalate oxidase gene expression during wheat embryo germination. , 1998, The Plant journal : for cell and molecular biology.

[80]  J. Sainis,et al.  60Co-γ radiation induces differential acetylation and phosphorylation of histones H3 and H4 in wheat. , 2011, Plant biology.

[81]  Matthew W Vaughn,et al.  Epigenomic Consequences of Immortalized Plant Cell Suspension Culture , 2008, PLoS biology.

[82]  B. Lane,et al.  Oxalate oxidases and differentiating surface structure in wheat: germins. , 2000, The Biochemical journal.

[83]  P. Schweizer,et al.  The germinlike protein GLP4 exhibits superoxide dismutase activity and is an important component of quantitative resistance in wheat and barley. , 2004, Molecular plant-microbe interactions : MPMI.

[84]  K. Osakabe,et al.  Regulatory Mechanisms of Homologous Recombination in Higher Plants , 2010 .

[85]  D. Schaefer Gene targeting in Physcomitrella patens. , 2001, Current opinion in plant biology.

[86]  G. Droc,et al.  High throughput T-DNA insertion mutagenesis in rice: a first step towards in silico reverse genetics. , 2004, The Plant journal : for cell and molecular biology.

[87]  J. Lehár,et al.  High-order combination effects and biological robustness , 2008, Molecular systems biology.

[88]  J. Greenberg,et al.  Programmed cell death: a way of life for plants. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[89]  C. Gutiérrez,et al.  Impact of nucleosome dynamics and histone modifications on cell proliferation during Arabidopsis development , 2010, Heredity.

[90]  N. Fedoroff The past, present and future of crop genetic modification. , 2010, New biotechnology.

[91]  N. Morozova,et al.  Two Phases of Chromatin Decondensation during Dedifferentiation of Plant Cells , 2001, The Journal of Biological Chemistry.

[92]  H. Blau,et al.  Nuclear reprogramming to a pluripotent state by three approaches , 2010, Nature.

[93]  Gang Wu,et al.  Insights into molecular mechanisms of mutual effect between plants and the environment. A review , 2007, Agronomy for Sustainable Development.

[94]  B. Zhivotovsky,et al.  Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. , 2000, Journal of cell science.

[95]  S. Costa,et al.  'Open minded' cells: how cells can change fate. , 2007, Trends in cell biology.

[96]  Michael Freeling,et al.  Grains of knowledge: genomics of model cereals. , 2005, Genome research.

[97]  A. Cuming,et al.  Formation of wheat (Triticum aestivum L.) embryogenic callus involves peroxide-generating germin-like oxalate oxidase , 2004, Planta.

[98]  I. Vasil A history of plant biotechnology: from the Cell Theory of Schleiden and Schwann to biotech crops , 2008, Plant Cell Reports.

[99]  E. Rebar,et al.  Genome editing with engineered zinc finger nucleases , 2010, Nature Reviews Genetics.

[100]  Ming-Bo Wang,et al.  Gene silencing as an adaptive defence against viruses , 2001, Nature.

[101]  P. Hilson Cloned sequence repertoires for small- and large-scale biology. , 2006, Trends in plant science.

[102]  C. Stasolla Glutathione redox regulation of in vitro embryogenesis. , 2010, Plant physiology and biochemistry : PPB.

[103]  P. Lazzeri,et al.  Transgenic wheat, barley and oats: production and characterization. , 2009, Methods in molecular biology.

[104]  D. Nigam,et al.  Differential transcriptional expression following thidiazuron-induced callus differentiation developmental shifts in rice. , 2010, Plant biology.

[105]  S. Filichkin,et al.  Divide and conquer: development and cell cycle genes in plant transformation. , 2006, Trends in biotechnology.

[106]  M. Matzke,et al.  Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates , 2000, Plant Molecular Biology.

[107]  V. Knauf,et al.  TILLING moves beyond functional genomics into crop improvement , 2005, Transgenic Research.

[108]  B. Dumas,et al.  Specific and constitutive expression of oxalate oxidase during the ageing of leaf sheaths of ryegrass stubble , 2001 .

[109]  T. Komari,et al.  Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. , 1994, The Plant journal : for cell and molecular biology.

[110]  K. Shinozaki,et al.  A genome-wide gain-of-function analysis of rice genes using the FOX-hunting system , 2007, Plant Molecular Biology.

[111]  E. Le Deunff,et al.  Oxidative burst and expression of germin/oxo genes during wounding of ryegrass leaf blades: comparison with senescence of leaf sheaths. , 2004, The Plant journal : for cell and molecular biology.

[112]  R. Dixon,et al.  Beyond Structural Genomics for Plant Science , 2007 .

[113]  L. Simmons,et al.  Reactive oxygen species as universal constraints in life-history evolution , 2009, Proceedings of the Royal Society B: Biological Sciences.

[114]  M. Fromm,et al.  Herbicide Resistant Fertile Transgenic Wheat Plants Obtained by Microprojectile Bombardment of Regenerable Embryogenic Callus , 1992, Bio/Technology.

[115]  Dean P. Jones,et al.  Redox control systems in the nucleus: mechanisms and functions. , 2010, Antioxidants & redox signaling.

[116]  B. Price,et al.  Chromatin dynamics and the repair of DNA double strand breaks , 2011, Cell cycle.