Microparticle bombardment as a tool in plant science and agricultural biotechnology.

Microparticle bombardment technology has evolved as a method for delivering exogenous nucleic acids into plant cells and is a commonly employed technique in plant science. Desired genetic material is precipitated onto micron-sized metal particles and placed within one of a variety of devices designed to accelerate these "microcarriers" to velocities required to penetrate the plant cell wall. In this manner, transgenes can be delivered into the cell's genome or plastome. Since the late 1980s microparticle bombardment has become a powerful tool for the study of gene expression and production of stably transformed tissues and whole transgenic plants for experimental purposes and agricultural applications. This paper reviews development and application of the technology, including the protocols and mechanical systems employed as delivery systems, and the types of plant cells and culture systems employed to generate effective "targets" for receiving the incoming genetic material. Current understanding of how the exogenous DNA becomes integrated into the plant's native genetic background are assessed as are methods for improving the efficiency of this process. Pros and cons of particle bombardment technologies compared to alternative direct gene transfer methods and Agrobacterium based transformation systems are discussed.

[1]  M. Fromm,et al.  Factors Influencing Gene Delivery into Zea Mays Cells by High–Velocity Microprojectiles , 1988, Bio/Technology.

[2]  A. Cockburn,et al.  Silicon carbide fiber-mediated stable transformation of plant cells , 1992, Theoretical and Applied Genetics.

[3]  Superfluous Transgene Integration in Plants , 2001 .

[4]  H. Morikawa,et al.  Presence of an SAR-like sequence in junction regions between an introduced transgene and genomic DNA of cultured tobacco cells: its effect on transformation frequency. , 2001, The Plant journal : for cell and molecular biology.

[5]  H. Morikawa,et al.  Evidence That More than 90% of beta-Glucuronidase-Expressing Cells after Particle Bombardment Directly Receive the Foreign Gene in their Nucleus. , 1991, Plant physiology.

[6]  G. W. Snyder,et al.  Introduction of pathogen defense genes and a cytokinin biosynthesis gene into sugarbeet (Beta vulgaris L.) by Agrobacterium or particle bombardment , 1999, Plant Cell Reports.

[7]  R. Briddon,et al.  Infectivity of African cassava mosaic virus clones to cassava by biolistic inoculation , 1998, Archives of Virology.

[8]  G. Hahne,et al.  Early events in microprojectile bombardment: cell viability and particle location , 1994 .

[9]  J. Finer,et al.  Intron-mediated enhancement of gene expression in maize (Zea mays L.) and bluegrass (Poa pratensis L.) , 1996, Plant Cell Reports.

[10]  P. Christou.  Electric discharge particle acceleration (Accell®) technology for the creation of transgenic plants with altered characteristics , 1996 .

[11]  P. Barceló,et al.  Procedures allowing the transformation of a range of European elite wheat (Triticum aestivum L.) varieties via particle bombardment. , 2001, Journal of experimental botany.

[12]  Peter Meyer,et al.  Transcriptional transgene silencing and chromatin components , 2000, Plant Molecular Biology.

[13]  P. Christou,et al.  Multiple traits of agronomic importance in transgenic indica rice plants: analysis of transgene integration patterns, expression levels and stability , 2004, Molecular Breeding.

[14]  P. Lemaux,et al.  Transformation of Maize Cells and Regeneration of Fertile Transgenic Plants. , 1990, The Plant cell.

[15]  Shiping Zhang,et al.  Expression and inheritance of multiple transgenes in rice plants , 1998, Nature Biotechnology.

[16]  P. Maliga,et al.  Stable transformation of plastids in higher plants. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[17]  James M. Wilson,et al.  Fas ligand—a double-edged sword , 1998, Nature Biotechnology.

[18]  W. Mark Saltzman,et al.  Synthetic DNA delivery systems , 2000, Nature Biotechnology.

[19]  N. Yang,et al.  In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[20]  M. McMullen,et al.  Transformation of 12 different plasmids into soybean via particle bombardment , 1996, Plant Cell Reports.

[21]  J. Sanford.  The biolistic process , 1988 .

[22]  P. Maliga,et al.  Engineering the plastid genome of higher plants. , 2002, Current opinion in plant biology.

[23]  M. E. John,et al.  Transgenic cotton resistant to herbicide bialaphos , 1997, Transgenic Research.

[24]  V. Citovsky,et al.  The Agrobacterium DNA Transfer Complex , 1997 .

[25]  Varsha,et al.  Microprojectile mediated plant transformation: A bibliographic search , 1997, Euphytica.

[26]  M. Chilton,et al.  "Agrolistic" transformation of plant cells: integration of T-strands generated in planta. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[27]  P. Christou,et al.  An Efficient Rice Transformation System Utilizing Mature Seed-derived Explants and a Portable, Inexpensive Particle Bombardment Device , 1998, Transgenic Research.

[28]  Misa Takahashi,et al.  Structures of transgene loci in transgenic Arabidopsis plants obtained by particle bombardment: junction regions can bind to nuclear matrices. , 1998, Gene.

[29]  M. D. Beuckeleer,et al.  Transgenic maize plants by tissue electroporation. , 1992, The Plant cell.

[30]  M. Roy,et al.  Physical trauma and tungsten toxicity reduce the efficiency of biolistic transformation. , 1992, Plant physiology.

[31]  J. Petolino.  Direct DNA Delivery Into Intact Cells and Tissues , 2002 .

[32]  M. Bevan,et al.  GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. , 1987, The EMBO journal.

[33]  Li-li Chen,et al.  A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 , 1995, Science.

[34]  P. Jauhar,et al.  Chromosome-mediated and direct gene transfers in wheat , 1999 .

[35]  T. Komari,et al.  High efficiency transformation of maize (Zea mays L.) mediated by Agrobacterium tumefaciens , 1996, Nature Biotechnology.

[36]  M. Fromm,et al.  Inheritance and Expression of Chimeric Genes in the Progeny of Transgenic Maize Plants , 1990, Bio/Technology.

[37]  C. Fauquet,et al.  Transgenic Cassava for Food Security and Economic Development , 2002 .

[38]  R. Vierstra,et al.  Soluble, highly fluorescent variants of green fluorescent protein (GFP) for use in higher plants , 1998, Plant Molecular Biology.

[39]  C D Day,et al.  Transgene integration into the same chromosome location can produce alleles that express at a predictable level, or alleles that are differentially silenced. , 2000, Genes & development.

[40]  M. Fromm,et al.  Stably Transformed Callus Lines from Microprojectile Bombardment of Cell Suspension Cultures of Wheat , 1991, Bio/Technology.

[41]  T. Komari,et al.  Advances in cereal gene transfer. , 1998, Current opinion in plant biology.

[42]  John C. Sanford,et al.  Biolistic nuclear transformation of Saccharomyces cerevisiae and other fungi , 1990, Current Genetics.

[43]  D. J. Peterson,et al.  Structure and function of selectable and non-selectable transgenes in maize after introduction by particle bombardment , 1994, Plant Molecular Biology.

[44]  A. Kohli,et al.  Transgene organization in rice engineered through direct DNA transfer supports a two-phase integration mechanism mediated by the establishment of integration hot spots. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[45]  W. Broekaert,et al.  Different approaches for multi-transgene-stacking in plants , 2002 .

[46]  A. Gleave,et al.  Transformation of citrus embryogenic cells using particle bombardment and production of transgenic embryos , 1996 .

[47]  R. Newton,et al.  Transformation of Picea Species , 2000 .

[48]  P. Ozias‐Akins,et al.  Transgenic peanut plants containing a nucleocapsid protein gene of tomato spotted wilt virus show divergent levels of gene expression , 1998, Plant Cell Reports.

[49]  S. Mayfield,et al.  Stable nuclear transformation of Chlamydomonas reinhardtii by using a C. reinhardtii gene as the selectable marker. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Yves-Jacques Schneider,et al.  Compartmentalized coculture of porcine arterial endothelial and smooth muscle cells on a microporous membrane , 1997, In Vitro Cellular & Developmental Biology - Animal.

[51]  N. Yang,et al.  Gene gun and other non-viral approaches for cancer gene therapy , 1995, Nature Medicine.

[52]  A. Nuutila,et al.  Transgenic oat plants via visual selection of cells expressing green fluorescent protein , 2000, Plant Cell Reports.

[53]  R. Swennen,et al.  Genetic Transformation of Banana and Plantain (Musa spp.) via Particle Bombardment , 1995, Bio/Technology.

[54]  C. Fauquet,et al.  Regeneration of transgenic cassava plants (Manihot esculenta Crantz) through Agrobacterium-mediated transformation of embryogenic suspension cultures , 1998, Plant Cell Reports.

[55]  Bao-jian Li,et al.  Fertile transgenic Indica rice plants obtained by electroporation of the seed embryo cells , 2004, Plant Cell Reports.

[56]  S. Jain,et al.  Molecular Biology of Woody Plants , 2000, Forestry Sciences.

[57]  P. Beyer,et al.  Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. , 2000, Science.

[58]  G. Adam,et al.  Biolistic transfer of large DNA fragments to tobacco cells using YACs retrofitted for plant transformation , 1998, Molecular Breeding.

[59]  D. Somers,et al.  Genomic interspersions determine the size and complexity of transgene loci in transgenic plants produced by microprojectile bombardment. , 2001, Genome.

[60]  T. Minamikawa,et al.  Transformation and regeneration of French bean plants by the particle bombardment process , 1996 .

[61]  L. Iyer,et al.  Transgene silencing in monocots , 2000, Plant Molecular Biology.

[62]  T. Clemente,et al.  Regeneration of transgenic peanut plants from stably transformed embryogenic callus , 1993 .

[63]  N. Yang,et al.  In vivo promoter activity and transgene expression in mammalian somatic tissues evaluated by using particle bombardment. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[64]  P. Lemaux,et al.  High-frequency transformation of oat via microprojectile bombardment of seed-derived highly regenerative cultures , 1999 .

[65]  J. Sanford,et al.  Inheritance of foreign genes in transgenic bean (Phaseolus vulgaris L.) co-transformed via particle bombardment , 1996, Theoretical and Applied Genetics.

[66]  T. Clemente,et al.  Inheritance of Multiple Transgenes in Wheat , 2000 .

[67]  S. Ullrich,et al.  Stability of transgene expression, field performance and recombination breeding of transformed barley lines , 2001, Theoretical and Applied Genetics.

[68]  M. Chilton,et al.  Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis , 1977, Cell.

[69]  J. Dunwell,et al.  Production of Fertile Transgenic Maize Plants by Silicon Carbide Whisker-Mediated Transformation , 1994 .

[70]  T. Klein,et al.  Transformation of Microbes, Plants and Animals by Particle Bombardment , 1992, Bio/Technology.

[71]  W. F. Thompson,et al.  Use of matrix attachment regions (MARs) to minimize transgene silencing , 2000, Plant Molecular Biology.

[72]  H. Fukuoka,et al.  Direct gene delivery into isolated microspores of rapeseed (Brassica napus L.) and the production of fertile transgenic plants , 1998, Plant Cell Reports.

[73]  T. Klein,et al.  DELIVERY OF SUBSTANCES INTO CELLS AND TISSUES USING A PARTICLE BOMBARDMENT PROCESS , 1987 .

[74]  P. Waterhouse,et al.  Application of gene silencing in plants. , 2002, Current opinion in plant biology.

[75]  I. Potrykus,et al.  In situmonitoring of DNA: the plant nuclear envelope allows passage of short DNA fragments , 1998 .

[76]  P. Barceló,et al.  Analysis of particle bombardment parameters to optimise DNA delivery into wheat tissues , 1999, Plant Cell Reports.

[77]  V. Brukhin,et al.  Basta tolerance as a selectable and screening marker for transgenic plants of Norway spruce , 2000, Plant Cell Reports.

[78]  P. Hasegawa,et al.  Transgenic sorghum plants obtained after microprojectile bombardment of immature inflorescences , 1997, In Vitro Cellular & Developmental Biology - Plant.

[79]  P. Christou,et al.  Molecular Characteristics of Transgenic Wheat and the Effect on Transgene Expression , 1998, Transgenic Research.

[80]  K. Mysore,et al.  An Arabidopsis histone H2A mutant is deficient in Agrobacterium T-DNA integration. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[81]  Claude Fauquet,et al.  Regeneration of transgenic cassava plants (Manihot esculenta Crantz) from microbombarded embryogenic suspension cultures , 1996, Nature Biotechnology.

[82]  P. Christou,et al.  Molecular and genetic characterization of elite transgenic rice plants produced by electric-discharge particle acceleration , 2004, Theoretical and Applied Genetics.

[83]  P. Christou.  Chapter 27 Particle Bombardment , 1995 .

[84]  J. Brown,et al.  Biotic, molecular, and phylogenetic characterization of bean calico mosaic virus, a distinct begomovirus species with affiliation in the squash leaf curl virus cluster. , 1999, Phytopathology.

[85]  H. Daniell,et al.  Antibiotic-free chloroplast genetic engineering - an environmentally friendly approach. , 2001, Trends in plant science.

[86]  M. Smith,et al.  Genetic transformation of Cavendish banana (Musa spp. AAA group) cv 'Grand Nain' via microprojectile bombardment , 2000, Plant Cell Reports.

[87]  E. Earle,et al.  Stable transformation of tomato cell cultures after bombardment with plasmid and YAC DNA , 1995, Plant Cell Reports.

[88]  J. Sanford,et al.  Biolistic transformation of prokaryotes: factors that affect biolistic transformation of very small cells. , 1992, Journal of general microbiology.

[89]  P. Jauhar,et al.  Genetic enrichment of cereal crops via alien gene transfer: New challenges , 2001, Plant Cell, Tissue and Organ Culture.

[90]  H. Vaucheret,et al.  RNA Silencing in Plants--Defense and Counterdefense , 2001, Science.

[91]  P. Meyer,et al.  The transformation booster sequence from Petunia hybrida is a retrotransposon derivative that binds to the nuclear scaffold , 1995, Molecular and General Genetics MGG.

[92]  P. Christou,et al.  Molecular analysis of the genome of transgenic rice (Oryza sativa L.) plants produced via particle bombardment or intact cell electroporation , 1998, Molecular Breeding.

[93]  S. Riazuddin,et al.  Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests , 2004, Molecular Breeding.

[94]  E. Southgate,et al.  Factors affecting the genetic engineering of plants by microprojectile bombardment. , 1995, Biotechnology advances.

[95]  D. Songstad,et al.  Advances in alternative DNA delivery techniques , 2004, Plant Cell, Tissue and Organ Culture.

[96]  M. McMullen,et al.  Osmotic treatment enhances particle bombardment-mediated transient and stable transformation of maize , 2004, Plant Cell Reports.

[97]  Yasuyuki Yamada,et al.  Efficiency of particle-bombardment-mediated transformation is influenced by cell cycle stage in synchronized cultured cells of tobacco. , 1991, Plant physiology.

[98]  E. Meiri,et al.  Simple hand-held devices for the efficient infection of plants with viral-encoding constructs by particle bombardment. , 1997, Journal of virological methods.

[99]  Paul Christou,et al.  Matrix attachment regions increase transgene expression levels and stability in transgenic rice plants and their progeny , 1999 .

[100]  W. F. Thompson,et al.  A tobacco matrix attachment region reduces the loss of transgene expression in the progeny of transgenic tobacco plants , 1999 .

[101]  Strategies for variety-independent genetic transformation of important cereals, legumes and woody species utilizing particle bombardment , 1995 .

[102]  P. Vain,et al.  Foreign gene delivery into monocotyledonous species. , 1995, Biotechnology advances.

[103]  G. Brar,et al.  Recovery of transgenic peanut (Arachis hypogaea L.) plants from elite cultivars utilizing ACCELL® technology , 1994 .

[104]  Michael D. McMullen,et al.  Development of the particle inflow gun for DNA delivery to plant cells , 1992, Plant Cell Reports.

[105]  Henry Daniell,et al.  New tools for chloroplast genetic engineering , 1999, Nature Biotechnology.

[106]  P. Jauhar,et al.  An evaluation of target cells and tissues used in genetic transformation of cereals , 1997 .

[107]  J. Puonti-Kaerlas,et al.  PIG-mediated cassava transformation using positive and negative selection , 2000, Plant Cell Reports.

[108]  T. Thykjær,et al.  Gene targeting approaches using positive-negative selection and large flanking regions , 1997, Plant Molecular Biology.

[109]  J. Finer,et al.  Particle bombardment mediated transformation. , 1999, Current topics in microbiology and immunology.

[110]  P. Hasegawa,et al.  Transgenic sorghum plants via microprojectile bombardment. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[111]  L. Comai,et al.  Nuclear matrix attachment regions and plant gene expression , 1998 .

[112]  B. Gordon-Kamm,et al.  Germline Transformation of Maize Following Manipulation of Chimeric Shoot Meristems , 1995, Bio/Technology.

[113]  C. Fauquet,et al.  Production of embryogenic tissues and regeneration of transgenic plants in cassava (Manihot esculenta Crantz) , 2001, Euphytica.

[114]  W F Thompson,et al.  High-level transgene expression in plant cells: effects of a strong scaffold attachment region from tobacco. , 1996, The Plant cell.

[115]  P. Beyer,et al.  Transgenic rice (Oryza sativa) endosperm expressing daffodil (Narcissus pseudonarcissus) phytoene synthase accumulates phytoene, a key intermediate of provitamin A biosynthesis. , 1997, The Plant journal : for cell and molecular biology.

[116]  P. Christou,et al.  Parameters Influencing Stable Transformation of Rice Immature Embryos and Recovery of Transgenic Plants using Electric Discharge Particle Acceleration , 1995 .

[117]  P. Lemaux,et al.  Generation of Large Numbers of Independently Transformed Fertile Barley Plants , 1994, Plant physiology.

[118]  Clive James,et al.  Global review of commercialized transgenic crops , 2003 .

[119]  P. Christou,et al.  Stable Transformation of Soybean (Glycine Max) by Particle Acceleration , 1988, Bio/Technology.

[120]  D. Ow,et al.  Biolistic mediated site-specific integration in rice , 2002, Molecular Breeding.

[121]  R. Fabbro,et al.  X‐ray sources for microlithography created by laser radiation at λ=0.26 μm , 1987 .

[122]  S. Dalton,et al.  Transgenic plants of Lolium multiflorum, Lolium perenne, Festuca arundinacea and Agrostis stolonifera by silicon carbide fibre-mediated transformation of cell suspension cultures , 1998 .