The full text of this article hosted at iucr.org is unavailable due to technical difficulties.

Open Access

Gene stacking in transgenic plants – the challenge for 21st century plant biotechnology

Claire Halpin

Corresponding Author

Plant Research Unit, School of Life Sciences, University of Dundee at SCRI, Invergowrie, Dundee DD2 5DA, UK

Correspondence (fax 44 (0)1382 568505; e‐mail

c.halpin@dundee.ac.uk

)
Search for more papers by this author
First published: 03 February 2005
Cited by: 194

Summary

One of the major technical hurdles impeding the advance of plant genetic engineering and biotechnology is the fact that the expression or manipulation of multiple genes in plants is still difficult to achieve. Although a small proportion of commercial genetically modified (GM) crops present ‘stacked’ or ‘pyramided’ traits, only a handful of products have been developed by introducing three or more novel genes. On the research front, a variety of conventional and more novel methods have been employed to introduce multiple genes into plants, but all techniques suffer from certain drawbacks. In this review, the potential and problems of these various techniques and strategies are discussed, and the prospects for improving these technologies in the future are presented.

Number of times cited: 194

  • , An osmotin from the resurrection plant Tripogon loliiformis () confers tolerance to multiple abiotic stresses in transgenic rice, Physiologia Plantarum, 162, 1, (13-34), (2017).
  • , Development of a multiplex fluorescence quantitative PCR for detection of genetically modified organisms, Biologia, (2018).
  • , Transgenic Research in Tuber and Root Crops, Genetic Engineering of Horticultural Crops, 10.1016/B978-0-12-810439-2.00011-8, (225-248), (2018).
  • , A toolkit for Nannochloropsis oceanica CCMP1779 enables gene stacking and genetic engineering of the eicosapentaenoic acid pathway for enhanced long‐chain polyunsaturated fatty acid production, Plant Biotechnology Journal, 16, 1, (298-309), (2017).
  • , RNAi-Mediated Simultaneous Resistance Against Three RNA Viruses in Potato, Molecular Biotechnology, 59, 2-3, (73), (2017).
  • , Environmental impacts of genetically modified plants: A review, Environmental Research, 10.1016/j.envres.2017.03.011, 156, (818-833), (2017).
  • , Metabolic Engineering of Secondary Plant Metabolism, Plant Biotechnology: Principles and Applications, 10.1007/978-981-10-2961-5_6, (173-190), (2017).
  • , Metabolic engineering of micronutrients in crop plants, Annals of the New York Academy of Sciences, 1390, 1, (59-73), (2016).
  • , EliteTree™: an advanced biomass tree crop technology that features greater wood density and accelerated stem growth, Biofuels, Bioproducts and Biorefining, 11, 3, (521-533), (2017).
  • , Double overexpression of DREB and PIF transcription factors improves drought stress tolerance and cell elongation in transgenic plants, Plant Biotechnology Journal, 15, 4, (458-471), (2016).
  • , Molecular genetics to discover and improve nitrogen use efficiency in crop plants, Plant Macronutrient Use Efficiency, 10.1016/B978-0-12-811308-0.00006-5, (93-122), (2017).
  • , Host induced gene silencing, an emerging science to engineer crop resistance against harmful plant pathogens, Physiological and Molecular Plant Pathology, 10.1016/j.pmpp.2017.10.003, 100, (242-254), (2017).
  • , Conferring resistance to pre-harvest sprouting in durum wheat by a QTL identified in Triticum spelta, Euphytica, 213, 1, (2017).
  • , Current perspectives on genetically modified crops and detection methods, 3 Biotech, 10.1007/s13205-017-0809-3, 7, 3, (2017).
  • , Genome Editing of Plants, Critical Reviews in Plant Sciences, 10.1080/07352689.2017.1281663, 36, 1, (1-23), (2017).
  • , Genetic engineering approaches to enhance oil content in oilseed crops, Plant Growth Regulation, 83, 2, (207), (2017).
  • , MicroRNA dynamics in a wild and cultivated species of Convolvulaceae exposed to drought stress, Physiology and Molecular Biology of Plants, 23, 2, (291), (2017).
  • , Biotechnological Perspective of Reactive Oxygen Species (ROS)-Mediated Stress Tolerance in Plants, Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress, 10.1007/978-981-10-5254-5_3, (53-87), (2017).
  • , Simultaneous Expression of Abiotic Stress-Responsive Genes: An Approach to Improve Multiple Stress Tolerance in Crops, Plant Tolerance to Individual and Concurrent Stresses, 10.1007/978-81-322-3706-8_10, (151-163), (2017).
  • , Effective Screening of Transgenic Pigeonpea in Presence of Negative Selection Agents, Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, (2017).
  • , Development of an R4 dual-site (R4DS) gateway cloning system enabling the efficient simultaneous cloning of two desired sets of promoters and open reading frames in a binary vector for plant research, PLOS ONE, 12, 5, (e0177889), (2017).
  • , Metabolic engineering to simultaneously activate anthocyanin and proanthocyanidin biosynthetic pathways in Nicotiana spp., PLOS ONE, 12, 9, (e0184839), (2017).
  • , Development and Characterization of Transgenic Sugarcane with Insect Resistance and Herbicide Tolerance, Frontiers in Plant Science, 8, (2017).
  • , Novel technologies in doubled haploid line development, Plant Biotechnology Journal, 15, 11, (1361-1370), (2017).
  • , A simple, rapid and systematic method for the developed GM rice analysis, Plant Biotechnology Reports, 10, 1, (25), (2016).
  • , Stakeholder views on issues to consider when assessing the sustainability of genetically modified potato, International Journal of Agricultural Sustainability, 14, 3, (357), (2016).
  • , Construction and Quality Analysis of Transgenic Rehmannia glutinosa Containing TMV and CMV Coat Protein, Molecules, 21, 12, (1134), (2016).
  • , Isolation and Functional Validation of Salinity and Osmotic Stress Inducible Promoter from the Maize Type-II H+-Pyrophosphatase Gene by Deletion Analysis in Transgenic Tobacco Plants, PLOS ONE, 11, 4, (e0154041), (2016).
  • , Promoter isolation and characterization of GhAO-like1, a Gossypium hirsutum gene similar to multicopper oxidases that is highly expressed in reproductive organs, Genome, 59, 1, (23), (2016).
  • , PCR Methods for Detecting GM Crops and Food in Agriculture and the Food Chain: A Review, Functional Nucleic Acids Detection in Food Safety, 10.1007/978-981-10-1618-9_14, (323-342), (2016).
  • , Plant artificial chromosome technology and its potential application in genetic engineering, Plant Biotechnology Journal, 14, 5, (1175-1182), (2015).
  • , Transgenic trait deployment using designed nucleases, Plant Biotechnology Journal, 14, 2, (503-509), (2015).
  • , Comparative expression analysis of five caulimovirus promoters in citrus, Plant Cell, Tissue and Organ Culture (PCTOC), 126, 2, (229), (2016).
  • , Genetically modified (GM) crops: milestones and new advances in crop improvement, Theoretical and Applied Genetics, 129, 9, (1639), (2016).
  • , Metabolic Engineering of Chemical Defence Pathways in Plant Disease Control, Plant Pathogen Resistance Biotechnology, (71-89), (2016).
  • , Simultaneous knockdown of six non-family genes using a single synthetic RNAi fragment in Arabidopsis thaliana, Plant Methods, 12, 1, (2016).
  • , High Expression of Cry1Ac Protein in Cotton (Gossypium hirsutum) by Combining Independent Transgenic Events that Target the Protein to Cytoplasm and Plastids, PLOS ONE, 11, 7, (e0158603), (2016).
  • , Rpi-blb2 gene from Solanum bulbocastanum confers extreme resistance to late blight disease in potato, Plant Cell, Tissue and Organ Culture (PCTOC), 125, 2, (269), (2016).
  • , Combining Selective Pressures to Enhance the Durability of Disease Resistance Genes, Frontiers in Plant Science, 7, (2016).
  • , Fitness correlates of crop transgene flow into weedy populations: a case study of weedy rice in China and other examples, Evolutionary Applications, 9, 7, (857-870), (2016).
  • , Engineered Minichromosomes in Plants, , 10.1016/bs.ircmb.2015.05.002, (63-119), (2015).
  • , Improving Rice Ability to Degrade Different Polycyclic Aromatic Hydrocarbons Through Multigene Transformation of a Hybrid Dioxygenase System, Plant Molecular Biology Reporter, 33, 4, (1030), (2015).
  • , Characterization of a small constitutive promoter from Arabidopsis translationally controlled tumor protein (AtTCTP) gene for plant transformation, Plant Cell Reports, 34, 2, (265), (2015).
  • , Do Sesamia nonagrioides (Lepidoptera; Noctuidae) Gravid Females Discriminate Between Bt or Multivitamin Corn Varieties? Role of Olfactory and Visual Cues, Journal of Insect Science, 15, 1, (33), (2015).
  • , Pyramiding of AtEDT1/HDG11 and Cry2Aa2 into pepper (Capsicum annuum L.) enhances drought tolerance and insect resistance without yield decrease, Plant Cell, Tissue and Organ Culture (PCTOC), 120, 3, (919), (2015).
  • , Selectable Marker Gene Removal and Expression of Transgene by Inducible Promoter Containing FFDD Cis-Acting elements in Transgenic Plants, Iranian Journal of Biotechnology, 13, 3, (1), (2015).
  • , A combinatorial bidirectional and bicistronic approach for coordinated multi-gene expression in corn, Plant Molecular Biology, 87, 4-5, (341), (2015).
  • , Generation of insect-resistant and glyphosate-tolerant rice by introduction of a T-DNA containing two Bt insecticidal genes and an EPSPS gene, Journal of Zhejiang University-SCIENCE B, 16, 10, (824), (2015).
  • , Characterization of the acetohydroxyacid synthase multigene family in the tetraploide plant Chenopodium quinoa, Electronic Journal of Biotechnology, 10.1016/j.ejbt.2015.07.003, 18, 6, (393-398), (2015).
  • , Developing transgenic maize (Zea mays L.) with insect resistance and glyphosate tolerance by fusion gene transformation, Journal of Integrative Agriculture, 14, 2, (305), (2015).
  • , Enhanced Genetic Tools for Engineering Multigene Traits into Green Algae, New Biotechnologies for Increased Energy Security, 10.1201/b18537-14, (187-205), (2015).
  • , Minichromosomes: Vectors for Crop Improvement, Agronomy, 5, 4, (309), (2015).
  • , Safety Evaluation of Stacked Genetically Modified Corn Event (MON89034 × MON88017) Using Zebrafish as an Animal Model, Food and Nutrition Sciences, 06, 14, (1285), (2015).
  • , A Dual-Intein Autoprocessing Domain that Directs Synchronized Protein Co-Expression in Both Prokaryotes and Eukaryotes, Scientific Reports, 5, 1, (2015).
  • , Transformation of rice with large maize genomic DNA fragments containing high content repetitive sequences, Plant Cell Reports, 34, 6, (1049), (2015).
  • , Cry1Ac insecticidal protein levels in genetically modified Coffea canephora Pierre coffee plants were negatively correlated with the growth speed in a field experiment, Euphytica, 202, 3, (373), (2015).
  • , Development of marker-free transformants by site-specific recombinases, Cytology and Genetics, 49, 6, (397), (2015).
  • , Compositional analysis of genetically modified corn events (NK603, MON88017×MON810 and MON89034×MON88017) compared to conventional corn, Food Chemistry, 176, (99), (2015).
  • , Plant synthetic biology: a new platform for industrial biotechnology, Journal of Experimental Botany, 65, 8, (1927), (2014).
  • , Exploring Plant-Microorganism Relationships for Natural Solutions to Sustainable Agriculture and Food Production, Industrial Biotechnology, 10, 5, (336), (2014).
  • , Elimination of the nptII marker gene in transgenic apple and pear with a chemically inducible R/Rs recombinase, Plant Cell, Tissue and Organ Culture (PCTOC), 117, 3, (335), (2014).
  • , Isolation and Characterization of the Diatom Phaeodactylum Δ5-Elongase Gene for Transgenic LC-PUFA Production in Pichia pastoris, Marine Drugs, 12, 12, (1317), (2014).
  • , Highly interactive nature of flower‐specific enhancers and promoters, and its potential impact on tissue‐specific expression and engineering of multiple genes or agronomic traits, Plant Biotechnology Journal, 12, 7, (951-962), (2014).
  • , A simple and reliable multi-gene transformation method for switchgrass, Plant Cell Reports, 33, 7, (1161), (2014).
  • , Pyramiding Bt genes for increasing resistance of cotton to two major lepidopteran pests: Spodoptera litura and Heliothis armigera, Acta Physiologiae Plantarum, 10.1007/s11738-014-1642-5, 36, 10, (2717-2727), (2014).
  • , Yeast cell surface display for lipase whole cell catalyst and its applications, Journal of Molecular Catalysis B: Enzymatic, 106, (17), (2014).
  • , Regulation of Transgene Expression and Containment in Forest Trees, Tree Biotechnology, 10.1201/b16714-16, (2014).
  • , Increased expression of native cytosolic Cu/Zn superoxide dismutase and ascorbate peroxidase improves tolerance to oxidative and chilling stresses in cassava (Manihot esculenta Crantz), BMC Plant Biology, 14, 1, (2014).
  • , Increased Drought Tolerance through the Suppression of ESKMO1 Gene and Overexpression of CBF-Related Genes in Arabidopsis, PLoS ONE, 9, 9, (e106509), (2014).
  • , Wood Formation in Trees, Tree Biotechnology, 10.1201/b16714-5, (2014).
  • , The Ph-3 gene from Solanum pimpinellifolium encodes CC-NBS-LRR protein conferring resistance to Phytophthora infestans, Theoretical and Applied Genetics, 127, 6, (1353), (2014).
  • , Engineering Complex Metabolic Pathways in Plants, Annual Review of Plant Biology, 65, 1, (187), (2014).
  • , Guiding deployment of resistance in cereals using evolutionary principles, Evolutionary Applications, 7, 6, (609-624), (2014).
  • , Enhanced Genetic Tools for Engineering Multigene Traits into Green Algae, PLoS ONE, 9, 4, (e94028), (2014).
  • , Establishment of a quadruplex real-time PCR for screening of genetically modified tomatoes, European Food Research and Technology, 238, 4, (683), (2014).
  • , Transgene Pyramiding of theHVA1andmtlDin T3 Maize (Zea maysL.) Plants Confers Drought and Salt Tolerance, along with an Increase in Crop Biomass, International Journal of Agronomy, 2013, (1), (2013).
  • , Plant Adaptation to Abiotic and Genotoxic Stress: Relevance to Climate Change and Evolution, Climate Change and Plant Abiotic Stress Tolerance, (251-294), (2013).
  • , Pyramiding of Bt cry1Ia8 and cry1Ba3 genes into cabbage (Brassica oleracea L. var. capitata) confers effective control against diamondback moth, Plant Cell, Tissue and Organ Culture (PCTOC), 10.1007/s11240-013-0373-4, 115, 3, (419-428), (2013).
  • , Defensin (TvD1) from Tephrosia villosa exhibited strong anti-insect and anti-fungal activities in transgenic tobacco plants, Journal of Pest Science, 86, 2, (337), (2013).
  • , Vector integration in triple R gene transformants and the clustered inheritance of resistance against potato late blight, Transgenic Research, 22, 2, (315), (2013).
  • , Trait stacking via targeted genome editing, Plant Biotechnology Journal, 11, 9, (1126-1134), (2013).
  • , Selection of Nontarget Testing Organisms for ERA of GM Potato with Increased Resistance to Late Blight, Potato Research, 56, 4, (293), (2013).
  • , Development of an efficient bi-directional promoter with tripartite enhancer employing three viral promoters, Journal of Biotechnology, 163, 3, (311), (2013).
  • , Enhanced Expression Levels of Cellulase Enzymes Using Multiple Transcription Units, BioEnergy Research, 6, 2, (699), (2013).
  • , The rice OsLTP6 gene promoter directs anther-specific expression by a combination of positive and negative regulatory elements, Planta, 238, 5, (845), (2013).
  • , Characterization and regulation of Bacillus thuringiensis Cry toxin binding aminopeptidases N (APNs) from non-gut visceral tissues, Malpighian tubule and salivary gland: Comparison with midgut-specific APN in the moth Achaea janata, Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 166, 3-4, (194), (2013).
  • , Using biolistics and hybridization to combine multiple glycosidase inhibitor transgenes in wheat, Euphytica, 10.1007/s10681-013-0972-5, 194, 3, (443-457), (2013).
  • , Targeted molecular trait stacking in cotton through targeted double-strand break induction, Plant Biotechnology Journal, 11, 8, (933), (2013).
  • , Turning over a new leaf in plant genomics, Genome Biology, 14, 6, (2013).
  • , A Modified MultiSite Gateway Cloning Strategy for Consolidation of Genes in Plants, Molecular Biotechnology, 53, 2, (129), (2013).
  • , Applications of biotechnology and genomics in potato improvement, Plant Biotechnology Journal, 11, 8, (907), (2013).
  • , Functional stacking of three resistance genes against Phytophthora infestans in potato, Transgenic Research, 21, 1, (89), (2012).
  • , Engineering Mammalian Mucin-typeO-Glycosylation in Plants, Journal of Biological Chemistry, 287, 15, (11911), (2012).
  • , Genomics and Breeding in Food Crops, OMICs Technologies, 10.1201/b11534-8, (141-162), (2012).
  • , Acquiring transgenic tobacco plants with insect resistance and glyphosate tolerance by fusion gene transformation, Plant Cell Reports, 31, 10, (1877), (2012).
  • , Progress in Cre/lox site-specific recombination system in higher eukaryotes, Hereditas (Beijing), 10.3724/SP.J.1005.2012.00177, 34, 2, (177-189), (2012).
  • , Cis-acting motifs in artificially synthesized expression cassette leads to enhanced transgene expression in tomato (Solanum lycopersicum L.), Plant Physiology and Biochemistry, 61, (131), (2012).
  • , The interaction of plant biotic and abiotic stresses: from genes to the field, Journal of Experimental Botany, 10.1093/jxb/ers100, 63, 10, (3523-3543), (2012).
  • , Recent advances in development of marker-free transgenic plants: Regulation and biosafety concern, Journal of Biosciences, 37, 1, (167), (2012).
  • , Stable integration of an engineered megabase repeat array into the maize genome, The Plant Journal, 70, 2, (357-365), (2012).
  • , Ecological risk assessments for transgenic crops with combined insect-resistance traits: the example of Bt11 × MIR604 maize, Journal of Applied Entomology, 136, 1-2, (27), (2012).
  • , Expression of complete metabolic pathways in transgenic plants, Biotechnology and Genetic Engineering Reviews, 28, 1, (1), (2012).
  • , Petunia Floral Defensins with Unique Prodomains as Novel Candidates for Development of Fusarium Wilt Resistance in Transgenic Banana Plants, PLoS ONE, 7, 6, (e39557), (2012).
  • , Microbes in Agriculture, Microbes, (481-566), (2012).
  • , Impact of gene stacking on gene flow: the case of maize, Transgenic Research, 21, 2, (243), (2012).
  • , Transgenic banana plants expressing small interfering RNAs targeted against viral replication initiation gene display high-level resistance to banana bunchy top virus infection, Journal of General Virology, 93, Pt_8, (1804), (2012).
  • , Genetic Modification of the Soybean to Enhance the β-Carotene Content through Seed-Specific Expression, PLoS ONE, 7, 10, (e48287), (2012).
  • , Stacking of antimicrobial genes in potato transgenic plants confers increased resistance to bacterial and fungal pathogens, Journal of Biotechnology, 157, 2, (334), (2012).
  • , Overproduction of recombinant proteins in plants, Plant Science, 184, (83), (2012).
  • , Synthetic Chromosome Platforms in Plants, Annual Review of Plant Biology, 63, 1, (307), (2012).
  • , Potential Environmental Impacts of Transgene Flow in Rice with a Particular View on Herbicide Resistance, Plant Gene Containment, (1-25), (2012).
  • , Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana, Proceedings of the National Academy of Sciences, 10.1073/pnas.1203145109, 109, 14, (5370-5375), (2012).
  • , Transgene regulation in plants by alternative splicing of a suicide exon, Nucleic Acids Research, 40, 10, (4701), (2012).
  • , Stacking small segments of the 1D chromosome of bread wheat containing major gluten quality genes into durum wheat: transfer strategy and breeding prospects, Molecular Breeding, 30, 1, (149), (2012).
  • , Expression of wheat Na+/H+ antiporter TNHXS1 and H+- pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance, Plant Molecular Biology, 79, 1-2, (137), (2012).
  • , Double Candida antarctica lipase B co-display on Pichia pastoris cell surface based on a self-processing foot-and-mouth disease virus 2A peptide, Applied Microbiology and Biotechnology, 96, 6, (1539), (2012).
  • , Strategies for Controlling Plant Diseases and Mycotoxin Contamination Using Antimicrobial Synthetic Peptides, Small Wonders: Peptides for Disease Control, 10.1021/bk-2012-1095.ch014, (295-315), (2012).
  • , A novel light-dependent selection marker system in plants, Plant Biotechnology Journal, 9, 3, (348), (2011).
  • , Fate of transgenes in the forest tree genome, Tree Genetics & Genomes, 7, 2, (221), (2011).
  • , Transformation of Cabbage (Brassica oleracea L. var. capitata) with Bt cry1Ba3 Gene for Control of Diamondback Moth, Agricultural Sciences in China, 10, 11, (1693), (2011).
  • , Bidirectionalization of a methyl jasmonate-inducible plant promoter, Biotechnology Letters, 33, 2, (387), (2011).
  • , Transgenic alfalfa plants co-expressing glutathione S-transferase (GST) and human CYP2E1 show enhanced resistance to mixed contaminates of heavy metals and organic pollutants, Journal of Hazardous Materials, 10.1016/j.jhazmat.2011.02.042, 189, 1-2, (357-362), (2011).
  • , Plants with genetically modified events combined by conventional breeding: An assessment of the need for additional regulatory data, Food and Chemical Toxicology, 49, 1, (1), (2011).
  • , Pyramided rice lines harbouring Allium sativum (asal) and Galanthus nivalis (gna) lectin genes impart enhanced resistance against major sap-sucking pests, Journal of Biotechnology, 152, 3, (63), (2011).
  • , Transgenic Plants for Phytoremediation, International Journal of Phytoremediation, 10.1080/15226514.2011.568549, 13, sup1, (264-279), (2011).
  • , Transgene stacking and marker elimination in transgenic rice by sequential Agrobacterium-mediated co-transformation with the same selectable marker gene, Plant Cell Reports, 30, 7, (1241), (2011).
  • , Recombinase technology: applications and possibilities, Plant Cell Reports, 30, 3, (267), (2011).
  • , Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress, Journal of Experimental Botany, 62, 8, (2599), (2011).
  • , Comparison of DNA Walking Methods for Isolation of Transgene-Flanking Regions in GM Potato, Molecular Biotechnology, 49, 1, (19), (2011).
  • , Changes in fitness-associated traits due to the stacking of transgenic glyphosate resistance and insect resistance in Brassica napus L., Heredity, 107, 4, (328), (2011).
  • , Combinatorial biosynthesis in plants: A (p)review on its potential and future exploitation, Natural Product Reports, 28, 12, (1897), (2011).
  • , Increased growth in sunflower correlates with reduced defences and altered gene expression in response to biotic and abiotic stress, Molecular Ecology, 20, 22, (4683-4694), (2011).
  • , Combined expression of the Arabidopsis metallothionein MT2b and the heavy metal transporting ATPase HMA4 enhances cadmium tolerance and the root to shoot translocation of cadmium and zinc in tobacco, Environmental and Experimental Botany, 72, 1, (71), (2011).
  • , Expression of Multiple Resistance Genes Enhances Tolerance to Environmental Stressors in Transgenic Poplar (Populus × euramericana ‘Guariento’), PLoS ONE, 6, 9, (e24614), (2011).
  • , Towards the development of better crops by genetic transformation using engineered plant chromosomes, Plant Cell Reports, 30, 5, (799), (2011).
  • , Development and characterisation of transgenic rice expressing two Bacillus thuringiensis genes, Pest Management Science, 67, 4, (414-422), (2011).
  • , Development of a qualitative, multiplex real-time PCR kit for screening of genetically modified organisms (GMOs), Analytical and Bioanalytical Chemistry, 396, 6, (2043), (2010).
  • , Folates and Folic Acid: From Fundamental Research Toward Sustainable Health, Critical Reviews in Plant Sciences, 10.1080/07352680903436283, 29, 1, (14-35), (2010).
  • , Mathematical modeling of monolignol biosynthesis in Populus xylem, Mathematical Biosciences, 228, 1, (78), (2010).
  • , Application of two bicistronic systems involving 2A and IRES sequences to the biosynthesis of carotenoids in rice endosperm, Plant Biotechnology Journal, 8, 8, (928-938), (2010).
  • , Engineering the K+ uptake regulatory pathway by MultiRound Gateway, Journal of Plant Physiology, 167, 16, (1412), (2010).
  • , Stability of transgene expression as a challenge for genetic engineering, Plant Science, 179, 3, (164), (2010).
  • , Selectable marker-free transgenic orange plants recovered under non-selective conditions and through PCR analysis of all regenerants, Plant Cell, Tissue and Organ Culture (PCTOC), 102, 3, (329), (2010).
  • , Engineered Minichromosomes in Plants, Critical Reviews in Plant Sciences, 29, 3, (135), (2010).
  • , Genetically modified plants for non-food or non-feed purposes: Straightforward screening for their appearance in food and feed, Food and Chemical Toxicology, 48, 2, (453), (2010).
  • , Metabolic engineering of ketocarotenoid biosynthesis in higher plants, Archives of Biochemistry and Biophysics, 483, 2, (182), (2009).
  • , Plants: Genetic Transformation, Encyclopedia of Industrial Biotechnology, (1-11), (2009).
  • , Wheat Breeding: Procedures and Strategies, Wheat Science and Trade, (273-308), (2009).
  • , Poplars, Compendium of Transgenic Crop Plants, (1-34), (2009).
  • , Why farming with high tech methods should integrate elements of organic agriculture, New Biotechnology, 25, 6, (378), (2009).
  • , A leaf‐based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways, Plant Biotechnology Journal, 7, 9, (914-924), (2009).
  • , Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways, Proceedings of the National Academy of Sciences, 106, 19, (7762), (2009).
  • , Genome-wide comparative analysis of putative bidirectional promoters from rice, Arabidopsis and Populus, Gene, 429, 1-2, (65), (2009).
  • , Key Issues and Open Questions in GMO Controls, Global Issues in Food Science and Technology, 10.1016/B978-0-12-374124-0.00020-X, (353-365), (2009).
  • , Phytoremediation of small organic contaminants using transgenic plants, Current Opinion in Biotechnology, 20, 2, (237), (2009).
  • , Tomato, Compendium of Transgenic Crop Plants, (1-46), (2009).
  • , Sweet Potato, Compendium of Transgenic Crop Plants, (157-176), (2009).
  • , Analysis and stability of the Respiratory Syncytial Virus antigen in a T3 generation of transgenic tomato plants, Plant Cell, Tissue and Organ Culture (PCTOC), 96, 3, (335), (2009).
  • , 2A to the Fore – Research, Technology and Applications, Biotechnology and Genetic Engineering Reviews, 26, 1, (223), (2009).
  • , Modification of isoflavones in soybean seeds via expression of multiple phenolic biosynthetic genes, Plant Physiology and Biochemistry, 47, 9, (769), (2009).
  • , Inducible gene expression systems and plant biotechnology, Biotechnology Advances, 10.1016/j.biotechadv.2009.05.006, 27, 6, (733-743), (2009).
  • , Evaluation of Viability, Shedding Pattern, and Longevity of Pollen from Genetically Modified (GM) Herbicide-tolerant and Wild-type Zoysiagrass (Zoysia japonica Steud.), Journal of Plant Biology, 10.1007/s12374-009-9074-2, 52, 6, (630-634), (2009).
  • , Gene stacking in transgenic plants: towards compliance between definitions, terminology, and detection within the EU regulatory framework, Environmental Biosafety Research, 7, 4, (197), (2008).
  • , Comparative safety assessment of plant-derived foods, Regulatory Toxicology and Pharmacology, 10.1016/j.yrtph.2007.09.007, 50, 1, (98-113), (2008).
  • , Genetic Engineering for Forage Quality in Alfalfa, Handbook of New Technologies for Genetic Improvement of Legumes, 10.1201/9781439801352.ch1, (1-18), (2010).
  • , Engineering with Precision: Tools for the New Generation of Transgenic Crops, BioScience, 10.1641/B580506, 58, 5, (391-401), (2008).
  • , Transgenic tobacco plants expressing synthetic Cry1Ac and Cry1Ie genes are more toxic to cotton bollworm than those containing one gene, Science Bulletin, 53, 9, (1381), (2008).
  • , Hybrid protease inhibitors for pest and pathogen control – a functional cost for the fusion partners?, Plant Physiology and Biochemistry, 46, 7, (701), (2008).
  • , The Chitinase A from the baculovirus AcMNPV enhances resistance to both fungi and herbivorous pests in tobacco, Transgenic Research, 17, 4, (557), (2008).
  • , Crop Breeding Methodologies: Classic and Modern, Breeding Major Food Staples, (38-40), (2008).
  • , Application prospect of new site-specific recombination systems in gene transformation and gene stacking, Hereditas (Beijing), 30, 2, (149), (2008).
  • , Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize, Proceedings of the National Academy of Sciences, 10.1073/pnas.0809737105, 105, 47, (18232-18237), (2008).
  • , Sequential transformation to pyramid two Bt genes in vegetable Indian mustard (Brassica juncea L.) and its potential for control of diamondback moth larvae, Plant Cell Reports, 27, 3, (479), (2008).
  • , A comparison of strategies for transformation with multiple genes via microprojectile-mediated bombardment, In Vitro Cellular & Developmental Biology - Plant, 10.1007/s11627-007-9099-5, 44, 3, (162-168), (2008).
  • , Molecular mechanisms of insect adaptation to plant defense: Lessons learned from a Bruchid beetle, Insect Science, 15, 6, (477), (2008).
  • , Multiple transgenes Populus xeuramericana ‘Guariento’ plants obtained by biolistic bombardment, Chinese Science Bulletin, 52, 2, (224), (2007).
  • , Genetic engineering approaches to improve bioethanol production from maize, Current Opinion in Biotechnology, 18, 3, (193), (2007).
  • , Synthetic promoters: genetic control through cis engineering, Trends in Plant Science, 12, 3, (118), (2007).
  • , Trends in analytical methodology in food safety and quality: monitoring microorganisms and genetically modified organisms, Trends in Food Science & Technology, 18, 6, (306), (2007).
  • , Functional analysis of cauliflower mosaic virus 35S promoter: re‐evaluation of the role of subdomains B5, B4 and B2 in promoter activity, Plant Biotechnology Journal, 5, 6, (696-708), (2007).
  • , A passage through in vitro culture leads to efficient production of marker-free transgenic plants in Brassica juncea using the Cre–loxP system, Transgenic Research, 16, 6, (703), (2007).
  • , Engineered minichromosomes in plants, Current Opinion in Biotechnology, 18, 5, (425), (2007).
  • , Developments in Transgenic Biology and the Genetic Engineering of Useful Traits, Potato Biology and Biotechnology, 10.1016/B978-044451018-1/50072-5, (669-686), (2007).
  • , Risk assessment of GM stacked events obtained from crosses between GM events, Trends in Food Science & Technology, 18, 2, (101), (2007).
  • , A Gateway-based platform for multigene plant transformation, Plant Molecular Biology, 62, 6, (927), (2006).
  • , Transgenic peas (Pisum sativum) expressing polygalacturonase inhibiting protein from raspberry (Rubus idaeus) and stilbene synthase from grape (Vitis vinifera), Plant Cell Reports, 25, 11, (1166), (2006).
  • , E unum pluribus: multiple proteins from a self-processing polyprotein, Trends in Biotechnology, 24, 2, (68), (2006).
  • , Biotechnology in Agriculture, Annual Review of Environment and Resources, 10.1146/annurev.energy.31.031405.091314, 31, 1, (265-295), (2006).
  • , Genetically modified crops: success, safety assessment, and public concern, Applied Microbiology and Biotechnology, 71, 5, (598), (2006).
  • , Environmental impact of genetically modified cotton in South Africa, Agriculture, Ecosystems & Environment, 117, 4, (277), (2006).
  • , Ratiometric Fluorescence-Imaging Assays of Plant Membrane Traffic Using Polyproteins, Traffic, 7, 12, (1701), (2006).
  • , Nature of stress and transgene locus influences transgene expression stability in barley, Plant Molecular Biology, 62, 1-2, (15), (2006).
  • , Multimodal Protein Constructs for Herbivore Insect Control, Toxins, 10.3390/toxins4060455, 4, 12, (455-475), (2012).
  • , Expression of Cry1Ab and Cry2Ab by a Polycistronic Transgene with a Self-Cleavage Peptide in Rice, PLoS ONE, 10.1371/journal.pone.0110006, 9, 10, (e110006), (2014).