Abstract
Main conclusion
While transgenic technology has heralded a new era in crop improvement, several concerns have precluded their widespread acceptance. Alternative technologies, such as cisgenesis and genome-editing may address many of such issues and facilitate the development of genetically engineered crop varieties with multiple favourable traits.
Abstract
Genetic engineering and plant transformation have played a pivotal role in crop improvement via introducing beneficial foreign gene(s) or silencing the expression of endogenous gene(s) in crop plants. Genetically modified crops possess one or more useful traits, such as, herbicide tolerance, insect resistance, abiotic stress tolerance, disease resistance, and nutritional improvement. To date, nearly 525 different transgenic events in 32 crops have been approved for cultivation in different parts of the world. The adoption of transgenic technology has been shown to increase crop yields, reduce pesticide and insecticide use, reduce CO2 emissions, and decrease the cost of crop production. However, widespread adoption of transgenic crops carrying foreign genes faces roadblocks due to concerns of potential toxicity and allergenicity to human beings, potential environmental risks, such as chances of gene flow, adverse effects on non-target organisms, evolution of resistance in weeds and insects etc. These concerns have prompted the adoption of alternative technologies like cisgenesis, intragenesis, and most recently, genome editing. Some of these alternative technologies can be utilized to develop crop plants that are free from any foreign gene hence, it is expected that such crops might achieve higher consumer acceptance as compared to the transgenic crops and would get faster regulatory approvals. In this review, we present a comprehensive update on the current status of the genetically modified (GM) crops under cultivation. We also discuss the issues affecting widespread adoption of transgenic GM crops and comment upon the recent tools and techniques developed to address some of these concerns.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acharjee S, Sarmah BK, Kumar PA, Olsen K, Mahon R, Moar WJ, Moore A, Higgins TJV (2010) Transgenic chickpeas (Cicer arietinum L.) expressing a sequence-modified cry2Aa gene. Plant Sci 178:333–339. https://doi.org/10.1016/j.plantsci.2010.02.001
Adang MJ, Brody MS, Cardineau G, Eagan N, Roush RT, Shewmaker CK, Jones A, Oakes JE, McBride KE (1993) The reconstruction and expression of a Bacillus thuringiensis cryIIIA gene in protoplasts and potato plants. Plant Mol Biol 21:1131–1145. https://doi.org/10.1007/bf00023609
Agarwal A, Yadava P, Kumar K, Singh I, Kaul T, Pattanayak A, Agrawal PA (2018) Insights into maize genome editing via CRISPR/Cas9. Physiol Mol Biol Plants 24:175–183. https://doi.org/10.1007/s12298-017-0502-3
Al-Babili S, Beyer P (2005) Golden Rice—Five years on the road—five years to go? Trends Plant Sci 10:565–573. https://doi.org/10.1016/j.tplants.2005.10.006
Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, Chen PJ, Wilson C, Newby GA, Raguram A, Liu DR (2019) Search and replace genome editing without double strand breaks or donor DNA. Nature 576:149–157. https://doi.org/10.1038/s41586-019-1711-4
Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426. https://doi.org/10.1016/j.tplants.2007.08.003
Azevedo RA, Lea PJ (2001) Lysine metabolism in higher plants. Amino Acids 20:261–279. https://doi.org/10.1007/s007260170043
Bagla P (2010) Hardy cotton-munching pests are latest blow to GM crops. Sci 327:1439. https://doi.org/10.1126/science.327.5972.1439
Barry GF, Kishore GM, Padgette SR, Stallings WC (1997) Glyphosate-tolerant 5-enolpyruvylshikimate-3-phosphate synthases. US Patent 5633435. https://patents.google.com/patent/US5633435A/en
Bawa AS, Anilakumar KR (2013) Genetically modified foods: safety, risks and public concerns—a review. J Food Sci Technol 50:1035–1046. https://doi.org/10.1007/s13197-012-0899-1
Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V (2013) Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9:39. https://doi.org/10.1186/1746-4811-9-39
Bevan MW, Flavell RB, Chilton MD (1983) A chimaeric antibiotic resistance gene as a selectable marker for plant cell transformation. Nature 304:184–187. https://doi.org/10.1038/304184a0
Bicar EH, Woodman CW, Sangtong V, Peterson JM, Yang SS, Lee M, Scott MP (2008) Transgenic maize endosperm containing a milk protein has improved amino acid balance. Transgenic Res 17:59–71. https://doi.org/10.1007/s11248-007-9081-3
Broadway RM, Duffey SS (1986) Plant proteinase inhibitors: Mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exiqua. J Insect Physiol 32:827–833. https://doi.org/10.1016/0022-1910(86)90097-1
Brookes G, Barfoot P (2017) Environmental impacts of genetically modified (GM) crop use 1996–2015: Impacts on pesticide use and carbon emissions. GM Crops Food 8:117–147. https://doi.org/10.1080/21645698.2017.1309490
Brookes G, Barfoot P (2018) Farm income and production impacts of using GM crop technology 1996–2016. GM Crops Food 9:59–89. https://doi.org/10.1080/21645698.2018.1464866
Brower LP, Taylor OR, Williams EH, Slayback DA, Zubieta RR, Ramirez MI (2012) Decline of monarch butterflies overwintering in Mexico: is the migratory phenomenon at risk? Insect Conserv Diver 5:95–100. https://doi.org/10.1111/j.1752-4598.2011.00142.x
Bucchini L, Goldman L (2002) Starlink Corn: A Risk analysis. Environ Health Perspect 110:5–13. https://doi.org/10.1289/ehp.021105
Business Wire (2016) Global Genetically Modified Seeds Market to Witness Growth Through 2020 Due to Rise in Adoption of Bio-fuels: Reports Technavio. https://www.businesswire.com/news/home/20160830005089/en/Global-Genetically-Modified-Seeds-Market-Witness-Growth
Cai Y, Chen L, Liu X, Guo C, Sun S, Wu C, Jiang B, Han T, Hou W (2017) CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnol J 16:176–185. https://doi.org/10.1111/pbi.12758
Callaway E (2018) CRISPR plants now subject to tough GM laws in European Union. Nature 560:16. https://doi.org/10.1038/d41586-018-05814-6
Carrière Y, Crowder DW, Tabashnik BE (2010) Evolutionary ecology of insect adaptation to Bt crops. Evol Appl 3:561–573. https://doi.org/10.1111/j.1752-4571.2010.00129.x
Castiglioni P, Warner D, Bensen RJ, Anstrom DC, Harrison J et al (2008) Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in Maize under water-limited conditions. Plant Physiol 147:446–455. https://doi.org/10.1104/pp.108.118828
Chaikam V (2012) In vivo maternal haploid induction in maize. In: B.M. Prasanna, V Chaikam, and G Mahuku, editors, Doubled haploid technology in maize breeding: Theory and practice. CIMMYT, D F, Mexico pp 9–13. https://hdl.handle.net/10883/1351
Chan RL, Cabello JV, Giacomelli JI (2013) HaHB11 provides improved plant yield and tolerance to abiotic stress. WO2013116750A1. https://patents.google.com/patent/WO2013116750A1
Chawla R, Shakya R, Rommens CM (2012) Tuber-specific silencing of asparagine synthetase-1 reduces the acrylamide-forming potential of potatoes grown in the field without affecting tuber shape and yield. Plant Biotechnol J 10:913–924. https://doi.org/10.1111/j.1467-7652.2012.00720.x
Chen JS, Dagdas YS, Kleinstiver BP, Welch MM, Sousa AA, Harrington LB, Sternberg SH, Joung JK, Yildiz A, Doudna JA (2017) Enhanced proofreading governs CRISPR–Cas9 targeting accuracy. Nature 550:407–410. https://doi.org/10.1038/nature24268
Chen LJ, Lee DS, Song ZP, Suh HS, Lu B (2004) Gene flow from cultivated rice (Oryza sativa) to its weedy and wild relatives. Ann Bot 93:67–73. https://doi.org/10.1093/aob/mch006
Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257. https://doi.org/10.1016/s1369-5266(02)00255-8
Chilton MD, Drummond MH, Merlo DJ, Sciaky D, Montoya AL, Gordon MP et al (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11:263–271. https://doi.org/10.1016/0092-8674(77)90043-5
Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761. https://doi.org/10.1534/genetics.110.120717
Christian M, Qi Y, Zhang Y, Voytas DF (2013) Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3 3:1697–1705. https://doi.org/10.1534/g3.113.007104
Chan RL, Cabello JV, Giacomelli JI (2013) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5(3):250–257. https://doi.org/10.1016/S1369-5266(02)00255-8
Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R, Davison S, Ray EE, Daulhac A, Coffman A, Yabandith A, Retterath A, Haun W, Baltes NJ, Mathis L, Voytas DF, Zhang F (2016) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14:169–176. https://doi.org/10.1111/pbi.12370
Cremer J, Treptow C, Eggeling L, Sahm H (1988) Regulation of enzymes of lysine biosynthesis in Corynebacterium glutamicum. Appl Environ Microbiol 134:3221–3229. https://doi.org/10.1099/00221287-134-12-3221
Curtin SJ, Xiong Y, Michno JM et al (2018) CRISPR/Cas9 and TALENs generate heritable mutations for genes involved in small RNA processing of Glycine max and Medicago truncatula. Plant Biotechnol J 16:1125–1137. https://doi.org/10.1111/pbi.12857
Dang W, Wei ZM (2007) An optimized Agrobacterium-mediated transformation for soybean for expression of binary insect resistance genes. Plant Sci 173:381–389. https://doi.org/10.1016/j.plantsci.2007.06.010
Davison J (2010) GM plants: Science, politics and EC regulations. Plant Sci 178:94–98. https://doi.org/10.1016/j.plantsci.2009.12.005
De Vos CJ, Swanenburg M (2018) Health effects of feeding genetically modified (GM) crops to livestock animals: A review. Food Chem Toxicol 117:3–12. https://doi.org/10.1016/j.fct.2017.08.031
Dezar CA, Gago GM, González DH, Chan RL (2005) Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res 14:429–440. https://doi.org/10.1007/s11248-005-5076-0
Dill GM, CaJacob CA, Padgette SR (2008) Glyphosate-resistant crops: adoption, use and future considerations. Pest Manag Sci 64:326–331. https://doi.org/10.1002/ps.1501
Dively GP, Rose R, Sears MK, Hellmich RL, Stanley-Horn DE, Calvin DD, Russo JM, Anderson PL (2004) Effects on monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expression corn during anthesis. Envn Entomol 33:1116–1125. https://doi.org/10.1603/0046-225x-33.4.1116
Domingo JL (2016) Safety assessment of GM plants: an updated review of the scientific literature. Food Chem Toxicol 95:12–18. https://doi.org/10.1016/j.fct.2016.06.013
Dong L, Li L, Liu C, Liu C, Geng S, Li X, Huang C, Mao L, Chen S, Xie C (2018) Genome editing and double-fluorescence proteins enable robust maternal haploid induction and identification in maize. Mol Plant 11:1214–1217. https://doi.org/10.1016/j.molp.2018.06.011
Doudna JA, Charpentier E (2014) The new frontier of genome engineering with CRISPR–Cas9. Science 346:1258096. https://doi.org/10.1126/science.1258096
Du H, Zeng X, Zhao M, Cui X, Wang Q, Yang H, Cheng H, Yu D (2016) Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotechnol 217:90–97. https://doi.org/10.1016/j.jbiotec.2015.11.005
Duan X, Li X, Xue Q, Abo-El-Saad M, Xu D, Wu R (1996) Transgenic rice plants harboring an introduced potato Proteinase inhibitor II gene are insect resistant. Nat Biotechnol 14:494–498. https://doi.org/10.1038/nbt0496-494
Dufourmantel N, Tissot G, Goutorbe F, Garcon F, Jansens S, Pelissier B, Peltier G, Dubald M (2005) Generation and analysis of soybean plastid transformants expressing Bacillus thuringiensis Cry1Ab protoxin. Plant Mol Biol 58:659–668. https://doi.org/10.1007/s11103-005-7405-3
EFSA Panel on Genetically Modified Organisms (GMO) (2012) Scientific opinion addressing the safety assessment of plants developed through cisgenesis and intragenesis. EFSA J 10(2561):33. https://doi.org/10.2903/j.efsa.2012.2561
FAO (2010) Fats and fatty acids in human nutrition. Report of an expert consultation. Rome: Food and Agricultural Organisation of the United Nations. 10–14 November 2008, Geneva. FAO Food and Nutrition Paper 91. https://agris.fao.org/agris-search/search.do?recordID=XF2016049106
Fang J, Xu X, Wang P, Zhao JZ, Shelton AM, Cheng J, Shen Z (2007) Characterization of chimeric Bacillus thuringiensis Vip3 toxins. Appl Environ Microbiol 73:956–961. https://doi.org/10.1128/aem.02079-06
Faria JC, Albino MMC, Dias BBA, Cancado LJ, Cunha NB, Silva LM, Vianna GR, Aragão FJL (2006) Partial resistance to Bean golden mosaic virus in a transgenic common bean (Phaseolus vulgaris L.) line expressing a mutated rep gene. Plant Sci 171:565–571. https://doi.org/10.1016/j.plantsci.2006.06.010
Ferreira SA, Pitz KY, Manshardt R, Zee F, Fitch M, Gonsalves D (2002) Virus coat protein transgenic papaya provides practical control of papaya ringspot virus in hawaii. Plant Dis 86:101–105. https://doi.org/10.1094/pdis.2002.86.2.101
Ford CS, Allainguillaume J, Grilli-Chantler P, Cuccato J, Allender CJ, Wilkinson MJ (2006) Spontaneous gene flow from rapeseed (Brassica napus) to wild Brassica oleracea. Proc Biol Sci 273:3111–3115. https://doi.org/10.1098/rspb.2006.3686
Foster SJ, Park TH, Pel M, Brigneti G, Sliwka J, Jagger L, Vossen EVD, Jones JD (2009) Rpi-vnt1.1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight. Mol Plant Microbe Interact 22:589–600. https://doi.org/10.1094/MPMI-22-5-0589
Fraley RT, Rogers SG, Horsch RB, Sanders PR, Flick JS et al (1983) Expression of bacterial genes in plant cells. Proc Natl Acad Sci USA 80:4803–4807. https://doi.org/10.1073/pnas.80.15.4803
Fujimoto H, Itoh K, Yamamoto M, Kyozuka J, Shimamoto K (1993) Insect resistant rice generated by introduction of a modifed δ-endotoxin gene of Bacillus thuringiensis. Nat Biotechnol 11:1151–1155. https://doi.org/10.1038/nbt1093-1151
Gago GM, Almoguera C, Jordano J, Gonzalez DH, Chan RL (2002) Hahb-4, a homeobox leucine zipper gene potentially involved in abscisic acid-dependent responses to water stress in sunflower. Plant Cell Environ 25:633–640. https://doi.org/10.1046/j.1365-3040.2002.00853.x
Galili G (1995) Regulation of lysine and threonine synthesis. Plant Cell 7:899–906. https://doi.org/10.1105/tpc.7.7.899
Gao JP, Chao DY, Lin HX (2007) Understanding abiotic stress tolerance mechanisms: recent studies on stress response in rice. J Integr Plant Biol 49:742–750. https://doi.org/10.1111/j.1744-7909.2007.00495.x
Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS ONE 6:e22629. https://doi.org/10.1371/journal.pone.0022629
Geiger HH (2009) Doubled haploids. In: Bennetzen JL, Hake S (eds) Maize handbook-volume II: genetics and genomics. Springer Verlag, Heidelberg, pp 641–657
Geliebter A, Torbay N, Bracco EF, Hashim SA, Van Itallie TB (1983) Overfeeding with medium-chain triglyceride diet results in diminished deposition of fat. Am J Clin Nutr 37:1–4. https://doi.org/10.1093/ajcn/37.1.1
Gilbert N (2013) A hard look at GM crops. Nature 497:24–26. https://doi.org/10.1038/497024a
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Gocal G (2015a) Non-transgenic trait development in crop plants using oligo-directed mutagenesis: Cibus’ Rapid Trait Development System. In: NABC Report 26. New DNA-Editing Approaches: Methods, Applications and Policy for Agriculture. pp 97–105. North American Agricultural Biotechnology Council, Ithaca, NY. https://ecommons.cornell.edu/bitstream/handle/1813/51428/nabc26_10_Gocal.pdf?sequence=1&isAllowed=y.
Gocal GFW, Schopke C, Beetham PR (2015) Oligomediated targeting gene editing. In: Puchta H, Thompson JG (eds) Advances in New Technology for Targeted Modification of Plant Genomes (Zhang F, Puchta H and Thompson JG Eds). Springer, New York, pp 73–89
Green JM (2012) The benefits of herbicide-resistant crops. Pest Manag Sci 68:1323–1331. https://doi.org/10.1002/ps.3374
Griffiths AJF, Wessler SR, Lewontin RC, Gelbart WM, Suzuki DT, Miller JH (2005) Introduction to genetic analysis. 8th (ed.) FreemanWH, New York. https://www.bio.bg.ac.rs/materijali_predmeta/med-eng-griffiths-an-introduction-to-genetic-analysis.pdf
Guilinger JP, Pattanayak V, Reyon D, Tsai SQ, Sander JD, Joung JK, Liu DR (2014) Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificity. Nat Methods 11:429–435. https://doi.org/10.1038/nmeth.2845
Guilinger JP, Thompson DB, Liu DR (2014) Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 32:577–582. https://doi.org/10.1038/nbt.2909
Guo J, Litao Y, Xin L, Xiaoyan G, Lingxi J, Dabing Z (2009) Characterization of the exogenous insert and development of event-specific PCR detection methods for genetically modified Huanong No. 1 Papaya. J Agric Food Chem 57:7205–7212. https://doi.org/10.1021/jf901198x
Guo Y, Xu Q, Canzio D, Shou J, Li J, Gorkin DU, Jung I et al (2015) CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162:900–910. https://doi.org/10.1016/j.cell.2015.07.038
Gupta B, Tripathi AK, Joshi R, Pareek A, Singla-Pareek SL (2015) Designing climate smart future crops employing signal transduction components. In: Pandey GK (ed) Elucidation of abiotic stress signaling in plants: functional genomics perspectives. Springer, New York, pp 393–414
Halfill MD, Richards HA, Mabon SA, Stewart CN (2001) Expression of GFP and Bt transgenes in Brassica napus and hybridization with Brassica rapa. Theor Appl Genet 103:659–667. https://doi.org/10.1007/s001220100613
Han SM, Lee B, Won OJ, Hwang KS, Suh SJ, Kim C, Park KW (2015) Gene flow from herbicide resistant genetically modified rice to conventional rice (Oryza sativa L.) cultivars. J Ecol Environ 38:397–403. https://doi.org/10.5141/ecoenv.2015.042
Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, Mathis L, Voytas DF, Zhang F (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J 12:934–940. https://doi.org/10.1111/pbi.12201
Haverkort J, Struik PC, Visser RGF, Jacobsen E (2009) Applied Biotechnology to Combat Late Blight in Potato Caused by Phytophthora Infestans. Potato Res 52:249–264. https://doi.org/10.1007/s11540-009-9136-3
Heap I (2014) Global perspective of herbicide-resistant weeds. Pest Manag Sci 70:1306–1315. https://doi.org/10.1002/ps.3696
Heap I, Duke SO (2018) Overview of glyphosate-resistant weeds worldwide. Pest Manag Sci 74:1040–1049. https://doi.org/10.1002/ps.4760
Heritage J (2004) The fate of transgenes in the human gut. Nat Biotechnol 22:170–172. https://doi.org/10.1038/nbt0204-170
Herrera-Estrella L, Block MD, Messens E, Hernalsteens JP, Montagu MV, Schell J (1983) Chimeric genes as dominant selectable markers in plant cells. EMBO J 2:987–995. https://doi.org/10.1002/j.1460-2075.1983.tb01532.x
Herrera-Estrella L, Depicker A, Montagu MV, Schell J (1983) Expression of chimaeric genes transfered into plant cells using a Ti-plasmid-derived vector. Nature 303:209–213. https://doi.org/10.1038/303209a0
Hilder VA, Gatehouse AMR, Sheerman SE, Barker RF, Boulter D (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330:160–163. https://doi.org/10.1038/330160a0
Hilton IB, D’Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA (2015) Epigenome editing by a CRISPR–Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol 33:510–517. https://doi.org/10.1038/nbt.3199
Holme IB, Dionisio G, Brinch-Pedersen H, Wendt T, Madsen CK, Vincze E, Holm PB (2012) Cisgenic barley with improved phytase activity. Plant Biotechnol J 10:237–247. https://doi.org/10.1111/j.1467-7652.2011.00660.x
Indurker S, Misra HS, Eapen S (2007) Genetic transformation of chickpea (Cicer arietinum L.) with insecticidal crystal protein gene using particle gun bombardment. Plant Cell Rep 26:755–763. https://doi.org/10.1007/s00299-006-0283-6
ISAAA (2017) Global Status of Commercialized Biotech/GM Crops in 2017: Biotech Crop Adoption Surges as Economic Benefits Accumulate in 22 Years. ISAAA Brief No. 53. ISAAA: Ithaca, NY. https://www.isaaa.org/resources/publications/briefs/53/
ISAAA (2018) Global Status of Commercialized Biotech/GM Crops in 2018: Biotech Crops Continue to Help Meet the Challenges of Increased Population and Climate Change. ISAAA Brief No. 54. ISAAA: Ithaca, NY. https://www.isaaa.org/resources/publications/briefs/54/executivesummary/pdf/B54-ExecSum-English.pdf
ISAAA database (2019) GM Approval Database retrieved on 17 Nov 2019. https://www.isaaa.org/gmapprovaldatabase/default.asp
James C (1997) Global Status of Transgenic Crops in 1997. ISAAA Brief No. 5. ISAAA: Ithaca, NY. pp 31. https://www.isaaa.org/purchasepublications/itemdescription.asp?ItemType=BRIEFS&Control=IB005-1997
James C (2013) Global Status of Commercialized Biotech/GM Crops: 2013. ISAAA Brief No.46. ISAAA: Ithaca, NY. https://www.isaaa.org/resources/publications/briefs/46/
James C (2015) 20th Anniversary (1996 to 2015) of the Global Commercialization of Biotech Crops and Biotech Crop Highlights in 2015. ISAAA Brief No. 51. ISAAA: Ithaca, NY. https://isaaa.org/resources/publications/briefs/51/default.asp
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821. https://doi.org/10.1126/science.1225829
Jones HD (2015) Regulatory uncertainty over genome editing. Nature Plants 1:14011. https://doi.org/10.1038/nplants.2014.11
Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55. https://doi.org/10.1038/nrm3486
Kalla R, Shimamoto K, Potter R, Nielsen PS, Linnestad C, Olsen OA (1994) The promoter of the barley aleurone-specific gene encoding a putative 7 kDa lipid transfer protein confers aleurone cell specific expression in transgenic rice. Plant J 6:849–860. https://doi.org/10.1046/j.1365-313X.1994.6060849.x
Kaniewski W, Lawson C, Sammons B, Haley L, Hart J, Delannay X, Tumer NE (1990) Field resistance of transgenic russet burbank potato to effects of infection by potato virus X and potato virus Y. Nat Biotechnol 8:750–754. https://doi.org/10.1038/nbt0890-750
Karlson D, Nakaminami K, Toyomasu T, Imai R (2002) A cold-regulated nucleic acid-binding protein of winter wheat shares a domain with bacterial cold shock proteins. J Biol Chem 277:35248–35256. https://doi.org/10.1074/jbc.m205774200
Keese P (2008) Risks from GMOs due to horizontal gene transfer. Environ Biosaf Res 7:123–149. https://doi.org/10.1051/ebr:2008014
Kelliher T, Starr D, Richbourg L, Chintamanani S, Delzer B, Nuccio ML, Green J, Chen Z, McCuiston J, Wang W, Liebler T, Bullock P, Martin B (2017) MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction. Nature 542:105–109. https://doi.org/10.1038/nature20827
Kereša S, Grdiša M, Barić M, Barčić J, Marchetti S (2008) Transgenic plants expressing insect resistance genes. Sjemenarstvo 25:139–153. https://hrcak.srce.hr/file/43734
Khan MS, Yu X, Kikuchi A, Asahina M, Watanabe KN (2009) Genetic engineering of glycinebetaine biosynthesis to enhance abiotic stress tolerance in plants. Plant Biotechnol 26:125–134. https://doi.org/10.5511/plantbiotechnology.26.125
Kim JS, Park SJ, Kwak KJ, Kim YO, Song J, Jang B, Jung CH, Kang H (2007) Cold shock domain proteins and glycine-rich RNA-binding proteins from Arabidopsis thaliana can promote cold adaptation process in Escherichia Coli. Nucleic Acids Res 35:506–516. https://doi.org/10.1093/nar/gkl1076
Kim MH, Sato S, Sasaki K, Saburi W, Matsui H, Imai R (2013) Cold shock domain protein 3 is involved in salt and drought stress tolerance in Arabidopsis. FEBS Open Biol 3:438–442. https://doi.org/10.1016/j.fob.2013.10.003
Kim H, Kim JS (2014) A guide to genome engineering with programmable nucleases. Nat Rev Genet 15:321–334. https://doi.org/10.1038/nrg3686
Kim Y, Kweon J, Kim JS (2013) TALENs and ZFNs are associated with different mutation signatures. Nat Methods 10:185. https://doi.org/10.1038/nmeth.2364
Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to FokI cleavage domain. Proc Natl Acad Sci USA 93:1156–1160. https://doi.org/10.1073/pnas.93.3.1156
Klümper W, Qaim M (2014) A Meta-Analysis of the Impacts of Genetically Modified Crops. PLoS ONE 9:e111629. https://doi.org/10.1371/journal.pone.0111629
Koul B, Srivastava S, Sanya I, Tripathi B, Sharma V, Amla DV (2014) Transgenic tomato line expressing modified Bacillus thuringiensis cry1Ab gene showing complete resistance to two lepidopteran pests. Springer Plus 3:84. https://doi.org/10.1186/2193-1801-3-84
Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203. https://doi.org/10.1074/jbc.M806337200
Koziel MG, Beland GL, Bowman C, Carozzi NB, Crenshaw C, Crossland L, Dawson J, Desai N, Hill M, Kadwell S et al (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Nat Biotechnol 11:194–200. https://doi.org/10.1038/nbt0293-194
Kumar H, Kumar V (2004) Tomato expressing Cry1A(b) insecticidal protein from Bacillus thuringiensis protected against tomato fruit borer, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) damage in the laboratory, greenhouse and field. Crop Prot 23:135–139. https://doi.org/10.1016/j.cropro.2003.08.006
Kumar K, Aggarwal C, Sapna B, Singh I, Yadava P (2018) Microbial genes in crop improvement. Crop improvement through microbial biotechnology. Elsevier, Amsterdam, Netherlands, pp 39–56
Lawrenson T, Shorinola O, Stacey N, Li C, Østergaard L, Patron N, Uauy C, Harwood W (2015) Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol 16:258. https://doi.org/10.1186/s13059-015-0826-7
Lea PJ, Joy KW, Ramos JL, Guerrero MG (1984) The action of 2-amino-4-(methylphosphinyl)-butanoic acid (phosphinothricin) and its 2-oxo-derivative on the metabolism of cyanobacteria and higher plants. Phytochemistry 23:1–6. https://doi.org/10.1016/0031-9422(84)83066-6
Li C, Zong Y, Wang Y, Jin S, Zhang D, Song Q, Zhang R, Gao C (2018) Expanded base editing in rice and wheat using a Cas9–adenosine deaminase fusion. Genome Biol 19:59. https://doi.org/10.1186/s13059-018-1443-z
Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistance rice. Nat Biotechnol 30:390–392. https://doi.org/10.1038/nbt.2199
Li Z, Zhang D, Xiong X, Yan B, Xie W, Sheen J, Li JF (2017) A potent Cas9-derived gene activator for plant and mammalian cells. Nat Plants 3:930–936. https://doi.org/10.1038/s41477-017-0046-0
Liang Z, Chen K, Li T, Zhang Y, Wang Y, Zhao Q, Liu J et al (2017) ARTICLE Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun 8:1–5. https://doi.org/10.1038/ncomms14261
Liu C, Li X, Meng D, Zhong Y, Chen C, Dong X, Xu X, Chen B, Li W, Li L et al (2017) A 4-bp insertion at ZmPLA1 encoding a putative phospholipase A generates haploid induction in maize. Mol Plant 10:520–522. https://doi.org/10.1016/j.molp.2017.01.011
Losey JE, Rayor LS, Carter ME (1999) Transgenic pollen harms monarch larvae. Nature 399:214. https://doi.org/10.1038/20338
Lowder LG, Paul JW, Qi Y (2017) Multiplexed transcriptional activation or repression in plants using CRISPR–dCas9-based Systems. In: Mueller-Roeber B, Kaufmann K (eds) Plant gene regulatory networks. Methods in molecular biology. Humana Press, New York, pp 167–184
Lu Y, Wu K, Jiang Y, Xia B, Li P, Feng H, Wyckhuys KAG, Guo Y (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328:1151–1154. https://doi.org/10.1126/science.1187881
Luttrell RG, Ali I, Allen KC, Young III SY, Szalanski A, Williams K, Lorenz G, Parker Jr CD, Blanco C, (2004) Resistance to Bt in Arkansas populations of cotton bollworm, pp. 1373–1383. In Richter DA [ed.], Proceedings, 2004 Beltwide Cotton Conferences, 5–9 January 2004, San Antonio, TX, National Cotton Council of America, Memphis, TN. https://naldc.nal.usda.gov/download/12012/PDF
Lovei GL, Bøhn T, Hilbeck A (2010) Biodiversity, Ecosystem Services and Genetically Modified Organisms Third World Network, 131 Macalister Road 10400 Penang, Malaysia. ISBN: 978-967-5412-13-4. https://www.twn.my/title2/biosafety/pdf/bio10.pdf
Ma L, Zhu F, Li Z, Zhang J, Li X, Dong J, Wang T (2015) TALEN-Based mutagenesis of lipoxygenase LOX3 enhances the storage tolerance of rice (Oryza sativa) seeds. PLoS ONE 10:e0143877. https://doi.org/10.1371/journal.pone.0143877
Ma L, Zhang D, Miao Q, Yang J, Xuan Y, Hu Y (2017) Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiol 58:863–873. https://doi.org/10.1093/pcp/pcx040
Mahfouz MM, Li L, Piatek M et al (2012) Targeted transcriptional repression using a chimeric TALE-SRDX repressor protein. Plant Molecular Biol 78:311–321. https://doi.org/10.1007/s11103-011-9866-x
Majeed A, Makhdoom R, Husnain T, Riazuddin S (2011) Assessment of potato proteinase inhibitor-II gene as an antifungal and insecticidal agent. Acta Agric Scand Sect 61:92–96. https://doi.org/10.1080/09064710903433777
Malinovski T, Cambra M, Capote N, Zawadska B, Gorris T, Scorza R, Ravelonandro M (2006) Field trials of plum clones transformed with Plum pox virus coat protein (PPV CP) gene. Plant Dis 90:1012–1018. https://doi.org/10.1094/pd-90-1012
Mandaokar AD, Goyal RK, Shukla A, Bisaria S, Bhalla R, Reddy VS, Chaurasia A, Sharma RP, Altosaar I, Ananda Kumar P (2000) Transgenic tomato plants resistant to fruit borer (Helicoverpa armigera Hübner). Crop Prot 19:307–312. https://doi.org/10.1016/j.cropro.2012.01.010
Marc F, Dennis G (1995) Resistance of transgenic hybrid squash zw-20 expressing the coat protein genes of zucchini yellow mosaic virus and watermelon mosaic virus 2 to mixed infections by both potyviruses. Nat Biotechnol 13:1466–1473. https://doi.org/10.1038/nbt1295-1466
McDougall P (2011) The Cost and Time Involved in the Discovery, Development and Authorisation of a New Plant Biotechnology Derived Trait. In: A Consultancy Study for Crop Life International, Pathhead, Midlothin, UK. https://croplife.org/wp-content/uploads/2014/04/Getting-a-Biotech-Crop-to-Market-Phillips-McDougall-Study.pdf
McPherson SA, Perlak FJ, Fuchs RL, Marrone PG, Lavrik PB, Fischho DA (1988) Characterization of the coleopteran specific protein gene of Bacillus thuringiensis var. tenebrionis. Nat Biotechnol 6:61–66. https://doi.org/10.1038/nbt0188-61
Mehrotra M, Singh AK, Sanyal I, Altosaar I, Amla DV (2011) Pyramiding of modified cry1Ab and cry1Ac genes of Bacillus thuringiensis in transgenic chickpea (Cicer arietinum L.) for improved resistance to pod borer insect Helicoverpa armigera. Euphytica 182:87–102. https://doi.org/10.1007/s10681-011-0501-3
Mertens M (2008) Assessment of Environmental Impacts of Genetically Modified Plants. BfN- Skripten 217. Federal Agency for Nature Conservation, New York, USA. https://www.bfn.de/fileadmin/MDB/documents/service/skript217.pdf
Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL et al (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25:778–785. https://doi.org/10.1038/nbt1319
Miller JC, Tan S, Qiao G, Barlow KA, Wang J et al (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29:143–148. https://doi.org/10.1038/nbt.1755
Miller JK, Bradford KJ (2010) The regulatory bottleneck for biotech specialty crops. Nat Biotechnol 28:1012–1014. https://doi.org/10.1038/nbt1010-1012
Mikami M, Toki S, Endo M (2016) Precision targeted mutagenesis via Cas9 paired nickases in Rice. Plant Cell Physiol 57(5):1058–1068. https://doi.org/10.1093/pcp/pcw049
Moradpour M, Abdulah SNA (2019) CRISPR/dCas9 platforms in plants: strategies and applications beyond genome editing. Plant Biotechnol J. https://doi.org/10.1111/pbi.13232
Morineau C, Bellec Y, Tellier F, Gissot L, Kelemen Z, Nogue F, Faure JD (2017) Selective gene dosage by CRISPR–Cas9 genome editing in hexaploid Camelina sativa. Plant Biotechnol J 15:729–739. https://doi.org/10.1111/pbi.12671
Murai N, Sutton DW, Murray MG, Slightom JL, Merlo DJ, Reichert NA, Sengupta-Gopalan C, Stock CA, Barker RF, Kemp JD, Hall TC (1983) Phaseolin gene from bean is expressed after transfer to sunflower via tumor-inducing plasmid vectors. Science 222:476–482. https://doi.org/10.1126/science.222.4623.476
Nahar K, Hasanuzzaman M, Fujita M (2016) Roles of osmolytes in plant adaptation to drought and salinity. In: Iqbal N, Nazar R, Khan AN (eds) Osmolytes and plants acclimation to changing environment: emerging omics technologies. Springer, New Delhi pp: 37–68
Netherwood T, Martín-Orúe SM, O'Donnell AG, Gockling S, Graham J, Mathers JC, Gilbert HJ (2004) Assessing the survival of transgenic plant DNA in the human gastrointestinal tract. Nat Biotechnol 22:204–209. https://doi.org/10.1038/nbt934
Oliva R, Ji C, Atienza-Grande G et al (2019) Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol. https://doi.org/10.1038/s41587-019-0267-z
Onaga G, Wydra K (2016) Advances in plant tolerance to biotic stresses, plant genomics, Ibrokhim Y. Abdurakhmonov, Intech Open. https://doi.org/10.5772/64351. https://www.intechopen.com/books/plant-genomics/advances-in-plant-tolerance-to-biotic-stresses
Osakabe K, Osakabe Y, Toki S (2010) Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc Natl Acad Sci USA 107:12034–12039. https://doi.org/10.1073/pnas.1000234107
Osakabe Y, Watanabe T, Sugano SS et al (2016) Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci Rep. https://doi.org/10.1038/srep26685
Padgette SR, Kolacz KH, Delannay X, Re DB, LaVallee BJ, Tinius CN, Rhodes WK, Otero YI, Barry GF, Eichholz DA et al (1995) Development, identification and characterization of a glyphosate-tolerant soybean line. Crop Sci 35:1451–1461. https://doi.org/10.2135/cropsci1995.0011183x003500050032x
Paine JA, Shipton CA, Chaggar S et al (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 223:482–487. https://doi.org/10.1038/nbt1082
Parrott WA, All JN, Adang MJ, Bailey MA, Boerma HR, Stewart CN Jr (1994) Recovery and evaluation of soybean plants transgenic for a Bacillus thuringiensis var. kurstaki insecticidal gene. Vitro Cell Dev Biol-Plant 30:144–149. https://doi.org/10.1007/bf02632204
Perlak FJ, Fuchs RL, Dean DA, McPherson SL, Fischho DA (1991) Modifcation of the coding sequence enhances plant expression of insect control protein genes. Proc Natl Acad Sci USA 88:3324–3328. https://doi.org/10.1073/pnas.88.8.3324
Perotti MF, Ribone PA, Chan RL (2017) Plant transcription factors from the homeodomain-leucine zipper family I. Role in development and stress responses. IUBMB Life 69:280–289. https://doi.org/10.1002/iub.1619
Rahman M, Hussain K, Khan MA, Bakhsh A, Rao AQ (2012) An insight of cotton leaf curl virus: a devastating plant pathogenic begomovirus. Pure Appl Bio 1:52–58. https://doi.org/10.19045/bspab.2012.13001
Ramachandran S, Buntin GD, All JN, Tabashnik BE, Raymer PL, Adang MJ, Pulliam DA, Stewart CN Jr (1998) Survival, development, and oviposition of resistant diamondback moth (Lepidoptera: Plutellidae) on transgenic canola producing a Bacillus thuringiensis toxin. J Econ Entomol 91:1239–1244. https://doi.org/10.1093/jee/91.6.1239
Rascón-Cruz Q, Sinagawa-García S, Osuna-Castro JA, Bohorova N, ParedesLopez O (2004) Accumulation, assembly, and digestibility of amarantin expressed in transgenic tropical maize. Theor Appl Genet 108:335–342. https://doi.org/10.1007/s00122-003-1430-x
Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mundy J (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161:1783–1794. https://doi.org/10.1104/pp.112.210773
Ravelonandro M, Scorza R, Bachelier JC, Labonne G, Levy L, Damsteegt V, Callahan AM, Dunez J (1997) Resistance of transgenic Prunus domestica to Plum pox virus infection. Plant Dis 81:1231–1235. https://doi.org/10.1094/pdis.1997.81.11.1231
Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154(6):1380–1389. https://doi.org/10.1016/j.cell.2013.08.021
Raza A, Razzaq A, Mehmood SS, Zou X, Zhang X, Lv Y, Xu J (2019) Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8:34. https://doi.org/10.3390/plants8020034
Rensburg JBJ (2007) First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S Afr J Plant Soil 27:147–151. https://doi.org/10.1080/02571862.2007.10634798
Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696. https://doi.org/10.1104/pp.103.033431
Rommens CM, Haring MA, Swords K, Davies HV (2007) The intragenic approach as a new extension to traditional plant breeding. Trends Plant Sci 12:397–403. https://doi.org/10.1016/j.tplants.2007.08.001
Ruiz-Lopez N, Haslam RP, Napier JA, Sayanova O (2014) Successful high-level accumulation of fish oil omega-3 long-chain polyunsaturated fatty acids in a transgenic oilseed crop. Plant J 77:198–208. https://doi.org/10.1111/tpj.12378
Sander JD, Dahlborg EJ, Goodwin MJ, Cade L, Zhang F, Cifuentes D, Curtin SJ, Blackburn JS, Thibodeau-Beganny S, Qi Y et al (2011) Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat Methods 8:67–69. https://doi.org/10.1038/nmeth.1542
Sanyal I, Singh AK, Kaushik M, Amla DV (2005) Agrobacterium mediated transformation of chickpea (Cicer arietinum L.) with Bacillus thuringiensis cry1Ac gene for resistance against pod borer insect Helicoverpa armigera. Plant Sci 168:1135–1146. https://doi.org/10.1016/j.plantsci.2004.12.015
Sauer H, Wild A, Ruhle W (1987) The effect of phosphinothricin (glufosinate) on photosynthesis II. The cause of inhibition of photosynthesis. Zeitschrift für Naturforschung C 42:270–278. https://doi.org/10.1515/znc-1987-0317
Sauer NJ, Mozoruk J, Miller RB, Warburg ZJ, Walker KA, Beetham PR et al (2016) Oligonucleotide-directed mutagenesis for precision gene editing. Plant Biotechnol J 14:496–502. https://doi.org/10.1111/pbi.12496
Schiml S, Fauser F, Puchta H (2014) The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J 80:1139–1150. https://doi.org/10.1111/tpj.12704
Schouten HJ, Krens FA, Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants. EMBO Rep 7:750–753. https://doi.org/10.1038/sj.embor.7400769
Sears MK, Hellmich RL, Stanley-Horn DE, Oberhauser KS, Pleasants JM, Mattila HR, Siegfried BD, Dively GP (2001) Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proc Natl Acad Sci USA 98:11937–11942. https://doi.org/10.1073/pnas.211329998
Seralini GE, Clair E, Mesnage R, Gress S, Defarge N, Malatesta M, Hennequin D, de Vendômois JS (2012) Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Food Chem Toxicol 50:4221–4231. https://doi.org/10.1016/j.fct.2013.11.047
Seralini GE, Clair E, Mesnage R, Gress S, Defarge N, Malatesta M, Hennequin D, de Vendômois JS (2014) Republished study: long-term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Environ Sci Eur 26:14. https://doi.org/10.1186/s12302-014-0014-5
Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791–800. https://doi.org/10.1111/pbi.12312
Shen L, Hua Y, Fu Y, Li J, Liu Q, Jiao X et al (2017) Rapid generation of genetic diversity by multiplex CRISPR/Cas9 genome editing in rice. Sci China Life Sci 60:506–515. https://doi.org/10.1007/s11427-017-9008-8
Shen L, Wang C, Fu Y, Wang J, Liu Q, Zhang X et al (2018) QTL editing confers opposing yield performance in different rice varieties. J Integr Plant Biol 60:89–93. https://doi.org/10.1111/jipb.12501
Sherkow JS (2018) The CRISPR patent landscape: past, present and future. CRISPR J 1:5–9. https://doi.org/10.1089/crispr.2017.0013
Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X, Choi VM, Rock JM, Wu YY, Katibah GE, Zhifang G, McCaskill D, Simpson MA, Blakeslee B, Greenwalt SA, Butler HJ, Hinkley SJ, Zhang L, Rebar EJ, Gregory PD, Urnov FD (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437–441. https://doi.org/10.1038/nature07992
Sindhu AS, Zheng ZW, Murai N (1997) The pea seed storage protein legumin was synthesized, processed and accumulated stably in transgenic rice endosperm. Plant Sci 130:189–196. https://doi.org/10.1016/S0168-9452(97)00219-7
Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: A review. Rev Environ Sci Biotechnol 14:407–426. https://doi.org/10.1007/s11157-015-9372-8
Smart RD, Blum M, Wesseler J (2017) Trends in approval times for genetically engineered crops in the United States and the European Union. J Agricul Econ 68:182–198. https://doi.org/10.1111/1477-9552.12171
Songstad DD, Petolino JF, Voytas DF, Reichert NA (2017) Genome Editing of Plants. Crit Rev Plant Sci 36:1–23. https://doi.org/10.1080/07352689.2017.1281663
Stewart CN Jr, Adang MJ, All JA, Raymer PL, Ramachandran S, Parrott WA (1996) Insect control and dosage effects in transgenic canola containing a synthetic Bacillus thuringiensis cryIAC gene. Plant Physiol 112:115–120. https://doi.org/10.1104/pp.112.1.115
St-Onge M, Jones P (2003) Greater rise in fat oxidation with medium-chain triglyceride consumption relative to long-chain triglyceride is associated with lower initial body weight and greater loss of subcutaneous adipose tissue. Int J Obes 27:1565–1571. https://doi.org/10.1038/sj.ijo.0802467
Stöger E, Parker M, Christou P, Casey R (2001) Pea legumin overexpressed in wheat endosperm assembles into an ordered para Crystalline matrix. Plant Physiol 125:1732–1742. https://doi.org/10.1104/pp.125.4.1732
Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, Bing JW, Huckaba RM (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103:1031–1038. https://doi.org/10.1603/ec10040
Suzie K, Ma JKC, Drake PMW (2008) Genetically modified plants and human health. J R Soc Med 101:290–298. https://doi.org/10.1258/jrsm.2008.070372
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43. https://doi.org/10.1111/nph.12797
Swarts DC, Jinek M (2018) Cas9 versus Cas12a/Cpf1: Structure–function comparisons and implications for genome editing. Wiley Interdiscip Rev RNA 9:e1481. https://doi.org/10.1002/wrna.1481
Tabashnik BE, Gassman AJ, Crowder DW, Carriere Y (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26:199–202. https://doi.org/10.1038/nbt1382
Tabashnik BE, Finson N, Johnson MW, Moar WJ (1993) Resistance to toxins from Bacillus thuringiensis subsp. kurstaki causes minimal cross-resistance to B. thuringiensis subsp. aizawai in diamondback moth (Lepidoptera: Plutellidae). Appl Environ Microbiol 59:1332–1335. https://aem.asm.org/content/59/5/1332
Tabashnik BE, Carrière Y (2010) Field-evolved resistance to Bt cotton: Bollworm in the US and pink bollworm in India. Southwest Entomologist 35:417–424. https://doi.org/10.3958/059.035.0326
Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521. https://doi.org/10.1038/nbt.2597
Tachibana K, Watanabe T, Sekizawa Y, Takematsu T (1986) Action mechanism of bialaphos 2. Accumulation of ammonia in plants treated with bialaphos. J Pestic Sci 1:33–37. https://doi.org/10.1584/jpestics.11.33
Takabe T, Nakamura T, Nomura M, Hayashi Y, Ishitani M, Muramoto Y, Tanaka A, Takabe T (1998) 8-Glycinebetaine and the genetic engineering of salinity tolerance in plants. Stress responses of photosynthetic organisms. Elsevier Science, Amsterdam, pp 115–131. https://doi.org/10.1016/b978-0-444-82884-2.50011-x
Thomas PE, Lawson EC, Zalewski JC, Reed GL, Kaniewski WK (2000) Extreme resistance to Potato leafroll virus in potato cv. Russet Burbank mediated by the viral replicase gene. Virus Res 71:49–62. https://doi.org/10.1016/s0168-1702(00)00187-8
Tohidfar M, Zare N, Jouzani GS, Efekhari SM (2013) Agrobacterium mediated transformation of alfalfa (Medicago sativa) using a synthetic cry3a gene to enhance resistance against alfalfa weevil. Plant Cell Tiss Org 113:227–235. https://doi.org/10.1007/s11240-012-0262-2
Tricoli DM, Carney KJ, Russell PF, McMaster JR, Groff DW et al (1995) Field evaluation of transgenic squash containing single or multiple virus coat protein gene constructs for resistance to cucumber mosaic virus, watermelon mosaic virus 2 and zucchini yellow mosaic virus. Nat Biotechnol 13:1458–1465. https://doi.org/10.1038/nbt1295-1458
Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, Goodwin MJ, Aryee MJ, Joung JK (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32:569–576. https://doi.org/10.1038/nbt.2908
Tsatsakis AM, Nawaz MA, Kouretas D, Balias G, Savolainen K, Tutelyan VA, Golokhvast KS, Lee JD, Yang SH, Chung G (2017) Environmental impacts of genetically modified plants: a review. Food Chem Toxicol 156:818–833. https://doi.org/10.1016/j.envres.2017.03.011
Tuteja N, Gill SS (2014) Climate change and plant abiotic stress tolerance. Wiley-Blackwell, Amsterdam p 1208. ISBN: 978-3-527-33491-9. https://www.wiley.com/en-us/Climate+Change+and+Plant+Abiotic+Stress+Tolerance-p-9783527334919
Tuteja N, Verma S, Sahoo R, Raveendar S, Reddy I (2012) Recent advances in development of marker free transgenic plants: regulation and biosafety concern. J Biosci 37:167–197. https://doi.org/10.1007/s12038-012-9187-5
US EPA (2017) Starlink™ corn regulatory information. Pesticides. US EPA. https://www3.epa.gov/pesticides/chem_search/reg_actions/pip/starlink_corn.htm#proposal
USDA APHIS (2020) https://www.aphis.usda.gov/aphis/ourfocus/biotechnology/am-i-regulated
Usher S, Han L, Haslam RP, Michaelson LV, Sturtevant D, Aziz M, Chapman KD, Sayanova O, Napier JA (2017) Tailoring seed oil composition in the real world: optimising omega-3 long chain polyunsaturated fatty acid accumulation in transgenic Camelina sativa. Sci Rep 7:6570. https://doi.org/10.1038/s41598-017-06838-0
Vanblaere T, Szankowski I, Schaart J, Schouten H, Flachowsky H, Broggini GA, Gessler C (2011) The development of a cisgenic apple plant. J Biotechnol 154:304–311. https://doi.org/10.1016/j.jbiotec.2011.05.013
Vaughn T, Cavato T, Brar G, Coombe T, DeGooyer T, Ford S, Groth M, Howe A, Johnson S, Kolacz K et al (2005) A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci 45:931–938. https://doi.org/10.2135/cropsci2004.0304
Vauterin M, Frankard V, Jacobs M (2000) Functional rescue of a bacterial dapA auxotroph with a plant cDNA library selects for mutant clones encoding a feedback-insensitive dihydrodipicolinate synthase. Plant J 21:239–248. https://doi.org/10.1046/j.1365-313x.2000.00668.x
Veillet F, Perrot L, Chauvin L, Kermarrec MP, Guyon-Debast A, Chauvin JE, Nogue F, Mazier M (2019) Transgene-free genome editing in tomato and potato plants using agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. Int J Mol Sci 20:402. https://doi.org/10.3390/ijms20020402
Wang B, Zhu L, Zhao B, Zhao Y, Xie Y, Zheng Z, Li Y, Sun J, Wang H (2019) Development of a haploid-inducer mediated genome editing (IMGE) system for accelerating maize breeding. Mol Plant 12:597–602. https://doi.org/10.1016/j.molp.2019.03.006
Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C et al (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951. https://doi.org/10.1038/nbt.2969
Waltz E (2014) Beating the heat. Nat Biotechnol 32:610–613. https://doi.org/10.1038/nbt.2948
Waltz E (2015) USDA approves next-generation GM potato. Nat Biotechnol 33:12–13. https://doi.org/10.1038/nbt0115-12
Waltz E (2016) CRISPR-edited crops free to enter market, skip regulation. Nat Biotechnol 34:582. https://doi.org/10.1038/nbt0616-582
Waltz E (2018) With a free pass, CRISPR-edited plants reach market in record time. Nat Biotechnol 36:6–7. https://doi.org/10.1038/nbt0118-6b
Waltz E (2019) Appetite grows for biotech foods with health benefits. Nat Biotechnol 37:573–580. https://doi.org/10.1038/d41587-019-00012-9
Watrud LS, Lee EH, Fairbrother A, Burdick C, Reichman JR, Bollman M, Storm M, King G, van de Water PK (2004) Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proc Natl Acad Sci USA 101:14533–14538. https://doi.org/10.1073/pnas.0405154101
Whelan AI, Lema MA (2015) Regulatory framework for gene editing and other new breeding techniques (NBTs) in Argentina. GM Crops Food 6:253–265. https://doi.org/10.1080/21645698.2015.1114698
WHO (2008) Interim summary of conclusions and dietary recommendations on total fat and fatty acids, from the Joint FAO/WHO Expert Consultation on fats and fatty acids in human nutrition. 10–14 November 2008, WHO: Geneva. https://www.who.int/nutrition/topics/FFA_summary_rec_conclusion.pdf
WHO (2009) Global prevalence of vitamin A deficiency in populations at risk 1995–2005. WHO global database on vitamin A deficiency. Geneva, World Health Organization. https://www.who.int/nutrition/publications/micronutrients/vitamin_a_deficiency/9789241598019/en/
Wolt JD, Wang K, Yang B (2016) The regulatory status of genome-edited crops. Plant Biotechnol J 14:510–518. https://doi.org/10.1111/pbi.12444
Wunn J, Kloti A, Burkhardt PK, Biswas GCG, Launis K, Iglesias VA, Potrykus I (1996) Transgenic Indica rice breeding line IR58 expressing a synthetic cryIA(b) gene from Bacillus thuringiensis provides effective insect pest control. BioTechnol 14:171–176. https://doi.org/10.1038/nbt0296-171
Yamamoto T, McLaughlin RE (1981) Isolation of a protein from the parasporal crystal of Bacillus thuringiensis var. kurstaki toxic to the mosquito larva Aedes taeniorhynchus. Biochem Biophys Res Commun 103:414–421. https://doi.org/10.1016/0006-291x(81)90468-x
Yan F, Zhang WW, Xiao H, Li SF, Cheng ZM (2007) Transgenic wheat expressing virus-derived hairpin RNA is resistant to Barley yellow dwarf virus. Yi Chuan 29:97–102. https://doi.org/10.1360/yc-007-0097. https://www.ncbi.nlm.nih.gov/pubmed/17284432
Yan S, Zhu J, Zhu W, Li Z, Shelton AM, Luo J, Cui J, Zhang Q, Liu X (2015) Pollen-mediated gene flow from transgenic cotton under greenhouse conditions is dependent on different pollinators. Sci Rep 5:15917. https://doi.org/10.1038/srep15917
Yang RC, Xu HL, Yu WG, Lu CG, Long MS, Liu CQ, Pan NS, Chen ZL (1995) Transgenic tomato plants expressing cucumber mosaic virus coat protein (CMV-cp) and their resistance to cucumber mosaic virus (CMV). Acta Agric Jiangsu 11:42–46
Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305. https://doi.org/10.1126/science.287.5451.303
Zhang C, Wohlhueter R, Zhang H (2016) Genetically modified foods: a critical review of their promise and problems. Food Sci Hum Wellness 5:116–123. https://doi.org/10.1016/j.fshw.2016.04.002
Zhou J, Xin X, He Y, Chen H, Li Q, Tang X et al (2018) Multiplex QTL editing of grain-related genes improves yield in elite rice varieties. Plant Cell Rep 38:475–485. https://doi.org/10.1007/s00299-018-2340-3
Zhu YX, Ou-Yang WJ, Zhang YF, Chen ZL (1996) Transgenic sweet pepper plants from Agrobacterium mediated transformation. Plant Cell Rep 16:71–75. https://doi.org/10.1007/s002990050179
Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C (2017) Precise base editing in rice, wheat and maize with a Cas9–cytidine deaminase fusion. Nat Biotechnol 35:438–440. https://doi.org/10.1038/nbt.3811
Acknowledgements
The maize transformation and genome editing work in the laboratory of the corresponding author is funded by National Agricultural Science Fund (NASF; competitive Grant no. NASF/GTR-5004/2015-16/204). The funds from the Indian Council of Agricultural Research (ICAR) are gratefully acknowledged. GG, AD and AKJ acknowledge NASF support in the form of SRF, RA and LA fellowships, respectively.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kumar, K., Gambhir, G., Dass, A. et al. Genetically modified crops: current status and future prospects. Planta 251, 91 (2020). https://doi.org/10.1007/s00425-020-03372-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-020-03372-8