Skip to main content

Genetically modified (GM) crops: milestones and new advances in crop improvement

Abstract

Key message

New advances in crop genetic engineering can significantly pace up the development of genetically improved varieties with enhanced yield, nutrition and tolerance to biotic and abiotic stresses.

Abstract

Genetically modified (GM) crops can act as powerful complement to the crops produced by laborious and time consuming conventional breeding methods to meet the worldwide demand for quality foods. GM crops can help fight malnutrition due to enhanced yield, nutritional quality and increased resistance to various biotic and abiotic stresses. However, several biosafety issues and public concerns are associated with cultivation of GM crops developed by transgenesis, i.e., introduction of genes from distantly related organism. To meet these concerns, researchers have developed alternative concepts of cisgenesis and intragenesis which involve transformation of plants with genetic material derived from the species itself or from closely related species capable of sexual hybridization, respectively. Recombinase technology aimed at site-specific integration of transgene can help to overcome limitations of traditional genetic engineering methods based on random integration of multiple copy of transgene into plant genome leading to gene silencing and unpredictable expression pattern. Besides, recently developed technology of genome editing using engineered nucleases, permit the modification or mutation of genes of interest without involving foreign DNA, and as a result, plants developed with this technology might be considered as non-transgenic genetically altered plants. This would open the doors for the development and commercialization of transgenic plants with superior phenotypes even in countries where GM crops are poorly accepted. This review is an attempt to summarize various past achievements of GM technology in crop improvement, recent progress and new advances in the field to develop improved varieties aimed for better consumer acceptance.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Ambavaram MMR, Basu S, Krishnan A, Ramegowda V, Batlang U, Rahman L, Baisakh N, Pereira A (2014) Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. Nat Commun 31:5302

    Article  CAS  Google Scholar 

  • Amin M, Elias SM, Hossain A, Ferdousi A, Rahman MS, Tuteja N, Seraj ZI (2012) Overexpression of a DEAD box helicase, PDH45, confers both seedling and reproductive stage salinity tolerance to rice (Oryza sativa L.). Mol Breed 30:345–354

    CAS  Article  Google Scholar 

  • Anand A, Zhou T, Trick HN, Gill BS, Bockus WW, Muthukrishnan S (2003) Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin-like protein, chitinase and glucanase against Fusarium graminearum. J Exp Bot 54:1101–1111

    CAS  PubMed  Article  Google Scholar 

  • Aragao FJ, Faria JC (2009) First transgenic geminivirus-resistant plant in the field. Nat Biotechnol 27:1086–1088

    CAS  PubMed  Article  Google Scholar 

  • Atkinson RG, Sutherland PW, Johnston SL, Gunaseelan K, Hallett IC, Mitra D, Brummell DA, Schroder R, Johnston JW, Schaffer RJ (2012) Down-regulation of polygalacturonase 1 alters firmness, tensile strength and water loss in apple (Malus domestica) fruit. BMC Plant Biol 12:129

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Azam M, Kesarwani M, Chakraborty S, Natarajan K, Datta A (2002) Cloning and characterization of 5′-flanking region of oxalate decarboxylase gene from Flammulina velutipes. Biochem J 367:67–75

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN, Bisaro DM, Voytas DF (2015) Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nat Plants 1:15145

    CAS  Article  Google Scholar 

  • Bapat VA, Trivedi PK, Ghosh A, Sane VA, Ganapathi TR, Nath P (2010) Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol Adv 28:94–107

    CAS  PubMed  Article  Google Scholar 

  • Bevan MW, Flavell RB, Chilton MD (1983) A chimeric antibiotic resistance gene as a selectable marker for plant cell transformation. Nature 304:184–187

    CAS  Article  Google Scholar 

  • Bhatnagar MK, Prasad P, Mathur PB, Narasu ML, Waliyar F, Sharma KK (2010) An efficient method for the production of marker-free transgenic plants of peanut (Arachis hypogaea L.). Plant Cell Rep 29:495–502

    CAS  PubMed  Article  Google Scholar 

  • Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424

    CAS  PubMed  Article  Google Scholar 

  • Bibikova M, Beumer K, Trautman JK, Carroll D (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300:764

    CAS  PubMed  Article  Google Scholar 

  • Bogdanove AJ, Voytas DF (2011) TAL effectors: customizable proteins for DNA targeting. Science 333:1843–1846

    CAS  PubMed  Article  Google Scholar 

  • Bonfim K, Faria JC, Nogueira EOPL, Mendes EA, Aragao JFJL (2007) RNAi-mediated resistance to bean golden mosaic virus in genetically engineered common bean (Phaseolus vulgaris). Mol Plant-Microbe Interact. 20:717–726

    CAS  PubMed  Article  Google Scholar 

  • Borsani O, Valpuesta V, Botella MA (2003) Developing salt tolerant plants in a new century: a molecular biology approach. Plant Cell Tissue Organ Cult 73:101–115

    CAS  Article  Google Scholar 

  • Brinch-Pedersen H, Hatzack F, Stoger E, Arcalis E, Pontopidan K, Holm PB (2006) Heat-stable phytases in transgenic wheat (Triticum aestivum L.): deposition pattern, thermostability, and phytate hydrolysis. J Agric Food Chem 54:4624–4632

    CAS  PubMed  Article  Google Scholar 

  • Brini F, Yamamoto A, Jlaiel L et al (2011) Pleiotropic effects of the wheat dehydrin DHN-5 on stress responses in Arabidopsis. Plant Cell Physiol 52:676–688

    CAS  PubMed  Article  Google Scholar 

  • Campbell MA, Fitzgerald HA, Ronald PC (2002) Engineering pathogen resistance in crop plants. Transgenic Res 11:599–613

    CAS  PubMed  Article  Google Scholar 

  • Cardoso FM et al (2014) Single domain antibodies targeting neuraminidase protect against an H5N1 influenza virus challenge. J Virol 88:82788296

    Article  CAS  Google Scholar 

  • Carpenter JE (2010) Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nat Biotechnol 28:319–321

    CAS  PubMed  Article  Google Scholar 

  • Carroll D (2011) Genome engineering with zinc-finger nucleases. Genetics 188:773–782

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor based agricultural biotechnology products. Plant Physiol 147:20–29

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Chakraborty S, Chakraborty N, Datta A (2000) Increased nutritive value of transgenic potato by expressing a non allergenic seed albumin gene from Amaranthus hypochondriacus. Proc Natl Acad Sci USA 97:3724–3729

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Chakraborty S, Chakraborty N, Agrawal L, Ghosh S, Narula K, Shekhar S, Prakash Naik S, Pande PC, Chakrborti SK, Datta A (2010) Next generation protein rich potato by expressing a seed protein gene Am A1 as a result of proteome rebalancing in transgenic tuber. Proc Natl Acad Sci USA 41:17533–17538

    Article  Google Scholar 

  • Chandra Babu R, Zhang J, Blum A, David Ho TH, Wu R, Nguyen HT (2004) HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci 166:855–862

    Article  CAS  Google Scholar 

  • Chapple C, Carpita N (1998) Plant cell walls as targets for biotechnology. Curr Opin Plant Biol 1:179–185

    CAS  PubMed  Article  Google Scholar 

  • Chauhan H, Khurana N, Nijhavan A, Khurana JP, Khurana P (2012) The wheat chloroplastic small heat shock protein (sHSP26) is involved in seed maturation and germination and imparts tolerance to heat stress. Plant Cell Environ 35:1912–1931

    CAS  PubMed  Article  Google Scholar 

  • Chawla R, Ariza-Nieto M, Wilson AJ, Moore SK, Srivastava V (2006) Transgene expression produced by biolistic-mediated, site-specific gene integration is consistently inherited by the subsequent generations. Plant Biotechnol J 4:209–218

    CAS  PubMed  Article  Google Scholar 

  • Chawla R, Shakya R, Rommens CM (2012) Tuber-specific silencing of aspargine synthetase-1 reduces the crylamide-forming potential of potatoes grown in the field without affecting tuber shape and yield. Plant Biotechnol J 10:913–924

    CAS  PubMed  Article  Google Scholar 

  • Chen R, Xue G, Chen P, Yao B, Yang W, Ma Q, Fan Y, Zhao Z, Tarczynski MC, Shi J (2008) Transgenic maize plants expressing a fungal phytase gene. Transgenic Res 17:633–643

    CAS  PubMed  Article  Google Scholar 

  • Chilton MD (1983) A vector for introducing new genes into plants. Sci Am 248:36–45

    Article  Google Scholar 

  • Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A et al (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Collier SM, Moffett P (2009) NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci 14:521–529

    CAS  PubMed  Article  Google Scholar 

  • Collinge DB, Lund OS, Thordal-Christensen H (2008) What are the prospects for genetically engineered, disease resistant plants? Eur J Plant Pathol 121:217–231

    CAS  Article  Google Scholar 

  • Cook DR, Varshney RK (2010) From genome studies to agricultural biotechnology: closing the gap between basic plant science and applied agriculture. Curr Opin Plant Biol 13:115–118

    PubMed  Article  Google Scholar 

  • Curtin SJ et al (2011) Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol 156:466–473

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Curtin SJ, Anderson JE, Starker CG, Baltes NJ, Mani D et al (2013) Targeted mutagenesis for functional analysis of gene duplication in legumes. Methods Mol Biol 1069:25–42

    CAS  PubMed  Article  Google Scholar 

  • Dale EC, Ow DW (1991) Gene transfer with subsequent removal of the selection gene from the host genome. Proc Natl Acad Sci USA 88:10558–10562

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Datta K, Baisakh N, Ganguly M, Krishnan S, Shinozaki KY, Datta SK (2012) Overexpression of Arabidopsis and rice stress genes inducible transcription factor confers drought and salinity tolerance to rice. Plant Biotechnol J 10:579–586

    CAS  PubMed  Article  Google Scholar 

  • Dhekney SA, Li ZT, Gray DJ (2011) Grapevines engineered to express cisgenic Vitis vinifera thaumatin-like protein exhibit fungal disease resistance. In Vitro Cell Dev Biol Plant 47:458–466

    CAS  Article  Google Scholar 

  • Djukanovic V et al (2013) Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J 76:888–899

    CAS  PubMed  Article  Google Scholar 

  • Dodo HW, Konan KN, Chen FC, Egnin M, Viquez OM (2008) Alleviating peanut allergy using genetic engineering: the silencing of the immunodominant allergen Ara h 2 leads to its significant reduction and a decrease in peanut allergenicity. Plant Biotechnol J 6:135–145

    CAS  PubMed  Article  Google Scholar 

  • Drakakaki G, Marcel S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stoger E (2005) Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Mol Biol 59:869–880

    CAS  PubMed  Article  Google Scholar 

  • Duan J, Cai W (2012) OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. PLoS One 7:e45117

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Duan CG, Wang CH, Fang RX, Guo HS (2008) Artificial microRNAs highly accessible to targets confer efficient virus resistance in plants. J Virol 82:11084–11095

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Ebinuma H, Komamine A (2001) MAT (multi auto-transformation) vector system. The oncogenes of Agrobacterium as positive markers for regeneration and selection of marker-free transgenic plants. In Vitro Cell Dev Biol Plant 37:103–113

    CAS  Article  Google Scholar 

  • Ebinuma H, Sugita K, Matsunaga E, Endo S, Yamada K, Komamine A (2001) Systems for the removal of a selection marker and their combination with a positive marker. Plant Cell Rep 20:383–392

    CAS  Article  Google Scholar 

  • Eggeling L, Oberle S, Sahm H (1998) Improved l-lysine yield with Corynebacterium glutamicum: use of dapA resulting in increased flux combined with growth limitation. Appl Microbiol Biotechnol 49:24–30

    CAS  PubMed  Article  Google Scholar 

  • Endo S, Sugita K, Sakai M, Tanaka H, Ebinuma H (2002) Single-step transformation for generating marker-free transgenic rice using the ipt-type MAT vector system. Plant J 30:115–122

    CAS  PubMed  Article  Google Scholar 

  • Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, Clemente-Moreno MJ, Alcobendas R, Artlip T, Hernandez JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J Exp Bot 62:2599–6132

    CAS  PubMed  Article  Google Scholar 

  • Falco SC, Guida T, Locke M, Mauvais J, Sanders C, Ward RT, Webber P (1995) Transgenic canola and soybean seeds with increased lysine. Bio/Technology 13:577–582

    CAS  PubMed  Article  Google Scholar 

  • Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P et al (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23:1229–1232

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Feng Z et al (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA 111:4632–4637

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Fraley RT, Rogers SG, Horsch RB, Sanders PR, Flick JS, Adams SP, Bittner ML, Brand LA, Fink CL (1983) Expression of bacterial genes in plant cells. Proc Natl Acad Sci USA 80:4803–4807

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Gadaleta A, Giancaspro A, Blechl AE, Blanco A (2008) A transgenic durum wheat line that is free of marker genes and expresses 1DY10. J Cereal Sci 48:439–445

    CAS  Article  Google Scholar 

  • Gao H et al (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J 61:176–187

    CAS  PubMed  Article  Google Scholar 

  • Gaskell G, Bauer M (2001) The years of controversy. In: Gaskell G, Bauer M (eds) Biotechnology 1996–1999. Science Museum, London, pp 3–11

    Google Scholar 

  • Geißler R et al (2011) Transcriptional activators of human genes with programmable DNA-specificity. PLoS One 6:e19509

    PubMed  Article  CAS  Google Scholar 

  • Ghosh S, Meli VK, Kumar A, Thakur A, Chakraborty N, Chakraborty S, Datta A (2011) The N-glycan processing enzymes α-mannosidase and β-D-1 N acetylhexosaminidase are involved in ripening-associated softening in the non climacteric fruits of capsicum. J Exp Bot 62:571–582

    CAS  PubMed  Article  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  PubMed  Article  Google Scholar 

  • Gonsalves D, Ferreira S, Manshardt R, Fitch M, Slightom J (1998) Transgenic virus resistant papaya: new hope for controlling papaya ringspot virus in Hawaii. APS Feature, American Pythopathological Society. doi:10.1094/PHP-2000-0621-01-RV

    Google Scholar 

  • Goto F, Yoshihara T, Saiki H (2000) Iron accumulation and enhanced growth in transgenic lettuce plants expressing the iron-binding protein ferritin. Theor Appl Genet 100:658–664

    CAS  Article  Google Scholar 

  • Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK, Park SW (2012) Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol. 78:51–65

    CAS  Article  Google Scholar 

  • Hallwass M et al (2014) The Tomato spotted wilt virus cell to cell movement protein (NSM) triggers a hypersensitive response in Sw5 containing resistant tomato lines and in Nicotiana benthamiana transformed with the functional Sw5b resistance gene copy Mol. Plant Pathol 15:871880

    Google Scholar 

  • Halpin C (2005) Gene stacking in transgenic plants—the challenge for 21st century plant biotechnology. Plant Biotechnol J 3:141–155

    CAS  PubMed  Article  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952

    CAS  PubMed  Article  Google Scholar 

  • Haun W et al (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol 12:934–940

    CAS  Article  Google Scholar 

  • Haverkort AJ, Struik PC, Visser RGF, Jacobsen E (2009) Applied biotechnology to combat late blight in potato caused by Phytophthora infestans. Potato Res 52:249–264

    Article  Google Scholar 

  • Herman EM, Helm RM, Jung R, Kinney AJ (2003) Genetic modification removes an immunodominant allergen from soybean. Plant Physiol 132:36–43

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Herrera-Estrella L, Depicker A, van Montagu M, Schell J (1983) Expression of chimaeric genes transferred into plant cells using aTi-plasmid-derived vector. Nature 303:209–213

    CAS  Article  Google Scholar 

  • Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Curr Opin Plant Biol 11:228–231

    CAS  PubMed  Article  Google Scholar 

  • 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

    CAS  PubMed  Article  Google Scholar 

  • Irfan M, Ghosh S, Kumar V, Chakraborty N, Chakraborty S, Datta A (2014) Insights into transcriptional regulation of β-D-N-acetylhexosaminidase, an N-glycan-processing enzyme involved in ripening-associated fruit softening. J Exp Bot 65:5835–5848

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Irfan M, Ghosh S, Meli VS, Kumar A, Kumar V, Chakraborty N, Chakraborty S, Datta A (2016) Fruit ripening regulation of α-mannosidase expression by the MADS box transcription factor RIPENING INHIBITOR and ethylene. Front Plant Sci 7:10. doi:10.3389/fpls.2016.00010

    PubMed  PubMed Central  Article  Google Scholar 

  • Jacobsen E, Schouten HJ (2009) Cisgenesis: an important subinvention for traditional plant breeding companies. Euphytica 170:235–247

    Article  Google Scholar 

  • Jagadeesh BH, Prabha TN (2002) β-Hexosaminidase, an enzyme from ripening bell capsicum (Capsicum annuum var. variata). Phytochemistry 61:295–300

    CAS  PubMed  Article  Google Scholar 

  • Jagadeesh BH, Prabha TN, Srinivasan K (2004) Activities of β-hexosaminidase and α-mannosidase during development and ripening of bell capsicum (Capsicum annuum var. variata). Plant Sci 167:1263–1271

    CAS  Article  Google Scholar 

  • James C (2013) Global status of commercialized biotech/GM crops. Brief no. 46. ISAAA, Ithaca

  • Jewell MC, Campbell BC, Godwin ID (2010) Transgenic plants for abiotic stress resistance. In: Kole C, Michler CH, Abbott AG, Hall TC (eds) Transgenic crop plants, vol 2. Springer, Berlin, pp 67–132

    Chapter  Google Scholar 

  • Ji X, Zhang H, Zhang Y, Wang Y, Gao C (2015) Establishing a CRISPR–Cas-like immune system conferring DNA virus resistance in plants. Nat Plants 1:15144

    CAS  PubMed  Article  Google Scholar 

  • Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One 9:e93806

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41:e188

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Johnson AA, Kyriacou B, Callahan DL, Carruthers L, Stangoulis J, Lombi E et al (2011) Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm. PLoS One 6:e24476. doi:10.1371/journal.pone.0024476

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Joshi SG, Schaart JG, Groenwold R, Jacobsen E, Schouten HJ, Krens FA (2011) Functional analysis and expression profiling of HcrVf1 and HcrVf2 for development of scab resistant cisgenic and intragenic apples. Plant Mol Biol 75:579–591

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kamthan A, Kamthan M, Azam M, Chakraborty N, Chakraborty S, Datta A (2012) Expression of a fungal sterol desaturase improves tomato drought tolerance, pathogen resistance and nutritional quality. Sci Rep 2:951

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Kamthan A, Kamthan M, Kumar A, Sharma P, Ansari S, Thakur SS, Chaudhuri A, Asis Datta (2015a) A Calmodulin like EF hand protein positively regulates oxalate decarboxylase expression by interacting with E-box elements of the promoter. Sci Rep 5:14578. doi:10.1038/srep14578

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kamthan A, Chaudhuri A, Kamthan M, Datta A (2015b) Small RNAs in plants: recent development and application for crop improvement. Front Plant Sci 6:208

    PubMed  PubMed Central  Article  Google Scholar 

  • Karaba A, Dixit S, Greco R et al (2007) Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc Natl Acad Sci USA 104:15270–15275

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kesarwani M, Azam M, Natarajan K, Mehta A, Datta A (2000) Oxalate decarboxylase from Collybia velutips: molecular cloning and its over expression to confer resistance to fungal infection in transgenic tobacco and tomato. J Biol Chem 275:7230–7238

    CAS  PubMed  Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kim YH, Kim CY, Song WK, Park DS, Kwon SY, Lee HS et al (2008) Overexpression of sweet potato swpa4 peroxidase results in increased hydrogen peroxide production and enhances stress tolerance in tobacco. Planta 227:867–881

    CAS  PubMed  Article  Google Scholar 

  • Komari T, Hiei Y, Saito Y, Murai N, Kumasiashiro T (1996) Vectors carrying two separate T-DNAs for co-transformation of higher plants mediated by Agrobacterium tumefaciens and segregation of transformants free from selection markers. Plant J 10:165–174

    CAS  PubMed  Article  Google Scholar 

  • Komor AC, Kim YB, Packer MS, Juris JA, Liu DR (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. doi:10.1038/nature17946

    Google Scholar 

  • Kumar V, Chattopadhyay A, Ghosh S, Irfan M, Chakraborty N, Chakraborty S, Datta A (2016) Improving nutritional quality and fungal tolerance in soya bean and grass pea by expressing an oxalate decarboxylase. Plant Biotechnol J 14:1394–1405

    CAS  PubMed  Article  Google Scholar 

  • Langdale JA (2011) C4 cycles: past, present, and future research on C4 photosynthesis. Plant Cell 23:3879–3892

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Lassen J, Madsen KH, Sandøe P (2002) Ethics and genetic engineering—lessons to be learned from GM foods. Bioprocess Biosyst Eng 24:263–271

    CAS  Article  Google Scholar 

  • Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748

    CAS  PubMed  Article  Google Scholar 

  • Li Y, Zhu B, Xu W, Zhu H, Chen A, Xie Y, Shao Y, Luo Y (2007) LeERF1 positively modulated ethylene triple response on etiolated seedling, plant development and fruit ripening and softening in tomato. Plant Cell Rep 26:1999–2008

    CAS  PubMed  Article  Google Scholar 

  • Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J et al (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31:688–691

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genom 41:63–68

    CAS  Article  Google Scholar 

  • Litz RE, Padilla G (2012) Genetic transformation of fruit trees. In: Priyadarshan PM, Schnell RJ (eds) Genomics of tree crops. Springer, Berlin, pp 117–153

    Chapter  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Liu HK, Yang C, Wei ZW (2005) Heat shock-regulated site-specific excision of extraneous DNA in transgenic plants. Plant Sci 168:997–1003

    CAS  Article  Google Scholar 

  • Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365

    CAS  PubMed  Article  Google Scholar 

  • Lucca P, Hurrell R, Potrykus I (2002) Fighting iron deficiency anemia with iron-rich rice. J Am Coll Nutr 21:184S–190S

    CAS  PubMed  Article  Google Scholar 

  • Mahfouz MM et al (2012) Targeted transcriptional repression using a chimeric TALE–SRDX repressor protein. Plant Mol Biol 78:311–321

    CAS  PubMed  Article  Google Scholar 

  • Maresca M, Lin VG, Guo N, Yang Y (2013) Obligate ligation-gated recombination (ObLiGaRe): custom-designed nuclease-mediated targeted integration through non homologous end joining. Genome Res 23:539–546

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Marra MC, Piggott NE, Goodwin BK (2010) The anticipated value of SmartStax™ for US corn growers Ag. BioForum 13:1–12

    Google Scholar 

  • Matas AJ, Gapper NE, Chung MY, Giovannoni JJ, Rose JKC (2009) Biology and genetic engineering of fruit maturation for enhanced quality and shelf-life. Curr Opin Biotechnol 20:197–203

    CAS  PubMed  Article  Google Scholar 

  • Mehta A, Datta A (1991) Oxalate decarboxylase from Collybia velutipes: purification, characterization and cDNA cloning. J Biol Chem 266:23548–23553

    CAS  PubMed  Google Scholar 

  • Meli VS, Ghosh S, Prabha TN, Chakraborty N, Chakraborty S, Datta A (2010) Enhancement of fruit shelf life by suppressing N-glycan processing enzymes. Proc Natl Acad Sci USA 107:2413–2418

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Mlalazi B, Welsch R, Namanya P, Khanna H, Geijskes RJ, Harrison MD, Harding R, Dale JL, Bateson M (2012) Isolation and functional characterization of banana phytoene synthase genes as potential cisgenes. Planta. 236:1585–1598

    CAS  PubMed  Article  Google Scholar 

  • Moeller L, Wang K (2008) Engineering with precision: tools for the new generation of transgenic crops. Bioscience 58:391–401

    Article  Google Scholar 

  • Molesini B, Pii Y, Pandolfini T (2012) Fruit improvement using intragenesis and artificial microRNA. Trends Biotechnol 30:80–88

    CAS  PubMed  Article  Google Scholar 

  • Murai N, Kemp JD, 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

    CAS  PubMed  Article  Google Scholar 

  • Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31:691–693

    CAS  PubMed  Article  Google Scholar 

  • Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW, Yeh SD et al (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428

    CAS  PubMed  Article  Google Scholar 

  • O’Quinn PR, Nelssen JL, Goodband RD, Knabe DA, Woodworth JC, Tokach MD, Lohrmann TT (2000) Nutritional value of a genetically improved high-lysine, high-oil corn for young pigs. J Anim Sci 78:2144–2149

    PubMed  Article  Google Scholar 

  • Otang NV et al (2014) Transgenic tobacco lines expressing defective CMV replicase derived dsRNA are resistant to CMVO and CMVY. Mol Biotechnol 56:5063

    Google Scholar 

  • Ow DW (2005) Transgene management via multiple site-specific recombination systems. In Vitro Cell Dev Biol Plant 41:213–219

    CAS  Article  Google Scholar 

  • Ow DW (2007) GM maize from site-specific recombination technology, what next? Curr Opin Biotechnol 18:115–120

    CAS  PubMed  Article  Google Scholar 

  • Paques F, Duchateau P (2007) Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr Gene Therapy 7:49–66

    CAS  Article  Google Scholar 

  • Peiró A et al (2014) The movement protein (NSm) of Tomato spotted wilt virus is the a virulence determinant in the tomato Sw5 gene based resistance. Mol Plant Pathol 15:802813

    Article  CAS  Google Scholar 

  • Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S et al (2014) RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 13:578–589

    PubMed  Article  CAS  Google Scholar 

  • Priem B, Gross KC (1992) Mannosyl and xylosyl-containing glycans promote tomato (Lycopersicon esculentum, Mill.) fruit ripening. Plant Physiol 98:399–401

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Priem B, Gitti R, Bush CA, Gross KC (1993) Structure of ten free N-glycans in ripening tomato fruit (arabinose is a constituent of a plant N-glycan). Plant Physiol 102:445–458

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • PriyaSethu KM, Prabha TN (1997) α-D-Mannosidase from Capsicum annuum. Phytochemistry 44:383–387

    CAS  Article  Google Scholar 

  • Qi Y, Li X, Zhang Y, Starker CG, Baltes NJ et al (2013) Targeted deletion and inversion of tandemly arrayed genes in Arabidopsis thaliana using zinc finger nucleases. G3 Genes Genom Genet 3:1707–1715

    Google Scholar 

  • Qu J, Ye J, Fang R (2007) Artificial micro RNA mediated virus resistance in plants. J Virol 81:6690–6699

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004) Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnol J 2:477–486

    CAS  PubMed  Article  Google Scholar 

  • Que Q, Chilton MD, de Fontes CM, He C, Nuccio M, Zhu T et al (2010) Trait stacking in transgenic crops: challenges and opportunities. GM Crops. 1(4):220–229

    PubMed  Article  Google Scholar 

  • Quesada MA, Blanco-Portales R, Pose S, Garcia-Gago JA, Jimenez-Bermudez S, Munoz-Serrano A, Caballero JL, Pliego-Alfaro F, Mercado JA, Munoz-Blanco J (2009) Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiol 150:1022–1032

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Rai MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection—an overview of the recent progress. Environ Exp Bot 71:89–98

    Article  Google Scholar 

  • Raina A, Datta A (1992) Molecular cloning of a gene encoding a seed-specific protein with nutritionally balanced amino acid composition from Amaranthus. Proc Natl Acad Sci USA 89:11774–11778

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Raymond PJ, McFarlane I, Hartley Phipps R, Ceddia G (2011) The role of transgenic crops in sustainable development. Plant Biotechnol J 9:2–21

    Article  Google Scholar 

  • Rommens CM, Haring MA, Swords K, Davies HV, Belknap WR (2007) The intragenic approach as a new extension of traditional plant breeding. Trends Plant Sci 12:397–403

    CAS  PubMed  Article  Google Scholar 

  • Rommens CM, Yan H, Swords K, Richael C, Ye J (2008) Low acrylamide French fries and potato chips. Plant Biotechnol J 6:843–853

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Russell S, Hoopes J, Odell J (1992) Directed excision of a transgene from the plant genome. Mol Gen Genet 223:369–378

    Google Scholar 

  • Sanahuja G, Banakar R, Twyman R, Capell T, Christou P (2011) Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol J 9:283–300

    CAS  PubMed  Article  Google Scholar 

  • Sasaki K, Iwai T, Hiraga S, Kuroda K, Seo S, Mitsuhara I et al (2004) Ten rice peroxidases redundantly respond to multiple stresses including infection with rice blast fungus. Plant Cell Physiol 45:1442–1452

    CAS  PubMed  Article  Google Scholar 

  • Schaffer RJ, Ireland HS, Ross JJ, Ling TJ, David KM (2013) SEPALLATA1/2-suppressed mature apples have low ethylene, high auxin and reduced transcription of ripening-related genes. AoB Plants 5:pls047

    PubMed  Article  CAS  Google Scholar 

  • Schouten HJ, Jacobsen E (2008) Cisgenesis and intragenesis, sisters in innovative plant breeding. Trends Plant Sci 13:260–261

    CAS  PubMed  Article  Google Scholar 

  • Schouten HJ, Krens FA, Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants. EMBO Rep 7:750–753

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Seo JS, Sohn HB, Noh K et al (2012) Expression of the Arabidopsis AtMYB44 gene confers drought/salt-stress tolerance in transgenic soybean. Mol Breed 29:601–608

    CAS  Article  Google Scholar 

  • Shadle GL, Wesley SV, Korth KL, Chen F, Lamb C, Dixon RA (2003) Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of l-phenylalanine ammonia-lyase. Phytochemistry 64:153–161

    CAS  PubMed  Article  Google Scholar 

  • Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688

    CAS  PubMed  Article  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    CAS  PubMed  Article  Google Scholar 

  • Singh A, Taneja J, Dasgupta I, Mukherjee SK (2015) Development of plants resistant to tomato geminiviruses using artificial trans-acting small interfering RNA. Mol Plant Pathol 16:724–734

    CAS  PubMed  Article  Google Scholar 

  • Singla-Pareek SL, Reddy MK, Sopory SK (2003) Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. Proc Natl Acad Sci USA 100:14672–14677

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Smith NA, Singh SP, Wang MB, Stoutjesdijk PA, Green AG, Waterhouse PM (2000) Total silencing by intron-spliced hairpin RNAs. Nature 407:319–320

    CAS  PubMed  Article  Google Scholar 

  • Smith J, Grizot S, Arnould S, Duclert A, Epinat JC et al (2006) A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Res 34:e149

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Song D, Chen J, Song F, Zheng Z (2006) A novel rice MAPK gene, OsBIMK2, is involved in disease-resistance responses. Plant Biol 8:587–596

    CAS  PubMed  Article  Google Scholar 

  • Srivastava V, Anderson OD, Ow DW (1999) Single-copy transgenic wheat generated through the resolution of complex integration patterns. Proc Natl Acad Sci USA 96:11117–11121

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sunilkumar G et al (2006) Engineering cottonseed for use in human nutrition by tissue-specific reduction of toxic gossypol. Proc Natl Acad Sci USA 103:18054–18059

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521

    CAS  PubMed  Article  Google Scholar 

  • Tada Y, Nakase M, Adachi T, Nakamura R, Shimada H, Takahashi M, Fujimura T, Matsuda T (1996) Reduction of 14-16 kDa allergenic proteins in transgenic rice plants by antisense gene. FEBS Lett 391:341–345

    CAS  PubMed  Article  Google Scholar 

  • Takahashi Y, Bin Nasir KH, Ito A, Kanzaki H, Matsumura H, Saitoh H (2007) A high-throughput screen of cell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1- induced cell death signaling and non-host resistance to Pseudomonas cichorii. Plant J 49:1030–1040

    CAS  PubMed  Article  Google Scholar 

  • Thamizhmani R, Vijayachari P (2014) Association of dengue virus infection susceptibility with polymorphisms of 2′5′ oligoadenylate synthetase genes: a case–control study. Braz J Infect Dis 18:548550

    Article  Google Scholar 

  • Tran LS, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1:32–39

    PubMed  Article  Google Scholar 

  • Tuteja N, Sahoo RK, Garg B, Tuteja R (2013) OsSUV3 dual Helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. IR64). Plant J 76:115–127

    CAS  PubMed  Google Scholar 

  • Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122

    CAS  PubMed  Article  Google Scholar 

  • Uozumi N, Schroeder JI (2010) Ion channels and plant stress: past, present and future. In: Demidchik V, Maathuis F (eds) Ion channels and plant stress responses, signaling and communication in plants. Springer, Berlin Heidelberg, pp 1–22

    Chapter  Google Scholar 

  • Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-guided genome editing for target gene mutations in wheat. G3 (Bethesda) 3:2233–2238

    CAS  Article  Google Scholar 

  • Ursin VA (2003) Modification of plant lipids for human health: development of functional land-based omega-3 fatty acids. Symposium: improving human nutrition through genomics, proteomics and biotechnologies. American Society for Nutritional Sciences, Bethesda, pp 4271–4274

    Google Scholar 

  • Vanblaere T, Szankowski I, Schaart J, Schouten H, Flachowsky H, Broggini GAL, Gessler C (2011) The development of a cisgenic apple plant. J Biotechnol 154:304–311

    CAS  PubMed  Article  Google Scholar 

  • Varshney RK, Bansal KC, Aggarwal PK, Datta SK, Craufurd PQ (2011) Agricultural biotechnology for crop improvement in a variable climate: hope or hype? Trends Plant Sci 16:363–371

    CAS  PubMed  Article  Google Scholar 

  • Wally O, Punja ZK (2010) Genetic engineering for increasing fungal and bacterial disease resistance in crop plants. GM Crops 1:199–206

    PubMed  Article  Google Scholar 

  • Wang Y, Chen B, Hu Y, Li J, Lin Z (2005) Inducible excision of selectable marker gene from transgenic plants by the cre/lox site specific recombination system. Transgenic Res 14:605–614

    CAS  PubMed  Article  Google Scholar 

  • Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951

    CAS  PubMed  Article  Google Scholar 

  • Way HM, Kazan K, Mitter N, Goulter KC, Birch RG, Manners JM (2002) Constitutive expression of a phenylalanine ammonia-lyase gene from Stylosanthes humilis in transgenic tobacco leads to enhanced disease resistance but impaired plant growth. Physiol Mol Plant Pathol 60:275–282

    CAS  Article  Google Scholar 

  • Weeks JT, Ye J, Rommens CM (2008) Development of an in planta method for transformation of alfalfa (Medicago sativa). Transgenic Res 17:587–597

    CAS  PubMed  Article  Google Scholar 

  • Wendt T et al (2013) TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol 83:279–285

    CAS  PubMed  Article  Google Scholar 

  • Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115

    CAS  PubMed  Article  Google Scholar 

  • Whitham S, Mccormick S, Baker B (1996) The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato (hypersensitive response/plant disease resistance. Proc Natl Acad Sci USA 93:8776–8781

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Woo HJ, Cho HS, Lim SH, Shin KS, Lee SM, Lee KJ, Kim DH, Cho YG (2009) Auto-excision of selectable marker genes from transgenic tobacco via a stress inducible FLP/FRT site-specific recombination system. Transgenic Res. 18:455–465

    CAS  PubMed  Article  Google Scholar 

  • Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep 28:21–30

    CAS  PubMed  Article  Google Scholar 

  • Wyman C, Kanaar R (2006) DNA double-strand break repair: all’s well that ends well. Annu Rev Genet 40:363–383

    CAS  PubMed  Article  Google Scholar 

  • Xie K, Yang Y (2013) RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant 6:1975–1983

    CAS  PubMed  Article  Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho T-HD, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SM, Gao MQ, Xu CW, Gao JC, Deshpande S, Lin SP et al (2008) Alfalfa benefits from Medicago truncatula: the RCT1 gene from M. truncatula confers broad spectrum resistance to anthracnose in alfalfa. Proc Natl Acad Sci USA 105:12164–12169

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Ye X, Al-Babili S, Kloti 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

    CAS  PubMed  Article  Google Scholar 

  • Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A et al (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–771

    CAS  PubMed  Article  Google Scholar 

  • Zhang W, Subbarao S, Addae P, Shen A, Armstrong C, Peschke V, Gilbertson L (2003) Cre/lox-mediated marker gene excision in transgenic maize (Zea mays L.) plants. Theor Appl Genet 107:1157–1168

    CAS  PubMed  Article  Google Scholar 

  • Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135:615–621

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhang P, Vanderschuren H, Futterer J, Gruissem W (2005) Resistance to cassava mosaic disease in transgenic cassava expressing antisense RNAs targeting virus replication genes. Plant Biotechnol J 3:385397

    Article  CAS  Google Scholar 

  • Zhang Y, Li H, Ouyang B, Lu Y, Ye Z (2006) Chemical-induced autoexcision of selectable markers in elite tomato plants transformed with a gene conferring resistance to lepidopteran insects. Biotechnol Lett 28:1247–1253

    CAS  PubMed  Article  Google Scholar 

  • Zhang F et al (2010) High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci USA 107:12028–12033

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhang H et al (2014) The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J 12:797–807

    CAS  PubMed  Article  Google Scholar 

  • Zhao BY, Lin XH, Poland J, Trick H, Leach J, Hulbert S (2005) A maize resistance gene functions against bacterial streak disease in rice. Proc Natl Acad Sci USA 102:15383–15388

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhou YL, Xu JL, Zhou SC, Yu J, Xie XW, Xu MR et al (2009) Pyramiding Xa23 and Rxo1 for resistance to two bacterial diseases into an elite indica rice variety using molecular approaches. Mol Breed 23:279–287

    CAS  Article  Google Scholar 

  • Zhu Q, Maher EA, Masoud S, Dixon RA, Lamb CJ (1994) Enhanced protection against fungal attack by constitutive coexpression of chitinase and glucanase genes in transgenic tobacco Bio Technol 12:807–812

    CAS  Google Scholar 

  • Zrachya A, Kumar PP, Ramakrishnan U, Levy Y, Loyter A, Arazi T, Lapidot M, Gafni Y (2006) Production of siRNA targeted against TYLCV coat protein transcripts leads to silencing of its expression and resistance to the virus. Transgenic Res 16:385–398

    PubMed  Article  CAS  Google Scholar 

  • Zuo J, Niu QW, Moller SG, Chua NH (2001) Chemical-regulated, site-specific DNA excision in transgenic plants. Nat Biotechnol 19:157–161

    CAS  PubMed  Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Asis Datta.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Communicated by R. K. Varshney.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kamthan, A., Chaudhuri, A., Kamthan, M. et al. Genetically modified (GM) crops: milestones and new advances in crop improvement. Theor Appl Genet 129, 1639–1655 (2016). https://doi.org/10.1007/s00122-016-2747-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-016-2747-6

Keywords

  • Genetically Modify
  • Genetically Modify Crop
  • Genome Editing
  • Climacteric Fruit
  • Pokeweed Antiviral Protein