Abstract
Steady increase in global population poses several challenges to plant science research, including demand for increased crop productivity, grain yield, nutritional quality and improved tolerance to different environmental factors. Transgene-based approaches are promising to address these challenges by transferring potential candidate genes to host organisms through different strategies. Agrobacterium-mediated gene transfer is one such strategy which is well known for enabling efficient gene transfer in both monocot and dicots. Due to its versatility, this technique underwent several advancements including development of improved in vitro plant regeneration system, co-cultivation and selection methods, and use of hyper-virulent strains of Agrobacterium tumefaciens harbouring super-binary vectors. The efficiency of this method has also been enhanced by the use of acetosyringone to induce the activity of vir genes, silver nitrate to reduce the Agrobacterium-induced necrosis and cysteine to avoid callus browning during co-cultivation. In the last two decades, extensive efforts have been invested towards achieving efficient Agrobacterium-mediated transformation in cereals. Though high-efficiency transformation systems have been developed for rice and maize, comparatively lesser progress has been reported in other graminaceous crops. In this context, the present review discusses the progress made in Agrobacterium-mediated transformation system in rice, maize, wheat, barley, sorghum, sugarcane, Brachypodium, millets, bioenergy and forage and turf grasses. In addition, it also provides an overview of the genes that have been recently transferred to these graminaceous crops using Agrobacterium, bottlenecks in this technique and future possibilities for crop improvement.
Similar content being viewed by others
References
Alam MM, Tanaka T, Nakamura H, Ichikawa H, Kobayashi K, Yaeno T, Yamaoka N, Shimomoto K, Takayama K, Nishina H, Nishiguchi M (2014) Overexpression of a rice heme activator protein gene (OsHAP2E) confers resistance to pathogens, salinity and drought, and increases photosynthesis and tiller number. Plant Biotechnol J 13:85–96
Altpeter F, Vasil V, Srivastava V, Stöger E, Vasil IK (1996) Accelerated production of transgenic wheat (Triticum aestivum L.) plants. Plant Cell Rep 16:12–17
Altpeter F, Fang YD, Xu J, Ma X (2004) Comparison of transgene expression stability after Agrobacterium-mediated or biolistic gene transfer into perennial ryegrass (Lolium perenne L.). In: Hopkins A, Wang ZY, Mian R, Sledge M, Barker RE (eds) Molecular breeding of forage and turf. Kluwer Academic Publishers, Dordrecht, pp 255–260
Alves SC, Worland B, Thole V, Snape JW, Bevan MW, Vain P (2009) A protocol for Agrobacterium-mediated transformation of Brachypodium distachyon community standard line Bd21. Nat Protoc 4:638–649
Andrieu A, Breitler JC, Siré C, Meynard D, Gantet P, Guiderdoni E (2012) An in planta, Agrobacterium-mediated transient gene expression method for inducing gene silencing in rice (Oryza sativa L.). Leaves Rice (N Y) 5:23
Anjaneyulu E, Reddy PS, Sunita MS, Kishor PB, Meriga B (2014) Salt tolerance and activity of antioxidative enzymes of transgenic finger millet overexpressing a vacuolar H+-pyrophosphatase gene (SbVPPase) from Sorghum bicolor. J Plant Physiol 171:789–798
Arencibia AD, Carmona ER, Tellezs P, Chan MT, Yu SM (1998) An efficient protocol for sugarcane (Saccharum spp. L.) transformation mediated by Agrobacterium tumefaciens. Trans Res 7:213–222
Arvinth S, Arun S, Selvakesavan RK, Srikanth J, Mukunthan N, Ananda Kumar P, Premachandran MN, Subramonian N (2010) Genetic transformation and pyramiding of aprotinin-expressing sugarcane with cry1Ab for shoot borer (Chilo infuscatellus) resistance. Plant Cell Rep 229:383–395
Augustine SM, Narayan JA, Syamaladevi DP, Appunu C, Chakravarthi M, Ravichandran V, Subramonian N (2015) Erianthus arundinaceus HSP70 (EaHSP70) overexpression increases drought and salinity tolerance in sugarcane (Saccharum spp. hybrid). Plant Sci 232:23–34
Bajaj S, Ran Y, Phillips J, Kularajathevan G, Pal S, Cohen D, Elborough K, Puthigae S (2006) A high throughput Agrobacterium tumefaciens-mediated transformation method for functional genomics of perennial ryegrass (Lolium perenne L.). Plant Cell Rep 25:651–659
Bartlett JG, Alves SC, Smedley M, Snape JW, Harwood WA (2008) High-throughput Agrobacterium-mediated barley transformation. Plant Methods 4:22
Bettany AJ, Dalton SJ, Timms E, Manderyck B, Dhanoa MS, Morris P (2003) Agrobacterium tumefaciens-mediated transformation of Festuca arundinacea (Schreb.) and Lolium multiflorum (Lam.). Plant Cell Rep 21:437–444
Bower R, Birch RG (1992) Transgenic sugarcane plants via microprojectile bombardment. Plant J 2:409–416
Campo S, Baldrich P, Messeguer J, Lalanne E, Coca M, San Segundo B (2014) Overexpression of a calcium-dependent protein kinase confers salt and drought tolerance in rice by preventing membrane lipid peroxidation. Plant Physiol 165:688–704
Cao M, Sato SJ, Behrens M, Jiang WZ, Clemente TE, Weeks DP (2011) Genetic engineering of maize (Zea mays) for high-level tolerance to treatment with the herbicide dicamba. J Agric Food Chem 59:5830–5834
Casas AM, Kononowicz AK, Zehr UB, Tomes DT, Axtell JD, Butler LG, Bressan RA, Hasegawa PM (1993) Transgenic sorghum plants via microprojectile bombardment. Proc Natl Acad Sci 90:11212–11216
Castillo AM, Vasil V, Vasil IK (1994) Rapid production of fertile transgenic plants of rye (Secale cereale L.). Nature Biotechnol 12:1366–1371
Ceasar SA, Ignacimuthu S (2011) Agrobacterium-mediated transformation of finger millet (Eleusine coracana (L.) Gaertn.) using shoot apex explants. Plant Cell Rep 30:1759–1770
Chai ML, Senthil KK, Kim DH (2004) Transgenic plants of colonial bentgrass from embryogenic callus via Agrobacterium-mediated transformation. Plant Cell Tiss Organ Cult 77:165–171
Chan MT, Chang HH, Ho SL, Tong WF, Yu SM (1993) Agrobacterium-mediated production of transgenic rice plants expressing a chimeric alpha amylase promoter/beta-glucuronidase gene. Plant Mol Biol 22:491–506
Chauhan H, Khurana P (2011) Use of doubled haploid technology for development of stable drought tolerant bread wheat (Triticum aestivum L.) transgenics. Plant Biotechnol J 9:408–17
Chen Y, Fan X, Song W, Zhang Y, Xu G (2012a) Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnol J 10:139–149
Chen Z, Pan Y, Wang S, Ding Y, Yang W, Zhu C (2012b) Overexpression of a protein disulfide isomerase-like protein from Methanothermobacter thermoautotrophicum enhances mercury tolerance in transgenic rice. Plant Sci 197:10–20
Chen L, Cong Y, He H, Yu Y (2014a) Maize (Zea mays L.) transformation by Agrobacterium tumefaciens infection of pollinated ovules. J Biotechnol 171:8–16
Chen M, Zhao Y, Zhuo C, Lu S, Guo Z (2014b) Overexpression of a NF-YC transcription factor from bermudagrass confers tolerance to drought and salinity in transgenic rice. Plant Biotechnol J. doi:10.1111/pbi.12270
Cheng M, Fry JE, Pang S, Zhou H, Hironaka CM, Duncan DR, Conner TW, Wan Y (1997) Genetic transformation of wheat mediated by Agrobacterium tumefaciens. Plant Physiol 115:971–980
Cheng M, Hu T, Layton J, Liu CN, Fry JE (2003) Desiccation of plant tissues post-Agrobacterium infection enhances T-DNA delivery and increases stable transformation efficiency in wheat. In Vitro Cell Dev Biol-Plant 39:595–604
Cho MJ, Wu E, Kwan J, Yu M, Banh J, Linn W, Anand A, Li Z, TeRonde S, Register JC 3rd, Jones TJ, Zhao ZY (2014) Agrobacterium-mediated high-frequency transformation of an elite commercial maize (Zea mays L.) inbred line. Plant Cell Rep 33:1767–1777
Christou P, Ford TL, Kofron M (1991) Production of transgenic rice (Oryza sativa L.) plants from agronomically important indica and japonica varieties via electric discharge particle acceleration of exogenous DNA into immature zygotic embryos. Bio Technol 9:957–962
Dai S, Zheng P, Marmey P, Zhang S, Tian W, Chen S, Beachy RN, Fauquet C (2001) Comparative analysis of transgenic rice plants obtained by Agrobacterium-mediated transformation and particle bombardment. Mol Breed 7:25–33
Dansana PK, Kothari KS, Vij S, Tyagi AK (2014) OsiSAP1 overexpression improves water-deficit stress tolerance in transgenic rice by affecting expression of endogenous stress-related genes. Plant Cell Rep 33:1425–1440
Datta K, Baisakh N, Ganguly M, Krishnan S, Yamaguchi Shinozaki K, 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
Dong S, Qu R (2005) High efficiency transformation of tall fescue with Agrobacterium tumefaciens. Plant Sci 168:1453–1458
Dong J, Teng WM, Buchholz WG, Hall TC (1996) Agrobacterium-mediated transformation of Javanica rice. Mol Breed 2:267–276
Dong Z, Zhao H, He J, Huai J, Lin H, Zheng J, Liu Y, Wang G (2011) Overexpression of a foxtail millet Acetyl-CoA carboxylase gene in maize increases sethoxydim resistance and oil content. African J Biotechnol 10:3986–3995
Draper J, Mur LAJ, Jenkins G, Ghosh-Biswas GC, Bablak P, Hasterok R, Routledge AP (2001) Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol 127:1539–1555
Enriquez, GA, Trujillo LE, Menendez C, Vazquez RI, Tiel K, Dafhnis F, Arrieta J, Selman G, Hernandez L (2000) Sugarcane (Saccharum hybrid) genetic transformation mediated by Agrobacterium tumefaciens: production of transgenic plants expressing proteins with agronomic and industrial value. Proc Int Symp on ‘Plant genetic engineering: towards the third millennium’, Havana, Cuba
Fan X, Xie D, Chen J, Lu H, Xu Y, Ma C, Xu G (2014) Over-expression of OsPTR6 in rice increased plant growth at different nitrogen supplies but decreased nitrogen use efficiency at high ammonium supply. Plant Sci 227:1–11
Fromm ME, Morrish F, Armstrong C, Williams R, Thomas J, Klein TM (1990) Inheritance and expression of chimeric genes in the progeny of transgenic maize plants. Biotechnology (N Y) 8:833–839
Fu C, Mielenz JR, Xiao X, Ge Y, Hamilton CY, Rodriguez M Jr, Chen F, Foston M, Ragauskas A, Bouton J, Dixon RA, Wang ZY (2011) Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc Natl Acad Sci U S A 108:3803–3808
Fu C, Sunkar R, Zhou C, Shen H, Zhang JY, Matts J, Wolf J, Mann DG, Stewart CN Jr, Tang Y, Wang ZY (2012) Overexpression of miR156 in switchgrass (Panicum virgatum L.) results in various morphological alterations and leads to improved biomass production. Plant Biotechnol J 10:443–452
Gao Z, Jayaraj J, Muthukrishnan S, Claflin L, Liang GH (2005a) Efficient genetic transformation of Sorghum using a visual screening marker. Genome 48:321–333
Gao Z, Xie X, Ling Y, Muthukrishnan S, Liang GH (2005b) Agrobacterium tumefaciens-mediated sorghum transformation using a mannose selection system. Plant Biotechnol J 3:591–599
Gill SS, Tajrishi M, Madan M, Tuteja N (2013) A DESD-box helicase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. PB1). Plant Mol Biol 82:1–22
Girgi M, O’Kennedy MM, Morgenstern A, Mayer G, Lorz H, Oldach KH (2002) Transgenic and herbicide resistant pearl millet (Pennisetum glaucum L.) R. Br. via microprojectile bombardment of scutellar tissue. Mol Breed 10:243–252
Goldman JJ, Hanna WW, Fleming G, Ozias-Akins P (2003) Fertile transgenic pearl millet [Pennisetum glaucum (L.) R. Br.] plants recovered through microprojectile bombardment and phosphinothricin selection of apical meristem-, inflorescence-, and immature embryo-derived embryogenic tissues. Plant Cell Rep 21:999–1009
Gordon-Kamm WJ, Spencer TM, Mangano ML, Adams TR, Daines RJ, Start WG, O'Brien JV, Chambers SA, Adams WR Jr, Willetts NG, Rice TB, Mackey CJ, Krueger RW, Kausch AP, Lemaux PG (1990) Transformation of maize cells and regeneration of fertile transgenic plants. Plant Cell 2:603–618
Gupta P, Raghuvanshi S, Tyagi AK (2001) Assessment of the efficiency of various gene promoters via biolistics in leaf and regenerating seed callus of millets, Eleusine coracana and Echinochloa crusgalli. Plant Biotechnol 18:275–282
Gurel S, Gurel E, Kaur R, Wong J, Meng L, Tan HQ, Lemaux PG (2009) Efficient, reproducible Agrobacterium-mediated transformation of sorghum using heat treatment of immature embryos. Plant Cell Rep 28:429–444
Han N, Chen D, Bian HW, Deng MJ, Zhu MY (2005) Production of transgenic creeping bentgrass Agrostis stolonifera var. palustris plants by Agrobacterium tumefaciens-mediated transformation using hygromycin selection. Plant Cell Tiss Organ Cult 81:131–138
Han J, Lakshman DK, Galvez LC, Mitra S, Baenziger PS, Mitra A (2012a) Transgenic expression of lactoferrin imparts enhanced resistance to head blight of wheat caused by Fusarium graminearum. BMC Plant Biol 12:33
Han YJ, Cho KC, Hwang OJ, Choi YS, Shin AY, Hwang I, Kim JI (2012b) Overexpression of an Arabidopsis β-glucosidase gene enhances drought resistance with dwarf phenotype in creeping bentgrass. Plant Cell Rep 31:1677–1686
He Y, Jones HD, Chen S, Chen XM, Wang DW, Li KX, Wang DS, Xia LQ (2010) Agrobacterium-mediated transformation of durum wheat (Triticum turgidum L. var. durum cv Stewart) with improved efficiency. J Exp Bot 61:1567–1581
Hema R, Vemanna RS, Sreeramulu S, Reddy CP, Senthil-Kumar M, Udayakumar M (2014) Stable expression of mtlD gene imparts multiple stress tolerance in finger millet. PLoS ONE 9, e99110
Hensel G, Valkov V, Middlefell-Williams J, Kumlehn J (2008) Efficient generation of transgenic barley: the way forward to modulate plant-microbe interactions. J Plant Physiol 165:71–82
Hiei Y, Komari T (2008) Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat Protoc 3:824–834
Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the DNA. Plant J 6:271–282
Holme IB, Brinch-Pedersen H, Lange M, Holm PB (2006) Transformation of barley (Hordeum vulgare L.) by Agrobacterium tumefaciens infection of in vitro cultured ovules. Plant Cell Rep 25:1325–1335
Hu F, Zhang L, Wang X, Ding J, Wu D (2005) Agrobacterium-mediated transformed transgenic triploid bermudagrass (Cynodon dactylon x C. transvaalensis) plants are highly resistant to the glufosinate herbicide Liberty. Plant Cell Tiss Organ Cult 83:13–19
Ignacimuthu S, Ceasar SA (2012) Development of transgenic finger millet (Eleusine coracana (L.) Gaertn.) resistant to leaf blast disease. J Biosci 37:135–147
Ignacimuthu S, Premkumar A (2014) Development of transgenic Sorghum bicolor (L.) Moench resistant to the Chilo partellus (Swinhoe) through Agrobacterium-mediated transformation. Mol Biol Genet Eng. doi:10.7243/2053-5767-2-1
Ishida Y, Saito H, Ohta S, Hiei Y, Komari T, Kumashiro T (1996) High efficiency transformation of maize (Zea mays L.) mediated by Agrobacterium tumefaciens. Nat Biotechnol 14:745–750
Ishida Y, Hiei Y, Komari T (2007) Agrobacterium-mediated transformation of maize. Nat Protoc 2:1614–1621
Ishida Y, Tsunashima M, Hiei Y, Komari T (2015) Wheat (Triticum aestivum L.) transformation using immature embryos. Methods Mol Biol 1223:189–198
Jeknić Z, Pillman KA, Dhillon T, Skinner JS, Veisz O, Cuesta-Marcos A, Hayes PM, Jacobs AK, Chen TH, Stockinger EJ (2014) Hv-CBF2A overexpression in barley accelerates COR gene transcript accumulation and acquisition of freezing tolerance during cold acclimation. Plant Mol Biol 84:67–82
Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197
Jha P, Shashi, Rustagi A, Agnihotri P, Kulkarni V, Bhat V (2011) Efficient Agrobacterium-mediated transformation of Pennisetum glaucum (L.) R. Br. using shoot apices as explant source. Plant Cell Tiss Organ Cult 107:501–512
Ji Q, Xu X, Wang K (2013) Genetic transformation of major cereal crops. Int J Dev Biol 57:495–508
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
Joyce P, Hermann S, O'Connell A, Dinh Q, Shumbe L, Lakshmanan P (2014) Field performance of transgenic sugarcane produced using Agrobacterium and biolistics methods. Plant Biotechnol J 12:411–424
Jung JH, Fouad WM, Vermerris W, Gallo M, Altpeter F (2012) RNAi suppression of lignin biosynthesis in sugarcane reduces recalcitrance for biofuel production from lignocellulosic biomass. Plant Biotechnol J 10:1067–1076
Jung JH, Vermerris W, Gallo M, Fedenko JR, Erickson JE, Altpeter F (2013) RNA interference suppression of lignin biosynthesis increases fermentable sugar yields for biofuel production from field-grown sugarcane. Plant Biotechnol J 11:709–716
Kang G, Liu G, Peng X, Wei L, Wang C, Zhu Y, Ma Y, Jiang Y, Guo T (2013) Increasing the starch content and grain weight of common wheat by overexpression of the cytosolic AGPase large subunit gene. Plant Physiol Biochem 73:93–98
Karthikeyan A, Pandian SK, Ramesh M (2011) Agrobacterium-mediated transformation of leaf base derived callus tissues of popular indica rice (Oryza sativa L. sub sp. indica cv. ADT 43). Plant Sci 181:258–268
Karthikeyan A, Shilpha J, Pandian SK, Ramesh M (2012) Agrobacterium-mediated transformation of indica rice cv. ADT 43. Plant Cell Tiss Organ Cult 109:153–165
Khanna HK, Daggard GE (2003) Agrobacterium tumefaciens-mediated transformation of wheat using a superbinary vector and a polyamine-supplemented regeneration medium. Plant Cell Rep 21:429–436
Kim KH, Alam I, Kim YG, Sharmin SA, Lee KW, Lee SH, Lee BH (2012) Overexpression of a chloroplast-localized small heat shock protein OsHSP26 confers enhanced tolerance against oxidative and heat stresses in tall fescue. Biotechnol Lett 34:371–377
Kole C, Muthamilarasan M, Henry R, Edwards D, Sharma R, Abberton M, Batley J, Bentley A, Blakeney M, Bryant J, Cai H, Cakir M, Cseke LJ, Cockram J, de Oliveira AC, De Pace C, Dempewolf H, Ellison S, Gepts P, Greenland A, Hall A, Hori K, Hughes S, Humphreys MW, Iorizzo M, Ismail AM, Marshall A, Mayes S, Nguyen HT, Ogbonnaya FC, Ortiz R, Paterson AH, Simon PW, Tohme J, Tuberosa R, Valliyodan B, Varshney RK, Wullschleger SD, Yano M, Prasad M (2015) Application of genomics-assisted breeding for generation of climate resilient crops: progress and prospects. Front Plant Sci 6:563
Komari T, Hiei Y, Ishida Y, Kumashiro T, Kubo T (1998) Advances in cereal gene transfer. Curr Opin in Plant Biol 1:161–165
Kovalchuk N, Jia W, Eini O, Morran S, Pyvovarenko T, Fletcher S, Bazanova N, Harris J, Beck-Oldach K, Shavrukov Y, Langridge P, Lopato S (2013) Optimization of TaDREB3 gene expression in transgenic barley using cold-inducible promoters. Plant Biotechnol J 11:659–670
Kumar V, Campbell LM, Rathore KS (2011) Rapid recovery- and characterization of transformants following Agrobacterium-mediated T-DNA transfer to sorghum. Plant Cell Tiss Organ Cult 104:137–146
Kumar T, Uzma, Khan MR, Abbas Z, Ali GM (2014) Genetic improvement of sugarcane for drought and salinity stress tolerance using Arabidopsis vacuolar pyrophosphatase (AVP1) gene. Mol Biotechnol 56:199–209
Kumar K, Muthamilarasan M, Bonthala VS, Roy R, Prasad M (2015) Unraveling 14-3-3 proteins in C4 panicoids with emphasis on model plant Setaria italica reveals phosphorylation-dependent subcellular localization of RS splicing factor. PLoS ONE 10, e0123236
Kumlehn J, Serazetdinova L, Hensel G, Becker D, Loerz H (2006) Genetic transformation of barley (Hordeum vulgare L.) via infection of androgenetic pollen cultures with Agrobacterium tumefaciens. Plant Biotechnol J 4:251–261
Lambe P, Dinant M, Matagne RF (1995) Differential long-term expression and methylation of the hygromycin phosphotranspherase (hph) and (b-glucuronidase (gus) genes in transgenic Pearl-Millet (Pennisetum glaucum) callus. Plant Sci 108:51–62
Lata C, Gupta S, Prasad M (2013) Foxtail millet: a model crop for genetic and genomic studies in bioenergy grasses. Crit Rev Biotechnol 33:328–343
Lata C, Mishra AK, Muthamilarasan M, Bonthala VS, Khan Y, Prasad M (2014) Genome-wide investigation and expression profiling of AP2/ERF transcription factor superfamily in foxtail millet (Setaria italica L.). PLoS ONE 9, e113092
Lee KW, Choi GJ, Kim KY, Yoon SH, Ji HC, Park HS, Lim YC, Lee SH (2010) Genotypic variation of Agrobacterium-mediated transformation of Italian ryegrass. Electronic J Biotechnol 13:3
Lee KW, Choi GJ, Kim KY, Ji HJ, Park HS, Kim YG, Lee BH, Lee SH (2012) Transgenic expression of MsHsp23 confers enhanced tolerance to abiotic stresses in tall fescue. Asian-Australas J Anim Sci 25:818–823
Li Z, Baldwin CM, Hu Q, Liu H, Luo H (2010) Heterologous expression of Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass (Agrostis stolonifera L.). Plant Cell Environ 33:272–289
Li Z, Gao Q, Liu Y, He C, Zhang X, Zhang J (2011) Overexpression of transcription factor ZmPTF1 improves low phosphate tolerance of maize by regulating carbon metabolism and root growth. Planta 233:1129–1143
Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392
Li W, Shao M, Yang J, Zhong W, Okada K, Yamane H, Qian G, Liu F (2013) Oscyp71Z2 involves diterpenoid phytoalexin biosynthesis that contributes to bacterial blight resistance in rice. Plant Sci 207:98–107
Liu Y, Yu J, Zhao Q, Zhu D, Ao G (2005) Genetic transformation of millet (Setaria italica) by Agrobacterium. J Agric Biotechnol 13:32–37
Lu Y, Li Y, Zhang J, Xiao Y, Yue Y, Duan L, Zhang M, Li Z (2013) Overexpression of Arabidopsis molybdenum cofactor sulfurase gene confers drought tolerance in maize (Zea mays L.). PLoS ONE 8, e52126
Luo H, Hu Q, Nelson K, Longo C, Kausch AP, Chandlee JM, Wipff JK, Fricker CR (2004) Agrobacterium tumefaciens-mediated creeping bentgrass (Agrostis stolonifera L.) transformation using phosphinothricin selection results in a high frequency of single-copy transgene integration. Plant Cell Rep 22:645–652
Mallikarjuna G, Mallikarjuna K, Reddy MK, Kaul T (2011) Expression of OsDREB2A transcription factor confers enhanced dehydration and salt stress tolerance in rice (Oryza sativa L.). Biotechnol Lett 33:1689–1697
Mamontova EM, Velikov VA, Volokhina IV, Chumakov MI (2010) Agrobacterium-mediated in Planta transformation of maize germ cells. Genetika 46:568–571
Martins PK, Dias BBA, Ribeiro AP, Kobayashi AK, Molinari HBC (2014) Setaria viridis: a tool for functional gene analysis in sugarcane. In: International Setaria Genetics Conference, pp 19
Matthysse AG (2006) The genus Agrobacterium. Prokaryotes 5:91–114
Matusuoka M, Ideta O, Tanio M, Hayakawa A, Miwa H (2001) Agrobacterium tumefaciens mediated transformation using cell suspension culture with a novel method. Proc XXIV Congr of Int Society of Sugarcane Technologists, Brisbane, Australia 2:660–662
Mayavan S, Subramanyam K, Jaganath B, Sathish D, Manickavasagam M, Ganapathi A (2015) Agrobacterium-mediated in planta genetic transformation of sugarcane setts. Plant Cell Rep 34:1835–1848
Mishra AK, Muthamilarasan M, Khan Y, Parida SK, Prasad M (2014) Genome-wide investigation and expression analyses of WD40 protein family in the model plant foxtail millet (Setaria italica L.). PLoS ONE 9, e86852
Mrízová K, Jiskrová E, Vyroubalová Š, Novák O, Ohnoutková L, Pospíšilová H, Frébort I, Harwood WA, Galuszka P (2013) Overexpression of cytokinin dehydrogenase genes in barley (Hordeum vulgare cv. Golden Promise) fundamentally affects morphology and fertility. PLoS ONE 8, e79029
Muthamilarasan M, Prasad M (2015) Advances in Setaria genomics for genetic improvement of cereals and bioenergy grasses. Theor Appl Genet 128:1–14
Muthamilarasan M, Theriappan P, Prasad M (2013) Recent advances in crop genomics for ensuring food security. Curr Sci 105:155–158
Muthamilarasan M, Bonthala VS, Mishra AK, Khandelwal R, Khan Y, Prasad M (2014a) C2H2-type of zinc finger transcription factors in foxtail millet define response to abiotic stresses. Funct Integr Genomics 14:531–543
Muthamilarasan M, Khandelwal R, Yadav CB, Bonthala VS, Khan Y, Prasad M (2014b) Identification and molecular characterization of MYB transcription factor superfamily in C4 model plant foxtail millet (Setaria italica L.). PLoS ONE 9, e109920
Muthamilarasan M, Dhaka A, Yadav R, Prasad M (2015a) Exploration of millet models for developing nutrient rich graminaceous crops. Plant Sci. doi:10.1016/j.plantsci.2015.08.023
Muthamilarasan M, Bonthala V, Khandelwal R, Jaishankar J, Shweta S, Nawaz K, Prasad M (2015b) Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signalling. Front Plant Sci 6:910
Muthamilarasan M, Khan Y, Jaishankar J, Shweta S, Lata C, Prasad M (2015c) Integrative analysis and expression profiling of secondary cell wall genes in C4 biofuel model Setaria italica reveals targets for lignocellulose bioengineering. Front Plant Sci (In press)
Ncanana S, Brandt W, Lindsey G, Farrant J (2005) Development of plant regeneration and transformation protocols for the desiccation-sensitive weeping lovegrass Eragrostis curvula. Plant Cell Rep 24:335–340
Nguyen TV, Thu TT, Claeys M, Angenon G (2007) Agrobacterium-mediated transformation of sorghum (Sorghum bicolor (L.) Moench) using an improved in vitro regeneration system. Plant Cell Tiss Organ Cult 91:155–164
Ombori O, Muoma J, Machuka J (2013) Agrobacterium-mediated genetic transformation of selected tropical inbred and hybrid maize (Zea mays L.) lines. Plant Cell Tiss Organ Cult 113:11–23
Ozawa K, Takaiwa F (2010) Highly efficient Agrobacterium-mediated transformation of suspension-cultured cell clusters of rice (Oryza sativa L.). Plant Sci 179:333–337
Park SH, Pinson SR, Smith RH (1996) T-DNA integration into genomic DNA of rice following Agrobacterium inoculation of isolated shoot apices. Plant Mol Biol 32:1135–1148
Parrott DL, Anderson AJ, Carman JG (2002) Agrobacterium induces plant cell death in wheat (Triticum aestivum L.). Physiol Mol Plant Pathol 60:59–6
Pei L, Wang J, Li K, Li Y, Li B, Gao F, Yang A (2012) Overexpression of Thellungiella halophila H+-pyrophosphatase gene improves Low phosphate tolerance in maize. PLoS ONE 7, e43501
Popelka JC, Altpeter F (2003) Agrobacterium tumefaciens-mediated genetic transformation of rye (Secale cereale L.). Mol Breeding 11:203–211
Puranik S, Sahu PP, Mandal SN, Venkata Suresh B, Parida SK, Prasad M (2013) Comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in foxtail millet (Setaria italica L.). PLoS ONE 8, e64594
Ramadevi R, Rao KV, Reddy VD (2014) Agrobacterium tumefaciens-mediated genetic transformation and production of stable transgenic pearl millet (Pennisetum glaucum [L.] R. Br.). In Vitro Cell Dev Biol-Plant 50:392–400
Ramineni R, Sadumpati V, Khareedu VR, Vudem DR (2014) Transgenic pearl millet male fertility restorer line (ICMP451) and hybrid (ICMH451) expressing Brassica juncea Nonexpressor of pathogenesis related genes 1 (BjNPR1) exhibit resistance to downy mildew disease. PLoS ONE 6, e90839
Rashid H, Yokoi S, Toriyama K, Hinata K (1996) Transgenic plant production mediated by Agrobacterium in indica rice. Plant Cell Rep 15:727–730
Ravikumar G, Manimaran P, Voleti SR, Subrahmanyam D, Sundaram RM, Bansal KC, Viraktamath BC, Balachandran SM (2014) Stress-inducible expression of AtDREB1A transcription factor greatly improves drought stress tolerance in transgenic indica rice. Transgenic Res 23:421–439
Regina A, Bird A, Topping D, Bowden S, Freeman J, Barsby T, Kosar-Hashemi B, Li Z, Rahman S, Morell M (2006) High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. Proc Natl Acad Sci U S A 103:3546–551
Rice EA, Khandelwal A, Creelman RA, Griffith C, Ahrens JE, Taylor JP, Murphy LR, Manjunath S, Thompson RL, Lingard MJ, Back SL, Larue H, Brayton BR, Burek AJ, Tiwari S, Adam L, Morrell JA, Caldo RA, Huai Q, Kouadio JL, Kuehn R, Sant AM, Wingbermuehle WJ, Sala R, Foster M, Kinser JD, Mohanty R, Jiang D, Ziegler TE, Huang MG, Kuriakose SV, Skottke K, Repetti PP, Reuber TL, Ruff TG, Petracek ME, Loida PJ (2014) Expression of a truncated ATHB17 protein in maize increases ear weight at silking. PLoS ONE 9, e94238
Risacher T, Craze M, Bowden S, Paul W, Barsby T (2009) Highly efficient Agrobacterium-mediated transformation of wheat via in planta inoculation. Methods Mol Biol 478:115–24
Saathoff AJ, Sarath G, Chow EK, Dien BS, Tobias CM (2011) Downregulation of cinnamyl-alcohol dehydrogenase in switchgrass by RNA silencing results in enhanced glucose release after cellulase treatment. PLoS One 6, e16416
Sadumpati V, Kalambur M, Vudem DR, Kirti PB, Khareedu VR (2013) Transgenic indica rice lines, expressing Brassica juncea Nonexpressor of pathogenesis-related genes 1 (BjNPR1), exhibit enhanced resistance to major pathogens. J Biotechnol 166:114–121
Sah SK, Kaur A, Kaur G, Cheema GS (2014) Genetic transformation of rice: problems, progress and prospects. J Rice Res 3:132
Sahoo RK, Gill SS, Tuteja N (2012) Pea DNA helicase 45 promotes salinity stress tolerance in IR64 rice with improved yield. Plant Signal Behav 7:1042–1046
Sharma M, Kothari-Chajer A, Jagga-Chugh S, Kothari SL (2011) Factors influencing Agrobacterium tumefaciens-mediated genetic transformation of Eleusine coracana (L.) Gaertn. Plant Cell Tiss Organ Cult 105:93–104
Shaw DJ, Gray JC (2011) Visualisation of stromules in transgenic wheat expressing a plastid-targeted yellow fluorescent protein. Planta 233:961–970
She JM, Liang LF, Zhang BL, He XL, Chen ZY, Ni WC (2005) Acquirement of Bt transgenic plants by Agrobacterium tumefaciens in Kentucky bluegrass (Poa pratensis L.). Jiangsu J Agr Sci 21:102–105
Shrawat AK, Lörz H (2006) Agrobacterium-mediated transformation of cereals: a promising approach crossing barriers. Plant Biotechnol J 4:575–603
Sohn SI, Kim YH, Kim SL, Lee JY, Oh YJ, Chung JH, Lee KR (2014) Genistein production in rice seed via transformation with soybean IFS genes. Plant Sci 217–218:27–35
Somleva MN, Tomaszewski Z, Conger BV (2002) Agrobacterium-mediated genetic transformation of switchgrass. Crop Sci 42:2080–2087
Supartana P, Shimizu T, Shioiri H, Nogawa M, Nozue M, Kojima M (2005) Development of simple and efficient in planta transformation method for rice (Oryza sativa L.) using Agrobacterium tumefaciens. J Biosci Bioeng 100:391–397
Supartana P, Shimizu T, Nogawa M, Shioiri H, Nakajima T, Haramoto N, Nozue M, Kojima M (2006) Development of simple and efficient in Planta transformation method for wheat (Triticum aestivum L.) using Agrobacterium tumefaciens. J Biosci Bioeng 102:162–170
Targonska M, Hromada-Judycka A, Bolibok-Brągoszewska H, Rakoczy-Trojanowska M (2013) The specificity and genetic background of the rye (Secale cereale L.) tissue culture response. Plant Cell Rep 32:1–9
Taylor MG, Vasil IK (1991) Histology of, and physical factors affecting, transient GUS expression in pearl millet (Pennisetum glaucum (L.) R.Br.) embryos following microprojectile bombardment. Plant Cell Rep 10:120–125
Tingay S, McElroy D, Kalla R, Fieg S, Wang M, Thornton S, Brettell R (1997) Agrobacterium tumefaciens-mediated barley transformation. Plant J 11:1369–1376
Tiong J, McDonald GK, Genc Y, Pedas P, Hayes JE, Toubia J, Langridge P, Huang CY (2014) HvZIP7 mediates zinc accumulation in barley (Hordeum vulgare) at moderately high zinc supply. New Phytol 201:131–143
Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976
Toyama K, Bae CH, Kang JG, Lim YP, Adachi T, Riu KZ, Song PS, Lee HY (2003) Production of herbicide-tolerant zoysiagrass by Agrobacterium-mediated transformation. Mol Cells 16:19–27
Trabucco GM, Matos DA, Lee SJ, Saathoff AJ, Priest HD, Mockler TC, Sarath G, Hazen SP (2013) Functional characterization of cinnamyl alcohol dehydrogenase and caffeic acid O-methyltransferase in Brachypodium distachyon. BMC Biotechnol 13:61
Ueki J, Komari T, Imaseki H (2004) Enhancement of reporter-gene expression by insertion of two introns in maize and tobacco protoplasts. Plant Biotechnol 21:15–24
Vain P, Worland B, Thole V, McKenzie N, Alves SC, Opanowicz M, Fish LJ, Bevan MW, Snape JW (2008) Agrobacterium-mediated transformation of the temperate grass Brachypodium distachyon (genotype Bd21) for T-DNA insertional mutagenesis. Plant Biotechnol J 6:941
Vasil V, Castillo AM, Fromm ME, Vasil IK (1992) Herbicide resistant fertile transgenic wheat plants obtained by microprojectile bombardment of regenerable embryogenic callus. Biotechnol 10:667–674
Vogel J, Hill T (2008) High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep 27:471–478
Wan Y, Lemaux PG (1994) Generation of large numbers of independently transformed fertile barley plants. Plant Physiol 104:37–48
Wang ZY, Ge Y (2005) Agrobacterium-mediated high efficiency transformation of tall fescue (Festuca arundinacea). J Plant Physiol 162:103–113
Wang ZY, Ge Y (2006) Recent advances in genetic transformation of forage and turf grasses. In Vitro cell Dev Bio-Plant 42:1–18
Wang MZ, Pan YL, Li C, Liu C, Zhao Q, Ao GM, Yu JJ (2011) Culturing of immature inflorescences and Agrobacterium-mediated transformation of foxtail millet (Setaria italica). African J Biotechnol 10:16466–16479
Wang F, Wang Z, Zhu C (2012) Heteroexpression of the wheat phytochelatin synthase gene (TaPCS1) in rice enhances cadmium sensitivity. Acta Biochim Biophys Sin 44:886–893
Wei S, Hu W, Deng X, Zhang Y, Liu X, Zhao X, Luo Q, Jin Z, Li Y, Zhou S, Sun T, Wang L, Yang G, He G (2014) A rice calcium-dependent protein kinase OsCPK9 positively regulates drought stress tolerance and spikelet fertility. BMC Plant Biol 14:133
Weinthal D, Tovkach A, Zeevi V, Tzfira T (2010) Genome editing in plant cells by zinc finger nucleases. Trends Plant Sci 15:308–321
Weir B, Gu X, Wang MB, Upadhyaya N, Elliott AR, Brettell RIS (2001) Agrobacterium tumefaciens-mediated transformation of wheat using suspension cells as a model system and green fluorescent protein as a visual marker. Aust J Plant Physiol 28:807–818
Wu H, Sparks C, Amoah B, Jones HD (2003) Factors influencing successful Agrobacterium-mediated genetic transformation of wheat. Plant Cell Rep 21:659–668
Wu YY, Chen QJ, Chen M, Chen J, Wang XC (2005) Salt-tolerant transgenic perennial ryegrass (Lolium perenne L.) obtained by Agrobacterium tumefaciens-mediated transformation of the vacuolar Naþ/Hþ antiporter gene. Plant Sci 169:65–73
Wu E, Lenderts B, Glassman K, Berezowska-Kaniewska M, Christensen H, Asmus T, Zhen S, Chu U, Cho MJ, Zhao ZY (2014) Optimized Agrobacterium-mediated sorghum transformation protocol and molecular data of transgenic sorghum plants. In Vitro Cell Dev Biol-Plant 50:9–18
Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:327
Xu M, Li L, Fan Y, Wan J, Wang L (2011) ZmCBF3 overexpression improves tolerance to abiotic stress in transgenic rice (Oryza sativa) without yield penalty. Plant Cell Rep 30:1949–1957
Xu B, Sathitsuksanoh N, Tang Y, Udvardi MK, Zhang JY, Shen Z, Balota M, Harich K, Zhang PY, Zhao B (2012) Overexpression of AtLOV1 in Switchgrass alters plant architecture, lignin content, and flowering time. PLoS ONE 7, e47399
Xu R, Li H, Qin R, Wang L, Li L, Wei P, Yang J (2014) Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice 7:5
Yadav CB, Muthamilarasan M, Pandey G, Prasad M (2014) Identification, characterization and expression profiling of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in foxtail millet. Plant Mol Biol Rep. doi:10.1007/s11105-014-0736-y
Yang R, Zhou Y, Cao Y, Yin Z, Yang L, Li J (2013) The transformation of the photo-thermo sensitive genic male-sterile line 261S of rice via an expression vector containing the anti-Waxy gene. Breed Sci 63:147–153
Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305
Yellisetty V, Reddy LA, Mandapaka M (2015) In planta transformation of sorghum (Sorghum bicolor (L.) Moench) using TPS1 gene for enhancing tolerance to abiotic stresses. J Genet 94:425–434
Yu TT, Skinner DZ, Liang GH, Trick HN, Huang B, Muthukrishnan S (2000) Agrobacterium-mediated transformation of creeping bentgrass using GFP as a reporter gene. Hereditas 133:229–33
Zhang S, Cho MJ, Koprek T, Yun R, Bregitzer P, Lemaux PG (1999) Genetic transformation of commercial cultivars of oat (Avena sativa L.) and barley (Hordeum vulgare L.) using in vitro shoot meristematic cultures derived from germinated seedlings. Plant Cell Rep 18:959–966
Zhang K, Wang J, Hu X, Yang A, Zhang J (2010a) Agrobacterium -mediated transformation of shoot apices of Kentucky bluegrass (Poa pratensis L.) and production of transgenic plants carrying a betA gene. Plant Cell Tiss Organ Cult 102:135–143
Zhang S, Li N, Gao F, Yang A, Zhang J (2010b) Over-expression of TsCBF1 gene confers improved drought tolerance in transgenic maize. Mol Breed 26:455–465
Zhang Z, Li F, Li D, Zhang H, Huang R (2010c) Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232:765–774
Zhang J, Li J, Wang X, Chen J (2011) OVP1, a vacuolar Hþ-translocating inorganic pyrophosphatase (V-PPase), overexpression improved rice cold tolerance. Plant Physiol Biochem 49:33–38
Zhangsun D, Luo S, Chen R, Tang K (2007) Improved Agrobacterium-mediated genetic transformation of GNA transgenic sugarcane. Biologia 62:386–393
Zhao ZY, Cai T, Tagliani L, Miller M, Wang N, Pang H, Rudert M, Schroeder S, Hondred D, Seltzer J, Pierce D (2000) Agrobacterium-mediated sorghum transformation. Plant Mol Biol 44:789–798
Zhao ZY, Gu W, Cai T, Tagliani L, Hondred D, Bond D, Schroeder S, Rudert M, Pierce D (2001) High throughput genetic transformation mediated by Agrobacterium tumefaciens in maize. Mol Breed 8:323–333
Zhou M, Hu Q, Li Z, Li D, Chen CF, Luo H (2011) Expression of a novel antimicrobial peptide Penaeidin4-1 in creeping bentgrass (Agrostis stolonifera L.) enhances plant fungal disease resistance. PLoS One 6, e24677
Zhou M, Li D, Li Z, Hu Q, Yang C, Zhu L, Luo H (2013) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol 161:1375–1391
Zou J, Liu C, Liu A, Zou D, Chen X (2012) Overexpression of OsHsp17.0 and OsHsp23.7 enhances drought and salt tolerance in rice. J Plant Physiol 169:628–635
Acknowledgments
The authors’ work in the area of millet genomics is supported by the core grant of the National Institute of Plant Genome Research (NIPGR), New Delhi, India. Mr. Roshan K Singh acknowledges the Council of Scientific and Industrial Research, Government of India, New Delhi, for awarding Research Fellowship. The authors also acknowledge Mr. Mehanathan Muthamilarasan, NIPGR, for his helpful suggestions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Handling Editor: Bhumi Nath Tripathi
Rights and permissions
About this article
Cite this article
Singh, R.K., Prasad, M. Advances in Agrobacterium tumefaciens-mediated genetic transformation of graminaceous crops. Protoplasma 253, 691–707 (2016). https://doi.org/10.1007/s00709-015-0905-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-015-0905-3