Abstract
The world population is expected to reach an estimated 9.2 billion by 2050. Therefore, food production globally has to increase by 70% in order to feed the world, while total arable land, which has reached its maximal utilization, may even decrease. Moreover, climate change adds yet another challenge to global food security. In order to feed the world in 2050, biotechnological advances in modern agriculture are essential. Plant genetic engineering, which has created a new wave of global crop production after the first green revolution, will continue to play an important role in modern agriculture to meet these challenges. Plastid genetic engineering, with several unique advantages including transgene containment, has made significant progress in the last two decades in various biotechnology applications including development of crops with high levels of resistance to insects, bacterial, fungal and viral diseases, different types of herbicides, drought, salt and cold tolerance, cytoplasmic male sterility, metabolic engineering, phytoremediation of toxic metals and production of many vaccine antigens, biopharmaceuticals and biofuels. However, useful traits should be engineered via chloroplast genomes of several major crops. This review provides insight into the current state of the art of plastid engineering in relation to agricultural production, especially for engineering agronomic traits. Understanding the bottleneck of this technology and challenges for improvement of major crops in a changing climate are discussed.
Similar content being viewed by others
References
Apel W, Bock R (2009) Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol 151:59–66
Apel W, Schulze WX, Bock R (2010) Identification of protein stability determinants in chloroplasts. Plant J 63:636–650
Bock R (2007) Plastid biotechnology: prospects for herbicide and insect resistance, metabolic engineering and molecular farming. Curr Opin Biotechnol 18:100–106
Bock R, Khan MS (2004) Taming plastids for a green future. Trends Biotechnol 22:311–318
Bock R, Warzecha H (2010) Solar-powered factories for new vaccines and antibiotics. Trends Biotechnol 28(5):246–252
Cheng L, Li HP, Qu B, Huang T, Tu JX, Fu TD, Liao YC (2010) Chloroplast transformation of rapeseed (Brassica napus) by particle bombardment of cotyledons. Plant Cell Rep 29:371–381
Corneille S, Lutz K, Svab Z, Maliga P (2001) Efficient elimination of selectable markergenes from the plastid genome by the CRE-lox site-specific recombination system. Plant J 72:171–178
Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Amer J Bot 75:1443–1458
Craig W, Lenzi P, Scotti N et al (2008) Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance. Transgenic Res 17:769–782
Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nat Biotechnol 20:581–586
Daniell H (2007) Transgene containment by maternal inheritance: effective or elusive? Proc Natl Acad Sci USA 104:6879–6880
Daniell H, Datta R, Varma S, Gray S, Lee SB (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nat Biotechnol 16:345–348
Daniell H, Khan M, Allison L (2002) Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology. Trends Plant Sci 7(2):84–91
Daniell H, Kumar S, Dufourmantel N (2005) Breakthrough in chloroplast genetic engineering of agronomically important crops. Trends Biotechnol 23:238–245
Daniell H, Lee SB, Grevich J et al (2006) Complete chloroplast genome sequences of Solanum bulbocastanum, Solanum lycopersicum and comparative analyses with other Solanaceae genomes. Theor Appl Genet 112:1503–1518
Daniell H, Singh ND, Mason H, Streatfield SJ (2009) Plant-made vaccines and biopharmaceuticals. Trends Plant Sci 14:669–679
De Cosa B, Moar W, Lee SB, Miller M, Daniell H (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 19:71–74
De Marchis F, Wang YX, Stevanato P, Arcioni S, Bellucci M (2009) Genetic transformation of the sugar beet plastome. Transgenic Res 18:17–30
DeGray G, Rajasekaran K, Smith F, Sanford J, Daniell H (2001) Expression of an antimicrobial peptide via the chloroplast genome to control phytopathogenic bacteria and fungi. Plant Physiol 127:852–862
Diekmann K, Hodkinson TR, Wolfe KH, Van Den Bekerom R, Dix PJ, Barth S (2009) Complete chloroplast genome sequence of a major allogamous forage species perennial ryegrass (Lolium perenne L.). DNA Res 16:165–176
Dufourmantel N, Pelissier B, Garcon F, Peltier G, Ferullo JM, Tissot G (2004) Generation of fertile transplastomic soybean. Plant Mol Biol 55:479–489
Dufourmantel N, Tissot G, Goutorbe F et al (2006) Generation and analysis of soybean plastid transformants expressing Bacillus thuringiensis Cry1Ab protoxin. Plant Mol Biol 58:659–668
Dufourmantel N, Dubald M, Matringe M, Canard H, Garcon F, Job C, Kay E, Wisniewski JP, Ferullo JM, Pelissier B, Sailland A, Tissot G (2007) Generation and characterization of soybean and marker-free tobacco plastid transformants over-expressing a bacterial 4-hydroxyphenylpyruvate dioxygenase which provides strong herbicide tolerance. Plant Biotechnol J 5:118–133
Filipecki M, Malepszy S (2006) Unintended consequences of plant transformation: a molecular insight. J Appl Genet 47:277–286
Grevich JJ, Daniell H (2005) Chloroplast genetic engineering: recent advances and future perspectives. Crit Rev Plant Sci 24:83–107
Hagemann R (2010) The foundation of extranuclear inheritance: plastid and mitochondrial genetics. Mol Genet Genomics 283:199–209
Harris SA, Ingram R (1991) Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon 40:393–412
Hu Y, Zhang Q, Rao G, Sodmergen (2008) Occurrence of plastids in the sperm cells of Caprifoliaceae: biparental plastid inheritance in Angiosperms is unilaterally derived from maternal inheritance. Plant Cell Physiol 49:958–968
Hussein SH, Ruiz ON, Terry N, Daniell H (2007) Phytoremediation of mercury and organomercurials in chloroplast transgenic plants: enhanced root uptake, translocation to shoots and volatilization. Environm Sci Technol 41:8439–8446
Iamtham S, Day A (2000) Removal of antibiotic resistance genes from transgenic tobacco plastids. Nat Biotechnol 18:1172–1176
James C (2009) Global status of commercialized biotech/GM Crops: 2009. ISAAA Brief No. 41. ISAAA, NY
Jansen RK, Raubeson LA, Boore JL et al (2005) Methods for obtaining and analyzing chloroplast genome sequences. Meth Enzym 395:348–384
Jin S, Kanagaraj A, Verma D, Lange T, Daniell H (2011) Release of hormones from conjugates: chloroplast expression of B-glucosidase results in elevated phytohormone levels with significant increase in biomass and protection from aphids and whiteflies conferred by sucrose esters. Plant Physiol 155:222–235
Kahlau S, Bock R (2008) Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell 20:856–874. doi:10.1105/tpc.107.055202
Kanamoto H, Yamashita A, Asao H, Okumura S, Takase H, Hattori M, Yokota A, Tomizawa K (2006) Efficient and stable transformation of Lactuca sativa L. cv. Cisco (lettuce) plastids. Transgenic Res 15:205–217
Kota M, Daniell H, Varma S, Garczynski SF, Gould F, Moar WJ (1999) Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. Proc Natl Acad Sci USA 96:1840–1845
Krichevsky A, Meyers B, Vainstein A, Maliga P, Citovsky V (2010) Autoluminescent plants. PLoS One 5:215461
Kumar S, Dhingra A, Daniell H (2004a) Plastid expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots and leaves confers enhanced salt tolerance. Plant Physiol 136:2843–2854
Kumar S, Dhingra A, Daniell H (2004b) Stable transformation of the cotton plastid genome and maternal inheritance of transgenes. Plant Mol Biol 56:203–216
Langbecker C, Ye GN, Broyles DL, Duggan LL, Xu CW, Hajdukiewicz PTJ, Armstrong CL, Staub JM (2004) High-frequency transformation of undeveloped plastids in tobacco suspension cells. Plant Physiol 135:39–46
Lee SB, Kwon HB, Kwon SJ, Park SC, Jeong MJ, Han SE, Byun MO, Daniell H (2003) Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breed 11:1–13
Lee SM, Kang KS, Chung H, Yoo SH, Xu XM, Lee SB, Cheong JJ, Daniell H, Kim M (2006) Plastid transformation in the monocotyledonous cereal crop, rice (Oryza sativa) and transmission of transgenes to their progeny. Mol Cells 21:401–410
Lee SB, Li B, Jin S, Daniell H (2011) Expression and characterization of antimicrobial peptides Retrocyclin-101 and Protegrin-1 in chloroplasts to control viral and bacterial infections. Plant Biotechnol J 9:100–115
Leelavathi S, Reddy VS (2003) Chloroplast expression of His-tagged GUS-fusions: a general strategy to overproduce and purify foreign proteins using transplastomic plants as bioreactors. Mol Breed 11:49–58
Lelivelt CLC, McCabe MS, Newell CA, deSnoo CB, van Dun KMP, Birch-Machin I, Gray JC, Mills KHG, Nugent JM (2005) Stable plastid transformation in lettuce (Lactuca sativa L.). Plant Mol Biol 58:763–774
Li W, Ruf S, Bock R (2010) Chloramphenicol acetyltransferase as selectable marker for plastid transformation. Plant Mol Biol. doi:10.1007/s11103-010-9678-4
Liu CW, Lin CC, Chen JJW, Tseng MJ (2007) Stable chloroplast transformation in cabbage (Brassica oleracea L. var. capitata L.) by particle bombardment. Plant Cell Rep 26:1733–1744
Lössl A, Bohmert K, Harloff H, Eibl C, Mühlbauer S, Koop HU (2005) Inducible trans-activation of plastid transgenes: expression of the Reutropha phb Operon in Transplastomic Tobacco. Plant Cell Physiol 46(9):1462–1471
Lutz KA, Maliga P (2007) Construction of marker-free transplastomic plants. Curr Opin Biotechnol 18:107–114
Lutz KA, Knapp JE, Maliga P (2001) Expression of bar in the plastid genome confers herbicide resistance. Plant Physiol 125:1585–1590
Lutz KA, Svab Z, Maliga P (2006) Construction of marker-free transplastomic tobacco using the Cre-loxP site-specific recombination system. Nat Protoc 1:900–910
Maliga P (2004) Plastid transformation in higher plants. Ann Rev Plant Biol 55:289–313
Mann CC (1999) Crop scientists seek a new revolution. Science 283:310–314
Martino-Catt SJ, Sachs ES (2008) Editor’s choice series: the next generation of biotech crops. Plant Physiol 147:3–5
McBride KE, Svab Z, Schaaf DJ, Hogan PS, Stalker DM, Maliga P (1995) Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Bio-Technol 13:362–365
Mullet J (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103:309–313
Nguyen TT, Nugent G, Cardi T, Dix PJ (2005) Generation of homoplasmic plastid transformants of a commercial cultivar of potato (Solanum tuberosum L.). Plant Sci 168:1495–1500
Nugent GD, Coyne S, Nguyen TT, Kavanagh TA, Dix PJ (2006) Nuclear and plastid transformation of Brassica oleracea var. botrytis (cauliflower) using PEG-mediated uptake of DNA into protoplasts. Plant Sci 170:135–142
Oey M, Lohse M, Kreikemeyer B, Bock R (2009) Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 57:436–445
Okumura S, Sawada M, Park YW, Hayashi T, Shimamura M, Takase H, Tomizawa KI (2006) Transformation of poplar (Populus alba) plastids and expression of foreign proteins in tree chloroplasts. Transgenic Res 15:637–646
Oldenburg DJ, Bendich AJ (2004a) Changes in the structure of DNA molecules and the amount of DNA per plastid during chloroplast development in maize. J Mol Biol 344:1311–1330
Oldenburg DJ, Bendich AJ (2004b) Most chloroplast DNA of maize seedlings in linear molecules with defined ends and branched forms. J Mol Biol 335:953–970
Quesada-Vargas T, Ruiz ON, Daniell H (2005) Characterization of heterologous multigene operons in transgenic chloroplasts. Transcription, processing, and translation. Plant Physiol 138:1746–1762
Ruf S, Hermann M, Berger IJ, Carrer H, Bock R (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat Biotechnol 19:870–875
Ruf S, Karcher D, Bock R (2007) Determining the transgene containment level provided by chloroplast transformation. Proc Natl Acad Sci USA 104:6998–7002
Ruhlman T, Ahangari R, Devine A, Samsam M, Daniell H (2007) Expression of cholera toxin B-proinsulin fusion protein in lettuce and tobacco chloroplasts—oral administration protects against development of insulitis in non-obese diabetic mice. Plant Biotechnol J 5:495–510
Ruhlman T, Verma D, Samson N, Daniell H (2010) The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol 152:2088–2104
Ruiz ON, Daniell H (2005) Engineering cytoplasmic male sterility via the chloroplast genome by expression of beta-ketothiolase. Plant Physiol 138:1232–1246
Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132:1344–1352
Saski C, Lee SB, Daniell H, Wood TC, Tomkins J, Kim HG, Jansen RK (2005) Complete chloroplast genome sequence of Glycine max and comparative analyses with other legume genomes. Plant Mol Biol 59(2):309–322
Saski C, Lee SB, Fjellheim S, Guda C, Jansen RK, Luo H, Tomkins J, Rognli OA, Daniell H, Clarke JL (2007) Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes. Theor Appl Genet 115:571–590
Sears BB (1980) Elimination of plastids during spermatogenesis and fertilization in the plant kingdom. Plasmid 4:233–255
Sharkey TD, Laporte M, Lu Y, Weise S, Weber APM (2004) Engineering plants for elevated CO2: a relationship between starch degradation and sugar sensing. Plant Biol 6:280–288
Sidorov VA, Kasten D, Pang SZ, Hajdukiewicz PTJ, Staub JM, Nehra NS (1999) Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J 19:209–216
Sikdar SR, Serino G, Chaudhuri S, Maliga P (1998) Plastid transformation in Arabidopsis thaliana. Plant Cell Rep 18:20–24
Silhavy D, Maliga P (1998) Plastid promoter utilization in a rice embryogenic cell culture. Curr Genet 34:67–70
Singh AK, Verma SS, Bansal KC (2010) Plastid transformation in eggplant (Solanum melongena L.). Transgenic Res 19:113–119
Sodmergen, Kawano S, Tano S, Kuroiwa T (1991) Degradation of chloroplast DNA in second leaves of rice (Oryza sativa) before leaf yellowing. Protoplasma 160:89–98
Svab Z, Maliga P (2007) Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. Proc Natl Acad Sci USA 104:7003–7008
Valkov V, Gargano D, Manna C, Formisano G, Dix PJ, Gray JC, Scotti N, Cardi T (2010) High efficiency plastid transformation in potato and regulation of transgene expression in leaves and tubers by alternative 5’ and 3’ regulatory sequences. Transgenic Res. doi:10.1007/s11248-010-9402-9
Verma D, Daniell H (2007) Chloroplast vector systems for biotechnology applications. Plant Physiol 145:1129–1143
Verma D, Samson NP, Koya V, Daniell H (2008) A protocol for expression of foreign genes in chloroplasts. Nat Protoc 3:739–758
Verma D, Kanagaraj A, Jin S, Singh ND, Kolattukudy PE, Daniell H (2010) Chloroplast-derived enzyme cocktails hydrolyse lignocellulosic biomass and release fermentable sugars. Plant Biotechnol J 8:332–350
Wurbs D, Ruf S, Bock R (2007) Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. Plant J 49:276–288
Ye GN, Hajdukiewicz PTJ, Broyles D, Rodriguez D, Xu CW, Nehra N, Staub JM (2001) Plastid-expressed 5-enolpyruvylshikimate-3-phosphate synthase genes provide high level glyphosate tolerance in tobacco. Plant J 25:261–270
Zhang Q, Liu Y, Sodmergen (2003) Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol 44:941–951
Zheng Q, Oldenburg DJ, Bendich AJ (2011) Independent effects of leaf growth and light on the development of the plastid and its DNA content in Zea species. J Exp Bot. doi:10.1093/jxb/erq441
Zhou F, Badillo-Corona JA, Karcher D, Gonzalez-Rabade N, Piepenburg K, Borchers AMI, Maloney AP, Kavanagh TA, Gray JC, Bock R (2008) High-level expression of human immunodeficiency virus antigens from the tobacco and tomato plastid genomes. Plant Biotechnol J 6:897–913
Zubko M, Zubko E, Zuilen K, Meyer P, Day A (2004) Stable transformation of petunia plastids. Transgenic Res 13:523–530
Acknowledgments
We thank the Research Council of Norway for grant BILAT-174998/D15 and Bioforsk core funding to Jihong Liu Clarke and USDA-CSREES, USDA-NIFA and NIH 2 R01 GM 063879 to Henry Daniell. The authors thank Nicholas Clarke and Sonja Klemsdal for critical reading and Shuai Guo for his help with references.
Author information
Authors and Affiliations
Corresponding author
Additional information
An erratum to this article can be found at http://dx.doi.org/10.1007/s11103-011-9809-6
Rights and permissions
About this article
Cite this article
Clarke, J.L., Daniell, H. Plastid biotechnology for crop production: present status and future perspectives. Plant Mol Biol 76, 211–220 (2011). https://doi.org/10.1007/s11103-011-9767-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-011-9767-z