The Concept of Chloroplast Transformation; Its Relevance Towards Food Security

Bushra Tabassum, Iqra Yousaf, Olawale Samuel Adeyinka, Rida Khalid, Anwar Khan

Abstract


The world population is expected to reach an estimated 9.2 billion by 2050 which means up to 70% increase in food production would be needed to feed the world. Moreover, climate changes pose yet another challenge to global food security. Genetic engineering is playing its role in modern agriculture to overcome food security challenges but for better crop production more biotechnological advances are required. Chloroplast genetic engineering provides a better alternative to nuclear genetic engineering due to its properties of precise transgene insertion through homologous recombination, lack of epigenetic changes and high transgene expression. We reviewed the fundamentals behind chloroplast transformation and divulge its various applications in nutritional enhancement and agricultural stress management. Furthermore, we provide recent efforts of Ribonucleic Acid interference (RNAi) technology in the transplastomic transformation towards insect-specific and environmentally friendly control measures. We envisage that targeted chloroplast genome editing could be a game changer in the future application of chloroplast transformation.

Keywords: Agricultural stress management; Chloroplast transformation; Genome editing; RNA interference; Transgenic crops  


Full Text:

PDF

References


Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, et al.. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proceedings of the National Academy of Sciences, (2002); 99 (19): 12246–12251.

del Campo E. Post-transcriptional control of chloroplast gene expression. Gene Regulation and Systems Biology, (2009); 3: 31–47.

Chumley TW, Palmer JD, Mower JP, Fourcade HM, Calie PJ, Boore JL, Jansen RK. The complete chloroplast genome sequence of Pelargonium× hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Molecular biology and evolution, (2006); 23(11): 2175-90.

Gao L, SU YJ, Wang T. Plastid genome sequencing, comparative genomics, and phylogenomics: current status and prospects. Journal of Systematics and Evolution, (2010); 48(2): 77-93.

Wambugu PW, Brozynska M, Furtado A, Waters DL, Henry RJ. Relationships of wild and domesticated rices (Oryza AA genome species) based upon whole chloroplast genome sequences. Scientific reports, (2015); 5(1): 13957.

Chacón S MI, Pickersgill B, Debouck DG. Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races. Theoretical and Applied Genetics, (2005); 110: 432-44.

Svab Z, Maliga PA. High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proceedings of the National Academy of Sciences, (1993); 90(3): 913-7.

Ahmad A, O Pereira E, J Conley A, S Richman A, Menassa R. Green biofactories: recombinant protein production in plants. Recent patents on biotechnology, (2010); 4(3): 242-59.

Ravi V, Khurana JP, Tyagi AK, Khurana PJ. An update on chloroplast genomes. Plant Systematics and Evolution, (2008); 271: 101-22.

Kavanagh TA, Thanh ND, Lao NT, McGrath N, Peter SO, Horváth EM, Dix PJ, Medgyesy P. Homeologous plastid DNA transformation in tobacco is mediated by multiple recombination events. Genetics, (1999); 152(3): 1111-22.

Guda C, Lee SB, Daniell H. Stable expression of a biodegradable protein-based polymer in tobacco chloroplasts. Plant Cell Reports, (2000); 19: 257-62.

Verma D, Daniell H. Chloroplast vector systems for biotechnology applications. Plant physiology, (2007); 145(4): 1129-43.

De Block M, Schell J, Van Montagu M. Chloroplast transformation by Agrobacterium tumefaciens. The EMBO journal, (1985); 4(6): 1367-72.

Chen Q, Lai H. Plant-derived virus-like particles as vaccines. Human vaccines & immunotherapeutics, (2013); 9(1): 26-49.

Cañizares MC, Nicholson L, Lomonossoff GP. Use of viral vectors for vaccine production in plants. Immunology and Cell Biology, (2005); 83(3): 263-70.

Hedtke B, Legen J, Weihe A, Herrmann RG, Börner T. Six active phage‐type RNA polymerase genes in Nicotiana tabacum. The Plant Journal, (2002);30(6):625-37.

Liere K, Weihe A, Börner T. The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. Journal of plant physiology, (2011);168(12):1345-60.

Stoppel R, Meurer J. The cutting crew–ribonucleases are key players in the control of plastid gene expression. Journal of experimental botany, (2012);63(4):1663-73.

Fernández‐San Millán A, Mingo‐Castel A, Miller M, Daniell H. A chloroplast transgenic approach to hyper‐express and purify Human Serum Albumin, a protein highly susceptible to proteolytic degradation. Plant biotechnology journal, (2003);1(2):71-9.

Kuroda H, Maliga P. Sequences downstream of the translation initiation codon are important determinants of translation efficiency in chloroplasts. Plant physiology, (2001);125(1):430-6.

Rasala BA, Muto M, Sullivan J, Mayfield SP. Improved heterologous protein expression in the chloroplast of Chlamydomonas reinhardtii through promoter and 5′ untranslated region optimization. Plant biotechnology journal, (2011);9(6):674-83.

Eibl C, Zou Z, Beck A, Kim M, Mullet J, Koop HU. In vivo analysis of plastid psbA, rbcL and rpl32 UTR elements by chloroplast transformation: tobacco plastid gene expression

is controlled by modulation of transcript levels and translation efficiency. The Plant Journal, (1999); 19(3): 333-45.

Skorski P, Leroy P, Fayet O, Dreyfus M, Hermann-Le Denmat S. The highly efficient translation initiation region from the Escherichia coli rpsA gene lacks a Shine-Dalgarno element. Journal of bacteriology, (2006); 188(17):6277-85.

Scharff LB, Childs L, Walther D, Bock R. Local absence of secondary structure permits translation of mRNAs that lack ribosome-binding sites. PLoS genetics, (2011); 7(6): e1002155.

Kuroda H, Suzuki H, Kusumegi T, Hirose T, Yukawa Y, Sugiura M. Translation of psbC mRNAs starts from the downstream GUG, not the upstream AUG, and requires the extended Shine–Dalgarno sequence in tobacco chloroplasts. Plant and cell physiology, (2007); 48(9):1374-8.

Zhou F, Badillo‐Corona JA, Karcher D, Gonzalez‐Rabade N, Piepenburg K, Borchers AM, Maloney AP, Kavanagh TA, Gray JC, Bock R. High‐level expression of human immunodeficiency virus antigens from the tobacco and tomato plastid genomes. Plant biotechnology journal, (2008); 6(9): 897-913.

Stern DB, Goldschmidt-Clermont M, Hanson MR. Chloroplast RNA metabolism. Annual review of plant biology, (2010); 61: 125-55.

Dufourmantel N, Dubald M, Matringe M, Canard H, Garcon F, Job C, Kay E, Wisniewski JP, Ferullo JM, Pelissier B, Sailland A. Generation and characterization of soybean and marker‐free tobacco plastid transformants over‐expressing a bacterial 4‐hydroxyphenylpyruvate dioxygenase which provides strong herbicide tolerance. Plant biotechnology journal, (2007); 5(1):118-33.

Ma JK, Drake PM, Christou P. The production of recombinant pharmaceutical proteins in plants. Nature reviews genetics, (2003); 4(10): 794-805.

Staub JM, Garcia B, Graves J, Hajdukiewicz PT, Hunter P, Nehra N, Paradkar V, Schlittler M, Carroll JA, Spatola L, Ward D. High-yield production of a human therapeutic protein in tobacco chloroplasts. Nature biotechnology, (2000); 18(3): 333-8.

McCabe MS, Klaas M, Gonzalez‐Rabade N, Poage M, Badillo‐Corona JA, Zhou F, Karcher D, Bock R, Gray JC, Dix PJ. Plastid transformation of high‐biomass tobacco variety Maryland Mammoth for production of human immunodeficiency virus type 1 (HIV‐1) p24 antigen. Plant biotechnology journal, (2008) ;6(9): 914-29.

Arntzen C. Plant‐made pharmaceuticals: from ‘Edible Vaccines’ to Ebola therapeutics. Plant biotechnology journal, (2015); 13(8):1013.

Mayfield SP, Franklin SE, Lerner RA. Expression and assembly of a fully active antibody in algae. Proceedings of the National Academy of Sciences, (2003); 100(2):438-42.

Tran M, Zhou B, Pettersson PL, Gonzalez MJ, Mayfield SP. Synthesis and assembly of a full‐length human monoclonal antibody in algal chloroplasts. Biotechnology and bioengineering, (2009);104(4):663-73.

Tran M, Van C, Barrera DJ, Pettersson PL, Peinado CD, Bui J, Mayfield SP. Production of unique immunotoxin cancer therapeutics in algal chloroplasts. Proceedings of the National Academy of Sciences, (2013); 110(1):E15-22.

Koya V, Moayeri M, Leppla SH, Daniell H. Plant-based vaccine: mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infection and immunity, (2005); 73(12):8266-74.

Watson J, Koya V, Leppla SH, Daniell H. Expression of Bacillus anthracis protective antigen in transgenic chloroplasts of tobacco, a non-food/feed crop. Vaccine, (2004); 22(31-32):4374-84.

Daniell H, Chebolu S, Kumar S, Singleton M, Falconer R. Chloroplast-derived vaccine antigens and other therapeutic proteins. Vaccine, (2005); 23(15): 1779-83.

Daniell H, Lee SB, Panchal T, Wiebe PO. Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. Journal of molecular biology, (2001); 311(5):1001-9.

Tregoning JS, Nixon P, Kuroda H, Svab Z, Clare S, Bowe F, Fairweather N, Ytterberg J, Wijk KJ, Dougan G, Maliga P. Expression of tetanus toxin fragment C in tobacco chloroplasts. Nucleic acids research, (2003);31(4):1174-9.

Molina A, Hervás‐Stubbs S, Daniell H, Mingo‐Castel AM, Veramendi J. High‐yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts. Plant biotechnology journal, (2004);2(2):141-53.

Chebolu S, Daniell H. Stable expression of Gal/GalNAc lectin of Entamoeba histolytica in transgenic chloroplasts and immunogenicity in mice towards vaccine development for amoebiasis. Plant biotechnology journal, (2007);5(2):230-9.

Wurbs D, Ruf S, Bock R. Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. The Plant Journal, (2007); 49(2): 276-88.

Apel W, Bock R. Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiology, (2009); 151(1): 59-66.

Craig W, Lenzi P, Scotti N, De Palma M, Saggese P, Carbone V, McGrath Curran N, Magee AM, Medgyesy P, Kavanagh TA, Dix PJ. Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance. Transgenic research, (2008); 17: 769-82.

Jin S, Daniell H. Expression of γ‐tocopherol methyltransferase in chloroplasts results in massive proliferation of the inner envelope membrane and decreases susceptibility to salt and metal‐induced oxidative stresses by reducing reactive oxygen species. Plant biotechnology journal, (2014); 12(9):1274-85.

Tang L, Kwon SY, Kim SH, Kim JS, Choi JS, Cho KY, Sung CK, Kwak SS, Lee HS. Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Reports, (2006);25:1380-6.

Fouad WM, Altpeter F. Transplastomic expression of bacterial L-aspartate-α-decarboxylase enhances photosynthesis and biomass production in response to high temperature stress. Transgenic research, (2009);18:707-18.

Munns R, Tester M. Mechanisms of salinity tolerance. Mechanisms of Salinity Tolerance. Annual Review of Plant Biology, (2008); 59: 651–81.

Karim S, Aronsson H, Ericson H, Pirhonen M, Leyman B, Welin B, Mäntylä E, Palva ET, Van Dijck P, Holmström KO. Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Molecular Biology, (2007); 64:371-86.

Iordachescu M, Imai R. Trehalose biosynthesis in response to abiotic stresses. Journal of integrative plant biology, (2008); 50(10):1223-9.

Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, Kubo A, Tanaka K. Over‐expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiologia Plantarum, (2004); 121(2):231-8.

Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA. Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. Journal of plant physiology, (2005); 162(4): 465-72.

Khan MS, Kanwal B, Nazir S. Metabolic engineering of the chloroplast genome reveals that the yeast ArDH gene confers enhanced tolerance to salinity and drought in plants. Frontiers in plant science, (2015); 6: 725.

Ruiz ON, Hussein HS, Terry N, Daniell H. Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiology, (2003); 132(3):1344-52.

Zhang J, Tan W, Yang XH, Zhang HX. Plastid-expressed choline monooxygenase gene improves salt and drought tolerance through accumulation of glycine betaine in tobacco. Plant cell reports, (2008); 27: 1113-24.

Le Martret B, Poage M, Shiel K, Nugent GD, Dix PJ. Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione‐S‐transferase, exhibit altered anti‐oxidant metabolism and improved abiotic stress tolerance. Plant Biotechnology Journal, (2011); 9(6): 661-73.

Ceccoli RD, Blanco NE, Segretin ME, Melzer M, Hanke GT, Scheibe R, Hajirezaei MR, Bravo-Almonacid FF, Carrillo N. Flavodoxin displays dose-dependent effects on photosynthesis and stress tolerance when expressed in transgenic tobacco plants. Planta, (2012); 236:1447-58.

Lee SB, Li B, Jin S, Daniell H. Expression and characterization of antimicrobial peptides Retrocyclin‐101 and Protegrin‐1 in chloroplasts to control viral and bacterial infections. Plant biotechnology journal, (2011); 9(1):100-15.

Chakrabarti SK, Lutz KA, Lertwiriyawong B, Svab Z, Maliga P. Expression of the cry9Aa2 Bt gene in tobacco chloroplasts confers resistance to potato tuber moth. Transgenic research, (2006); 15: 481-8.

Jin S, Zhang X, Daniell H. Pinellia ternata agglutinin expression in chloroplasts confers broad spectrum resistance against aphid, whitefly, Lepidopteran insects, bacterial and viral pathogens. Plant biotechnology journal, (2012); 10(3): 313-27.

Jin S, Kanagaraj A, Verma D, Lange T, Daniell H. Release of hormones from conjugates: chloroplast expression of β-glucosidase results in elevated phytohormone levels associated with significant increase in biomass and protection from aphids or whiteflies conferred by sucrose esters. Plant physiology, (2011); 155(1): 222-35.

Lu Y, Rijzaani H, Karcher D, Ruf S, Bock R. Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proceedings of the National Academy of Sciences, (2013); 110(8): E623-32.

Grant OM, Brennan DP, Mellisho Salas CD, Dix PJ. Impact of enhanced capacity to scavenge reactive oxygen species on cold tolerance of tobacco. International Journal of Plant Sciences, (2014); 175(5):544-54.

Kumar S, Dhingra A, Daniell H. Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiology, (2004); 136(1): 2843-54.

Chen PJ, Senthilkumar R, Jane WN, He Y, Tian Z, Yeh KW. Transplastomic Nicotiana benthamiana plants expressing multiple defence genes encoding protease inhibitors and chitinase display broad‐spectrum resistance against insects, pathogens and abiotic stresses. Plant Biotechnology Journal, (2014); 12(4): 503-15.

Wani SH, Sah SK, Sági L, Solymosi K. Transplastomic plants for innovations in agriculture. A review. Agronomy for sustainable development, (2015); 35: 1391-430.

Chan YL, Cai D, Taylor PW, Chan MT, Yeh KW. Adverse effect of the chitinolytic enzyme PjCHI‐1 in transgenic tomato on egg mass production and embryonic development of Meloidogyne incognita. Plant pathology, (2010); 59(5): 922-30.

Senthilkumar R, Cheng CP, Yeh KW. Genetically pyramiding protease‐inhibitor genes for dual broad‐spectrum resistance against insect and phytopathogens in transgenic tobacco. Plant biotechnology journal, (2010); 8(1):65-75.

Verma D, Kanagaraj A, Jin S, Singh ND, Kolattukudy PE, Daniell H. Chloroplast‐derived enzyme cocktails hydrolyse lignocellulosic biomass and release fermentable sugars. Plant biotechnology journal, (2010); 8(3): 332-50.

Cosa BD, Moar W, Lee SB, Miller M, Daniell H. Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nature biotechnology, (2001); 19(1):71-4.

Yu Y, Yu PC, Chang WJ, Yu K, Lin CS. Plastid transformation: how does it work? Can it be applied to crops? What can it offer?. International Journal of Molecular Sciences, (2020); 21(14): 4854.

Reddy VS, Leelavathi S, Selvapandiyan A, Raman R, Giovanni F, Shukla V, Bhatnagar RK. Analysis of chloroplast transformed tobacco plants with cry 1Ia5 under rice psbA transcriptional elements reveal high level expression of Bt toxin without imposing yield penalty and stable inheritance of transplastome. Molecular Breeding, (2002); 9: 259-69.

Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science, (2015); 347(6225): 991-4.

Sanz‐Barrio R, Corral‐Martinez P, Ancin M, Segui‐Simarro JM, Farran I. Overexpression of plastidial thioredoxin f leads to enhanced starch accumulation in tobacco leaves. Plant Biotechnology Journal, (2013); 11(5):618-27.

Adeyinka OS, Tabassum B, Koloko BL, Ogungbe IV. Enhancing the quality of staple food crops through CRISPR/Cas-mediated site-directed mutagenesis. Planta, (2023); 257(4): 78.

Jin S, Singh ND, Li L, Zhang X, Daniell H. Engineered chloroplast dsRNA silences cytochrome p450 monooxygenase, V‐ATPase and chitin synthase genes in the insect gut and disrupts Helicoverpa armigera larval development and pupation. Plant biotechnology journal, (2015); 13(3): 435-46.

He G. Engineering chloroplasts for insect pest control. Proceedings of the National Academy of Sciences, (2022);119(22):e2205125119.

Kadoić Balaško M, Mikac KM, Bažok R, Lemic D. Modern techniques in Colorado potato beetle (Leptinotarsa decemlineata Say) control and resistance management: history review and future perspectives. Insects, (2020);11(9):581.




DOI: http://dx.doi.org/10.62940/als.v11i1.1647

Refbacks

  • There are currently no refbacks.