Chloroplast genomes: Diversity, evolution, and applications in genetic engineering

Genome Biology

Volumn 17, Issue 1, 2016, Pages

  Daniell, Henry ^a   Lin, Choun Sea ^b   Yu, Ming ^a   Chang, Wan Jung ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AGRONOMIC TRAIT; BIOLOGY; CHLOROPLAST GENOME; CULTIVATED SPECIES; DOMESTICATION; EMBRYOPHYTA; GENE TRANSFER; GENETIC ENGINEERING; HUMAN; HUMAN CELL; TRANSGENE; CHLOROPLAST; GENETIC VARIATION; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; PLANT; PLANT GENOME;

CHLOROPLASTS; EVOLUTION, MOLECULAR; GENETIC ENGINEERING; GENETIC VARIATION; GENOME, CHLOROPLAST; GENOME, PLANT; PHYLOGENY; PLANTS; TRANSGENES;

EID: 84978110419     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-016-1004-2     Document Type: Review

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254. 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 Biotechnol J. 2014;12:503-15.
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256. McBride KE, Svab Z, Schaaf DJ, Hogan PS, Stalker DM, Maliga P. Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Biotechnology (N Y). 1995;13:362-5.
257. Kota M, Daniell H, Varma S, Garczynski SF, Gould F, Moar WJ. Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. Proc Natl Acad Sci U S A. 1999;96:1840-5.
258. Lee SB, Kwon HB, Kwon SJ, Park SC, Jeong MJ, Han SE, et al. Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breeding. 2003;11:1-13.
259. Ruiz ON, Hussein HS, Terry N, Daniell H. Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol. 2003;132:1344-52.
260. Ruiz ON, Alvarez D, Torres C, Roman L, Daniell H. Metallothionein expression in chloroplasts enhances mercury accumulation and phytoremediation capability. Plant Biotechnol J. 2011;9:609-17.
261. Lutz KA, Knapp JE, Maliga P. Expression of bar in the plastid genome confers herbicide resistance. Plant Physiol. 2001;125:1585-90.
262. Ye GN, Hajdukiewicz PT, Broyles D, Rodriguez D, Xu CW, Nehra N, Staub JM. Plastid-expressed 5-enolpyruvylshikimate-3-phosphate synthase genes provide high level glyphosate tolerance in tobacco. Plant J. 2001;25:261-70.
263. Shimizu M, Goto M, Hanai M, Shimizu T, Izawa N, Kanamoto H, et al. Selectable tolerance to herbicides by mutated acetolactate synthase genes integrated into the chloroplast genome of tobacco. Plant Physiol. 2008;147:1976-83.
264. Iamtham S, Day A. Removal of antibiotic resistance genes from transgenic tobacco plastids. Nat Biotechnol. 2000;18:1172-6.
265. Dufourmantel N, Dubald M, Matringe M, Canard H, Garcon F, Job C, et al. 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. 2007;5:118-33.
266. Fouad WM, Altpeter F. Transplastomic expression of bacterial L-aspartate-alpha-decarboxylase enhances photosynthesis and biomass production in response to high temperature stress. Transgenic Res. 2009;18:707-18.
267. Lu Y, Rijzaani H, Karcher D, Ruf S, Bock R. Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proc Natl Acad Sci U S A. 2013;110:E623-32.
268. Ruiz ON, Daniell H. Engineering cytoplasmic male sterility via the chloroplast genome by expression of beta-ketothiolase. Plant Physiol. 2005;138:1232-46.
269. Yabuta Y, Tanaka H, Yoshimura S, Suzuki A, Tamoi M, Maruta T, Shigeoka S. Improvement of vitamin E quality and quantity in tobacco and lettuce by chloroplast genetic engineering. Transgenic Res. 2013;22:391-402.
270. Harada H, Maoka T, Osawa A, Hattan J, Kanamoto H, Shindo K, et al. Construction of transplastomic lettuce (Lactuca sativa) dominantly producing astaxanthin fatty acid esters and detailed chemical analysis of generated carotenoids. Transgenic Res. 2014;23:303-15.
271. Pengelly JJ, Forster B, von Caemmerer S, Badger MR, Price GD, Whitney SM. Transplastomic integration of a cyanobacterial bicarbonate transporter into tobacco chloroplasts. J Exp Bot. 2014;65:3071-80.
272. 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 Biotechnol J. 2013;11:618-27.
273. Elghabi Z, Karcher D, Zhou F, Ruf S, Bock R. Optimization of the expression of the HIV fusion inhibitor cyanovirin-N from the tobacco plastid genome. Plant Biotechnol J. 2011;9:599-608.
274. Agrawal P, Verma D, Daniell H. Expression of Trichoderma reesei beta-mannanase in tobacco chloroplasts and its utilization in lignocellulosic woody biomass hydrolysis. PLoS One. 2011;6, e29302.
275. Verma D, Jin S, Kanagaraj A, Singh ND, Daniel J, Kolattukudy PE, et al. Expression of fungal cutinase and swollenin in tobacco chloroplasts reveals novel enzyme functions and/or substrates. PLoS One. 2013;8, e57187.
276. Saxena B, Subramaniyan M, Malhotra K, Bhavesh NS, Potlakayala SD, Kumar S. Metabolic engineering of chloroplasts for artemisinic acid biosynthesis and impact on plant growth. J Biosci. 2014;39:33-41.
277. Yu LX, Gray BN, Rutzke CJ, Walker LP, Wilson DB, Hanson MR. Expression of thermostable microbial cellulases in the chloroplasts of nicotine-free tobacco. J Biotechnol. 2007;131:362-9.
278. Petersen K, Bock R. High-level expression of a suite of thermostable cell wall-degrading enzymes from the chloroplast genome. Plant Mol Biol. 2011;76:311-21.
279. Arai Y, Shikanai T, Doi Y, Yoshida S, Yamaguchi I, Nakashita H. Production of polyhydroxybutyrate by polycistronic expression of bacterial genes in tobacco plastid. Plant Cell Physiol. 2004;45:1176-84.
280. Hasunuma T, Miyazawa SI, Yoshimura S, Shinzaki Y, Tomizawa KI, Shindo K, et al. Biosynthesis of astaxanthin in tobacco leaves by transplastomic engineering. Plant J. 2008;55:857-68.
281. Nakahira Y, Ishikawa K, Tanaka K, Tozawa Y, Shiina T. Overproduction of hyperthermostable beta-1,4-endoglucanase from the archaeon Pyrococcus horikoshii by tobacco chloroplast engineering. Biosci Biotechnol Biochem. 2013;77:2140-3.
282. Sherman A, Su J, Lin S, Wang X, Herzog RW, Daniell H. Suppression of inhibitor formation against FVIII in a murine model of hemophilia A by oral delivery of antigens bioencapsulated in plant cells. Blood. 2014;124:1659-68.
283. Sanz-Barrio R, Fernandez-San Millan A, Corral-Martinez P, Segui-Simarro JM, Farran I. Tobacco plastidial thioredoxins as modulators of recombinant protein production in transgenic chloroplasts. Plant Biotechnol J. 2011;9:639-50.
284. Farran I, McCarthy-Suarez I, Rio-Manterola F, Mansilla C, Lasarte JJ, Mingo-Castel AM. The vaccine adjuvant extra domain A from fibronectin retains its proinflammatory properties when expressed in tobacco chloroplasts. Planta. 2010;231:977-90.
285. Boyhan D, Daniell H. Low-cost production of proinsulin in tobacco and lettuce chloroplasts for injectable or oral delivery of functional insulin and C-peptide. Plant Biotechnol J. 2011;9:585-98.
286. Fernandez-San Millan 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 Biotechnol J. 2003;1:71-9.
287. Daniell H, Ruiz G, Denes B, Sandberg L, Langridge W. Optimization of codon composition and regulatory elements for expression of human insulin like growth factor-1 in transgenic chloroplasts and evaluation of structural identity and function. BMC Biotechnol. 2009;9:33.
288. + T cells. Blood. 2015;125:2418-27.
289. Su J, Sherman A, Doerfler PA, Byrne BJ, Herzog RW, Daniell H. Oral delivery of Acid Alpha Glucosidase epitopes expressed in plant chloroplasts suppresses antibody formation in treatment of Pompe mice. Plant Biotechnol J. 2015;13:1023-32.
290. Youm JW, Jeon JH, Kim H, Min SR, Kim MS, Joung H, et al. High-level expression of a human beta-site APP cleaving enzyme in transgenic tobacco chloroplasts and its immunogenicity in mice. Transgenic Res. 2010;19:1099-108.
291. Arlen PA, Falconer R, Cherukumilli S, Cole A, Cole AM, Oishi KK, Daniell H. Field production and functional evaluation of chloroplast-derived interferon-alpha2b. Plant Biotechnol J. 2007;5:511-25.
292. Ruhlman T, Ahangari R, Devine A, Samsam M, Daniell H. 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. 2007;5:495-510.
293. Leelavathi S, Reddy VS. Chloroplast expression of His-tagged GUS-fusions: a general strategy to overproduce and purify foreign proteins using transplastomic plants as bioreactors. Mol Breeding. 2003;11:49-58.
294. Lim S, Ashida H, Watanabe R, Inai K, Kim YS, Mukougawa K, et al. Production of biologically active human thioredoxin 1 protein in lettuce chloroplasts. Plant Mol Biol. 2011;76:335-44.
295. Nadai M, Bally J, Vitel M, Job C, Tissot G, Botterman J, Dubald M. High-level expression of active human alpha1-antitrypsin in transgenic tobacco chloroplasts. Transgenic Res. 2009;18:173-83.
296. Gisby MF, Mellors P, Madesis P, Ellin M, Laverty H, O'Kane S, et al. A synthetic gene increases TGF beta 3 accumulation by 75-fold in tobacco chloroplasts enabling rapid purification and folding into a biologically active molecule. Plant Biotechnol J. 2011;9:618-28.
297. Farran I, Rio-Manterola F, Iniguez M, Garate S, Prieto J, Mingo-Castel AM. High-density seedling expression system for the production of bioactive human cardiotrophin-1, a potential therapeutic cytokine, in transgenic tobacco chloroplasts. Plant Biotechnol J. 2008;6:516-27.
298. Staub JM, Garcia B, Graves J, Hajdukiewicz PT, Hunter P, Nehra N, et al. High-yield production of a human therapeutic protein in tobacco chloroplasts. Nat Biotechnol. 2000;18:333-8.
299. Oey M, Lohse M, Scharff LB, Kreikemeyer B, Bock R. Plastid production of protein antibiotics against pneumonia via a new strategy for high-level expression of antimicrobial proteins. Proc Natl Acad Sci U S A. 2009;106:6579-84.
300. Koya V, Moayeri M, Leppla SH, Daniell H. Plant-based vaccine: mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infect Immun. 2005;73:8266-74.
301. 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;22:4374-84.
302. Millan AFS, Ortigosa SM, Hervas-Stubbs S, Corral-Martinez P, Segui-Simarro JM, Gaetan J, et al. Human papillomavirus L1 protein expressed in tobacco chloroplasts self-assembles into virus-like particles that are highly immunogenic. Plant Biotechnol J. 2008;6:427-41.
303. Yacono MD, Farran I, Becher ML, Sander V, Sanchez VR, Martin V, et al. A chloroplast-derived Toxoplasma gondii GRA4 antigen used as an oral vaccine protects against toxoplasmosis in mice. Plant Biotechnol J. 2012;10:1136-44.
304. Kolotilin I, Kaldis A, Devriendt B, Joensuu J, Cox E, Menassa R. Production of a subunit vaccine candidate against porcine post-weaning diarrhea in high-biomass transplastomic tobacco. Plos One. 2012;7, e42405.
305. Arlen PA, Singleton M, Adamovicz JJ, Ding Y, Davoodi-Semiromi A, Daniell H. Effective plague vaccination via oral delivery of plant cells expressing F1-V antigens in chloroplasts. Infect Immun. 2008;76:3640-50.
306. Molina A, Hervas-Stubbs S, Daniell H, Mingo-Castel AM, Veramendi J. High-yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts. Plant Biotechnol J. 2004;2:141-53.
307. Lentz EM, Mozgovoj MV, Bellido D, Santos MJD, Wigdorovitz A, Bravo-Almonacid FF. VP8*antigen produced in tobacco transplastomic plants confers protection against bovine rotavirus infection in a suckling mouse model. J Biotechnol. 2011;156:100-7.
308. 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. J Mol Biol. 2001;311:1001-9.
309. Kang TJ, Loc NH, Jang MO, Jang YS, Kim YS, Seo JE, Yang MS. Expression of the B subunit of E. coli heat-labile enterotoxin in the chloroplasts of plants and its characterization. Transgenic Res. 2003;12:683-91.
310. 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 Biotechnol J. 2007;5:230-9.
311. Glenz K, Bouchon B, Stehle T, Wallich R, Simon MM, Warzecha H. Production of a recombinant bacterial lipoprotein in higher plant chloroplasts. Nat Biotechnol. 2006;24:76-7.
312. Rosales-Mendoza S, Alpuche-Solis AG, Soria-Guerra RE, Moreno-Fierros L, Martinez-Gonzalez L, Herrera-Diaz A, Korban SS. Expression of an Escherichia coli antigenic fusion protein comprising the heat labile toxin B subunit and the heat stable toxin, and its assembly as a functional oligomer in transplastomic tobacco plants. Plant J. 2009;57:45-54.
313. Soria-Guerra RE, Alpuche-Solis AG, Rosales-Mendoza S, Moreno-Fierros L, Bendik EM, Martinez-Gonzalez L, Korban SS. Expression of a multi-epitope DPT fusion protein in transplastomic tobacco plants retains both antigenicity and immunogenicity of all three components of the functional oligomer. Planta. 2009;229:1293-302.
314. Rubio-Infante N, Govea-Alonso DO, Alpuche-Solis AG, Garcia-Hernandez AL, Soria-Guerra RE, Paz-Maldonado LMT, et al. A chloroplast-derived C4V3 polypeptide from the human immunodeficiency virus (HIV) is orally immunogenic in mice. Plant Mol Biol. 2012;78:337-49.
315. Waheed MT, Thones N, Muller M, Hassan SW, Gottschamel J, Lossl E, et al. Plastid expression of a double-pentameric vaccine candidate containing human papillomavirus-16 L1 antigen fused with LTB as adjuvant: transplastomic plants show pleiotropic phenotypes. Plant Biotechnol J. 2011;9:651-60.
316. Gonzalez-Rabade N, McGowan EG, Zhou F, McCabe MS, Bock R, Dix PJ, et al. Immunogenicity of chloroplast-derived HIV-1 p24 and a p24-Nef fusion protein following subcutaneous and oral administration in mice. Plant Biotechnol J. 2011;9:629-38.
317. Zhou YX, Lee MYT, Ng JMH, Chye ML, Yip WK, Zee SY, Lam E. A truncated hepatitis E virus ORF2 protein expressed in tobacco plastids is immunogenic in mice. World J Gastroenterol. 2006;12:306-12.
318. Shao HB, He DM, Qian KX, Shen GF, Su ZL. The expression of classical swine fever virus structural protein E2 gene in tobacco chloroplasts for applying chloroplasts as bioreactors. C R Biol. 2008;331:179-84.
319. Tregoning JS, Nixon P, Kuroda H, Svab Z, Clare S, Bowe F, et al. Expression of tetanus toxin Fragment C in tobacco chloroplasts. Nucleic Acids Res. 2003;31:1174-9.
320. Morgenfeld M, Lentz E, Segretin ME, Alfano EF, Bravo-Almonacid F. Translational fusion and redirection to thylakoid lumen as strategies to enhance accumulation of human papillomavirus E7 antigen in tobacco chloroplasts. Mol Biotechnol. 2014;56:1021-31.