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Chloroplast Engineering: Fundamental Insights and Its Application in Amelioration of Environmental Stress

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Abstract

Chloroplasts are specialized organelle that are responsible for converting light energy to chemical energy, thereby driving the carbon dioxide fixation. Apart from photosynthesis, chloroplast is the site for essential cellular processes that determine the plant adaptation to changing environment. Owing to the presence of their own expression system, it provides an optimum platform for engineering valued traits as well as site for synthesis of bio-compounds. Advancements in technology have further enhanced the scope of using chloroplast as a multifaceted tool for the biotechnologist to develop stress-tolerant plants and ameliorate environmental stress. Focusing on chloroplast biotechnology, this review discusses the advances in chloroplast engineering and its application in enhancing plant adaptation and resistance to environmental stress and the development of new bioproducts and processes. This is accomplished through analysis of its biogenesis and physiological processes, highlighting the chloroplast engineering and recent developments in chloroplast biotechnology. In the first part of the review, the evolution and principles of structural organization and physiology of chloroplast are discussed. In the second part, the chief methods and mechanisms involved in chloroplast transformation are analyzed. The last part represents an updated analysis of the application of chloroplast engineering in crop improvement and bioproduction of industrial and health compounds.

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References

  1. Blankenship, R. E. (2010). Early evolution of photosynthesis. Plant Physiology, 154, 434–438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ahmad, N., Burgess, S. J., & Nielsen, B. L. (2016). Editorial: Advances in plastid biology and its applications. Frontiers in Plant Science, 7, 1396.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Lopez-Juez, E., & Pyke, K. A. (2005). Plastids unleashed: Their development and their integration in plant development. International Journal of Developmental Biology, 49, 557–577.

    Article  CAS  PubMed  Google Scholar 

  4. Marin, A., Passarini, F., van Stokkum, I. H., van Grondelle, R., & Croce, R. (2011). Minor complexes at work: Light-harvesting by carotenoids in the photosystem II antenna complexes CP24 and CP26. Biophys J, 100, 2829–2838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Richardson, L. G. L., & Schnell, D. J. (2020). Origins, function, and regulation of the TOC-TIC general protein import machinery of plastids. Journal of Experimental Botany, 71, 1226–1238.

    Article  CAS  PubMed  Google Scholar 

  6. Johnson, M. P. (2016). Photosynthesis. Essays in Biochemistry, 60, 255–273.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Wieczorek, A. M., & Wright, M. G. (2012). History of agricultural biotechnology: How crop development has evolved. Nature Education Knowledge, 3, 9.

    Google Scholar 

  8. Bansal, K. C., & Saha, D. (2012). Chloroplast genomics and genetic engineering for crop improvement. Agricultural Research, 1, 53–66.

    Article  CAS  Google Scholar 

  9. Sakamoto, W., & Takami, T. (2018). Chloroplast DNA dynamics: Copy number, quality control and degradation. Plant and Cell Physiology, 59, 1120–1127.

    Article  CAS  PubMed  Google Scholar 

  10. Neuhaus, H. E., & Emes, M. J. (2000). Nonphotosynthetic metabolism in plastids. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 111–140.

    Article  CAS  PubMed  Google Scholar 

  11. Ohlrogge, J., & Browse, J. (1995). Lipid biosynthesis. The Plant Cell, 7, 957–970.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Yoo, Y. H., Hong, W. J., & Jung, K. H. (2019). A systematic view exploring the role of chloroplasts in plant abiotic stress responses. BioMed Research International, 2019, 6534745.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Adem, M., Beyene, D., & Feyissa, T. (2017) Recent achievements obtained by chloroplast transformation. Plant Methods 13

  14. Whatley, J. M. (1981). Chloroplast evolution–Ancient and modern. Annals of the New York Academy of Sciences, 361, 154–165.

    Article  CAS  PubMed  Google Scholar 

  15. Dolganov, N. A., Bhaya, D., & Grossman, A. R. (1995). Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: Evolution and regulation. Proc Natl Acad Sci U S A, 92, 636–640.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Moreno, J. C. (2019). The proteOMIC era: A useful tool to gain deeper insights into plastid physiology. Theoretical and Experimental Plant Physiology, 31, 157–171.

    Article  CAS  Google Scholar 

  17. Arvidsson, P. O., & Sundby, C. (1999). A model for the topology of the chloroplast thylakoid membrane. Australian Journal of Plant Physiology, 26, 687–694.

    CAS  Google Scholar 

  18. Austin, J. R., 2nd., & Staehelin, L. A. (2011). Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiology, 155, 1601–1611.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Thomson, S. M., Pulido, P., & Jarvis, R. P. (2020). Protein import into chloroplasts and its regulation by the ubiquitin-proteasome system. Biochemical Society Transactions, 48, 71–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jarvis, P., & Lopez-Juez, E. (2013). Biogenesis and homeostasis of chloroplasts and other plastids. Nature Reviews Molecular Cell Biology, 14, 787–802.

    Article  CAS  PubMed  Google Scholar 

  21. Savage, L. J., Imre, K. M., Hall, D. A., & Last, R. L. (2013). Analysis of essential arabidopsis nuclear genes encoding plastid-targeted proteins. PLoS ONE, 8, e73291.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Dobrogojski, J., Adamiec, M., & Luciński, R. (2020). The chloroplast genome: A review. Acta Physiologiae Plantarum, 42, 98.

    Article  CAS  Google Scholar 

  23. Bendich, A. J. (1987). Why do chloroplasts and mitochondria contain so many copies of their genome? BioEssays, 6, 279–282.

    Article  CAS  PubMed  Google Scholar 

  24. Daniell, H., Lin, C. S., Yu, M., & Chang, W. J. (2016). Chloroplast genomes: Diversity, evolution, and applications in genetic engineering. Genome Biology, 17, 134.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Shrestha, B., Gilbert, L. E., Ruhlman, T. A., & Jansen, R. K. (2021) Clade-specific plastid inheritance patterns including frequent biparental inheritance in passiflora interspecific crosses. International Journal of Molecular Sciences 22.

  26. Liu, X., Li, Y., & Zhong, S. (2017). Interplay between light and plant hormones in the control of arabidopsis seedling chlorophyll biosynthesis. Frontiers in Plant Science, 8, 1433.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Fan, J., Andre, C., & Xu, C. (2011). A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Letters, 585, 1985–1991.

    Article  CAS  PubMed  Google Scholar 

  28. Chan, K. X., Phua, S. Y., Crisp, P., McQuinn, R., & Pogson, B. J. (2016). Learning the languages of the chloroplast: Retrograde signaling and beyond. Annual Review of Plant Biology, 67, 25–53.

    Article  CAS  PubMed  Google Scholar 

  29. Zhao, C., Wang, Y., Chan, K. X., Marchant, D. B., Franks, P. J., Randall, D., Tee, E. E., Chen, G., Ramesh, S., Phua, S. Y., Zhang, B., Hills, A., Dai, F., Xue, D., Gilliham, M., Tyerman, S., Nevo, E., Wu, F., Zhang, G., … Chen, Z. H. (2019). Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land. Proc Natl Acad Sci U S A, 116, 5015–5020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bischof, S., Baerenfaller, K., Wildhaber, T., Troesch, R., Vidi, P. A., Roschitzki, B., Hirsch-Hoffmann, M., Hennig, L., Kessler, F., Gruissem, W., & Baginsky, S. (2011). Plastid proteome assembly without Toc159: Photosynthetic protein import and accumulation of N-acetylated plastid precursor proteins. The Plant Cell, 23, 3911–3928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Granlund, I., Hall, M., Kieselbach, T., & Schroder, W. P. (2009). Light induced changes in protein expression and uniform regulation of transcription in the thylakoid lumen of Arabidopsis thaliana. PLoS ONE, 4, e5649.

    Article  PubMed  PubMed Central  Google Scholar 

  32. De Cosa, B., Moar, W., Lee, S. B., Miller, M., & Daniell, H. (2001). Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nature Biotechnology, 19, 71–74.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Castiglia, D., Sannino, L., Marcolongo, L., Ionata, E., Tamburino, R., De Stradis, A., Cobucci-Ponzano, B., Moracci, M., La Cara, F., & Scotti, N. (2016). High-level expression of thermostable cellulolytic enzymes in tobacco transplastomic plants and their use in hydrolysis of an industrially pretreated Arundo donax L biomass. Biotechnol Biofuels, 9, 154.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Molina, A., Hervas-Stubbs, S., Daniell, H., Mingo-Castel, A. M., & Veramendi, J. (2004). High-yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts. Plant Biotechnology Journal, 2, 141–153.

    Article  CAS  PubMed  Google Scholar 

  35. Lee, B., Kwon, H. B., Kwon, S. J., Park, S. C., Jeong, M., Han, S. E., & Daniell, H. (2003). Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Molecular Breeding, 11, 1–13.

    Article  CAS  Google Scholar 

  36. Leelavathi, S., Gupta, N., Maiti, S., Ghosh, A., & Reddy, V. S. (2003). Overproduction of an alkali- and thermo-stable xylanase in tobacco chloroplasts and efficient recovery of the enzyme. Molecular Breeding, 11, 59–67.

    Article  CAS  Google Scholar 

  37. Boynton, J. E., Gillham, N. W., Harris, E. H., Hosler, J. P., Johnson, A. M., Jones, A. R., Randolph-Anderson, B. L., Robertson, D., Klein, T. M., Shark, K. B., et al. (1988). Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science, 240, 1534–1538.

    Article  CAS  PubMed  Google Scholar 

  38. Diaz, A. H., & Koop, H. U. (2014). Nicotiana tabacum: PEG-mediated plastid transformation. In P. Maliga (Ed.), Chloroplast Biotechnology Methods in Molecular Biology 1132. Humana Press.

    Google Scholar 

  39. Golds, T., Maliga, P., & Koop, H. (1993). Stable plastid transformation in PEG-treated protoplasts of Nicotiana tabaccuum. Bio/Technology, 11, 95–97.

    CAS  Google Scholar 

  40. O’Neill, C., Horvath, G. V., Horvath, E., Dix, P. J., & Medgyesy, P. (1993). Chloroplast transformation in plants: Polyethylene glycol (PEG) treatment of protoplasts is an alternative to biolistic delivery systems. The Plant Journal, 3, 729–738.

    Article  CAS  PubMed  Google Scholar 

  41. Kwak, S. Y., Lew, T. T. S., Sweeney, C. J., Koman, V. B., Wong, M. H., Bohmert-Tatarev, K., Snell, K. D., Seo, J. S., Chua, N. H., & Strano, M. S. (2019). Chloroplast-selective gene delivery and expression in planta using chitosan-complexed single-walled carbon nanotube carriers. Nature Nanotechnology, 14, 447–455.

    Article  CAS  PubMed  Google Scholar 

  42. Santana, I., Wu, H., Hu, P., & Giraldo, J. P. (2020). Targeted delivery of nanomaterials with chemical cargoes in plants enabled by a biorecognition motif. Nature Communications, 11, 2045.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Daniell, H., Jin, S., Zhu, X. G., Gitzendanner, M. A., Soltis, D. E., & Soltis, P. S. (2021). Green giant-a tiny chloroplast genome with mighty power to produce high-value proteins: History and phylogeny. Plant Biotechnology Journal, 19, 430–447.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Krichevsky, A., Meyers, B., Vainstein, A., Maliga, P., & Citovsky, V. (2010). Autoluminescent plants. PLoS ONE, 5, e15461.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Daniell, H., Ruiz, O. N., & Dhingra, A. (2005). Chloroplast genetic engineering to improve agronomic traits. Methods in Molecular Biology, 286, 111–138.

    CAS  PubMed  Google Scholar 

  46. Guda, C., Lee, S. B., & Daniell, H. (2000). Stable expression of a biodegradable protein-based polymer in tobacco chloroplasts. Plant Cell Reports, 19, 257–262.

    Article  CAS  PubMed  Google Scholar 

  47. Lutz, K. A., Azhagiri, A. K., Tungsuchat-Huang, T., & Maliga, P. (2007). A guide to choosing vectors for transformation of the plastid genome of higher plants. Plant Physiology, 145, 1201–1210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Dauvillee, D., Delhaye, S., Gruyer, S., Slomianny, C., Moretz, S. E., d’Hulst, C., Long, C. A., Ball, S. G., & Tomavo, S. (2010). Engineering the chloroplast targeted malarial vaccine antigens in Chlamydomonas starch granules. PLoS ONE, 5, e15424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Fuentes, P., Zhou, F., Erban, A., Karcher, D., Kopka, J., & Bock, R. (2016) A new synthetic biology approach allows transfer of an entire metabolic pathway from a medicinal plant to a biomass crop. Elife 5

  50. Lu, Y., Rijzaani, H., Karcher, D., Ruf, S., & Bock, R. (2013). Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proc Natl Acad Sci U S A, 110, E623-632.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Newell, C. A., Birch-Machin, I., Hibberd, J. M., & Gray, J. C. (2003). Expression of green fluorescent protein from bacterial and plastid promoters in tobacco chloroplasts. Transgenic Research, 12, 631–634.

    Article  CAS  PubMed  Google Scholar 

  52. Caroca, R., Howell, K. A., Hasse, C., Ruf, S., & Bock, R. (2013). Design of chimeric expression elements that confer high-level gene activity in chromoplasts. The Plant Journal, 73, 368–379.

    Article  CAS  PubMed  Google Scholar 

  53. Valkov, V. T., Gargano, D., Manna, C., Formisano, G., Dix, P. J., Gray, J. C., Scotti, N., & Cardi, T. (2011). High efficiency plastid transformation in potato and regulation of transgene expression in leaves and tubers by alternative 5’ and 3’ regulatory sequences. Transgenic Research, 20, 137–151.

    Article  CAS  PubMed  Google Scholar 

  54. Wurbs, D., Ruf, S., & Bock, R. (2007). Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. The Plant Journal, 49, 276–288.

    Article  CAS  PubMed  Google Scholar 

  55. Occhialini, A., Piatek, A. A., Pfotenhauer, A. C., Frazier, T. P., Stewart, C. N., Jr., & Lenaghan, S. C. (2019). MoChlo: A versatile, modular cloning toolbox for chloroplast biotechnology. Plant Physiology, 179, 943–957.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Jin, S., & Daniell, H. (2015). The engineered chloroplast genome just got smarter. Trends in Plant Science, 20, 622–640.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Valkov, V. T., Scotti, N., Kahlau, S., Maclean, D., Grillo, S., Gray, J. C., Bock, R., & Cardi, T. (2009). Genome-wide analysis of plastid gene expression in potato leaf chloroplasts and tuber amyloplasts: Transcriptional and posttranscriptional control. Plant Physiology, 150, 2030–2044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Carter, A. P., Clemons, W. M., Brodersen, D. E., Morgan-Warren, R. J., Wimberly, B. T., & Ramakrishnan, V. (2000). Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature, 407, 340–348.

    Article  CAS  PubMed  Google Scholar 

  59. Goldschmidt-Clermont, M. (1991). Transgenic expression of aminoglycoside adenine transferase in the chloroplast: A selectable marker of site-directed transformation of chlamydomonas. Nucleic Acids Research, 19, 4083–4089.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Svab, Z., & Maliga, P. (1993). High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci U S A, 90, 913–917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Carrer, H., Hockenberry, T. N., Svab, Z., & Maliga, P. (1993). Kanamycin resistance as a selectable marker for plastid transformation in tobacco. Molecular and General Genetics, 241, 49–56.

    Article  CAS  PubMed  Google Scholar 

  62. Li, W., Ruf, S., & Bock, R. (2010). Chloramphenicol acetyltransferase as selectable marker for plastid transformation. Plant Molecular Biology, 76, 443–451.

    Article  PubMed  Google Scholar 

  63. Kumar, S., Dhingra, A., & Daniell, H. (2004). Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiology, 136, 2843–2854.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Cui, Y., Qin, S., & Jiang, P. (2014). Chloroplast transformation of Platymonas (Tetraselmis) subcordiformis with the bar gene as selectable marker. PLoS ONE, 9, e98607.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Queiroz, L. N., Maldaner, F. R., Mendes, E. A., Sousa, A. R., D’Allastta, R. C., Mendonca, G., Mendonca, D. B. S., & Aragao, F. J. L. (2019). Evaluation of lettuce chloroplast and soybean cotyledon as platforms for production of functional bone morphogenetic protein 2. Transgenic Research, 28, 213–224.

    Article  CAS  PubMed  Google Scholar 

  66. Ye, G. N., Hajdukiewicz, P. T., Broyles, D., Rodriguez, D., Xu, C. W., Nehra, N., & Staub, J. M. (2001). Plastid-expressed 5-enolpyruvylshikimate-3-phosphate synthase genes provide high level glyphosate tolerance in tobacco. The Plant Journal, 25, 261–270.

    Article  CAS  PubMed  Google Scholar 

  67. Shao, M., Kumar, S., & Thomson, J. G. (2014). Precise excision of plastid DNA by the large serine recombinase Bxb1. Plant Biotechnology Journal, 12, 322–329.

    Article  CAS  PubMed  Google Scholar 

  68. Park, J., Yan, G., Kwon, K. C., Liu, M., Gonnella, P. A., Yang, S., & Daniell, H. (2020). Oral delivery of novel human IGF-1 bioencapsulated in lettuce cells promotes musculoskeletal cell proliferation, differentiation and diabetic fracture healing. Biomaterials, 233, 119591.

    Article  CAS  PubMed  Google Scholar 

  69. Lin, M. T., Occhialini, A., Andralojc, P. J., Parry, M. A., & Hanson, M. R. (2014). A faster Rubisco with potential to increase photosynthesis in crops. Nature, 513, 547–550.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Lin, M. T., Orr, D. J., Worrall, D., Parry, M. A. J., Carmo-Silva, E., & Hanson, M. R. (2021). A procedure to introduce point mutations into the Rubisco large subunit gene in wild-type plants. The Plant Journal, 106, 876–887.

    Article  CAS  PubMed  Google Scholar 

  71. Whitney, S. M., Birch, R., Kelso, C., Beck, J. L., & Kapralov, M. V. (2015). Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone. Proc Natl Acad Sci U S A, 112, 3564–3569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Dhingra, A., Portis, A. R., Jr., & Daniell, H. (2004). Enhanced translation of a chloroplast-expressed RbcS gene restores small subunit levels and photosynthesis in nuclear RbcS antisense plants. Proc Natl Acad Sci U S A, 101, 6315–6320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Kebeish, R., Niessen, M., Thiruveedhi, K., Bari, R., Hirsch, H. J., Rosenkranz, R., Stabler, N., Schonfeld, B., Kreuzaler, F., & Peterhansel, C. (2007). Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nature Biotechnology, 25, 593–599.

    Article  CAS  PubMed  Google Scholar 

  74. Mantri N, Patade V, Penna S, Ford, R., and Pang, E. (2012) Abiotic stress responses in plants: Present and future. In Abiotic stress responses in plants New York: Springer

  75. Daniell, H., Datta, R., Varma, S., Gray, S., & Lee, S. B. (1998). Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nature Biotechnology, 16, 345–348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Dufourmantel, N., Dubald, M., Matringe, M., Canard, H., Garcon, F., Job, C., Kay, E., Wisniewski, J. P., Ferullo, J. M., 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 Biotechnology Journal, 5, 118–133.

    Article  CAS  PubMed  Google Scholar 

  77. Matringe, M., Sailland, A., Pelissier, B., Rolland, A., & Zink, O. (2005). p-Hydroxyphenylpyruvate dioxygenase inhibitor-resistant plants. Pest Management Science, 61, 269–276.

    Article  CAS  PubMed  Google Scholar 

  78. Le Martret, B., Poage, M., Shiel, K., Nugent, G. D., & Dix, P. J. (2011). 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, 9, 661–673.

    Article  PubMed  Google Scholar 

  79. You, L., Song, Q., Wu, Y., Li, S., Jiang, C., Chang, L., Yang, X., & Zhang, J. (2019). Accumulation of glycine betaine in transplastomic potato plants expressing choline oxidase confers improved drought tolerance. Planta, 249, 1963–1975.

    Article  CAS  PubMed  Google Scholar 

  80. McBride, K. E., Svab, Z., Schaaf, D. J., Hogan, P. S., Stalker, D. M., & Maliga, P. (1995). Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Biotechnology (N. Y), 13, 362–365.

    CAS  PubMed  Google Scholar 

  81. Chakrabarti, S. K., Lutz, K. A., Lertwiriyawong, B., Svab, Z., & Maliga, P. (2006). Expression of the cry9Aa2 B.t. gene in tobacco chloroplasts confers resistance to potato tuber moth. Transgenic Research, 15, 481–488.

    Article  CAS  PubMed  Google Scholar 

  82. Liu, C. W., Lin, C. C., Yiu, J. C., Chen, J. J., & Tseng, M. J. (2008). Expression of a Bacillus thuringiensis toxin (cry1Ab) gene in cabbage (Brassica oleracea L. var. capitata L.) chloroplasts confers high insecticidal efficacy against Plutella xylostella. TAG. Theoretical and Applied Genetics., 117, 75–88.

    Article  CAS  PubMed  Google Scholar 

  83. Wu, J., Luo, X., Zhang, X., Shi, Y., & Tian, Y. (2011). Development of insect-resistant transgenic cotton with chimeric TVip3A* accumulating in chloroplasts. Transgenic Research, 20, 963–973.

    Article  PubMed  Google Scholar 

  84. Wu, Y., Xu, L., Chang, L., Ma, M., You, L., Jiang, C., Li, S., & Zhang, J. (2019). Bacillus thuringiensis cry1C expression from the plastid genome of poplar leads to high mortality of leaf-eating caterpillars. Tree Physiology, 39, 1525–1532.

    Article  PubMed  Google Scholar 

  85. Xu, S., Zhang, Y., Li, S., Chang, L., Wu, Y., & Zhang, J. (2020). Plastid-expressed Bacillus thuringiensis (Bt) cry3Bb confers high mortality to a leaf eating beetle in poplar. Plant Cell Reports, 39, 317–323.

    Article  CAS  PubMed  Google Scholar 

  86. Zhang, J., Khan, S. A., Hasse, C., Ruf, S., Heckel, D. G., & Bock, R. (2015). Pest control. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science, 347, 991–994.

    Article  CAS  PubMed  Google Scholar 

  87. Chen, P. J., Senthilkumar, R., Jane, W. N., He, Y., Tian, Z., & Yeh, K. W. (2014). 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, 12, 503–515.

    Article  CAS  PubMed  Google Scholar 

  88. Hussein, H. S., Ruiz, O. N., Terry, N., & Daniell, H. (2007). Phytoremediation of mercury and organomercurials in chloroplast transgenic plants: Enhanced root uptake, translocation to shoots, and volatilization. Environmental Science and Technology, 41, 8439–8446.

    Article  CAS  PubMed  Google Scholar 

  89. Ruiz, O. N., Alvarez, D., Torres, C., Roman, L., & Daniell, H. (2011). Metallothionein expression in chloroplasts enhances mercury accumulation and phytoremediation capability. Plant Biotechnology Journal, 9, 609–617.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ruiz, O. N., Hussein, H. S., Terry, N., & Daniell, H. (2003). Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiology, 132, 1344–1352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Chu C, Liu B, Liu J, He J, Lv L, Wang H, Xie X, Tao Q, & Chen Q. (2020). Phytoremediation of acetochlor residue by transgenic Arabidopsis expressing the Acetochlor N-dealkylase from Sphingomonas wittichii DC-6. In Science of The Total Environment 728

  92. Iroegbu, A. O. C., Ray, S. S., Mbarane, V., Bordado, J. C., & Sardinha, J. P. (2021). Plastic pollution: A perspective on matters arising: Challenges and opportunities. ACS Omega, 6, 19343–19355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Oktavilia S, Hapsari M, Firmansyah, Setyadharma A, and Wahyuningsum IFS. (2020) Plastic industry and world environmental problems. In E3S Web of Conferences Vol. 202 p. 05020, EDP Sciences

  94. Bohmert-Tatarev, K., McAvoy, S., Daughtry, S., Peoples, O. P., & Snell, K. D. (2011). High levels of bioplastic are produced in fertile transplastomic tobacco plants engineered with a synthetic operon for the production of polyhydroxybutyrate. Plant Physiology, 155, 1690–1708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Viitanen, P. V., Devine, A. L., Khan, M. S., Deuel, D. L., Van Dyk, D. E., & Daniell, H. (2004). Metabolic engineering of the chloroplast genome using the Echerichia coli ubiC gene reveals that chorismate is a readily abundant plant precursor for p-hydroxybenzoic acid biosynthesis. Plant Physiology, 136, 4048–4060.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Agrawal, P., Verma, D., & Daniell, H. (2011). Expression of Trichoderma reesei beta-mannanase in tobacco chloroplasts and its utilization in lignocellulosic woody biomass hydrolysis. PLoS ONE, 6, e29302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Espinoza-Sánchez, E. A., Torres-Castillo, J. A., Rascón-Cruz, Q., Zavala-García, F., & Sinagawa-García, S. R. (2016). Production and characterization of fungal ß-glucosidase and bacterial cellulases by tobacco chloroplast transformation. Plant Biotechnology Reports, 10, 61–73.

    Article  Google Scholar 

  98. Kolotilin, I., Kaldis, A., Pereira, E. O., Laberge, S., & Menassa, R. (2013). Optimization of transplastomic production of hemicellulases in tobacco: Effects of expression cassette configuration and tobacco cultivar used as production platform on recombinant protein yields. Biotechnology for Biofuels, 6, 65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Petersen, K., & Bock, R. (2011). High-level expression of a suite of thermostable cell wall-degrading enzymes from the chloroplast genome. Plant Molecular Biology, 76, 311–321.

    Article  CAS  PubMed  Google Scholar 

  100. Nakahira, Y., Ishikawa, K., Tanaka, K., Tozawa, Y., & Shiina, T. (2013). Overproduction of hyperthermostable beta-1,4-endoglucanase from the archaeon Pyrococcus horikoshii by tobacco chloroplast engineering. Bioscience, Biotechnology, and Biochemistry, 77, 2140–2143.

    Article  CAS  PubMed  Google Scholar 

  101. Verma, D., Kanagaraj, A., Jin, S., Singh, N. D., Kolattukudy, P. E., & Daniell, H. (2010). Chloroplast-derived enzyme cocktails hydrolyse lignocellulosic biomass and release fermentable sugars. Plant Biotechnology Journal, 8, 332–350.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Jin, S., & Daniell, H. (2014). Expression of gamma-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, 12, 1274–1285.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Shintani, D., & DellaPenna, D. (1998). Elevating the vitamin E content of plants through metabolic engineering. Science, 282, 2098–2100.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Arlen, P. A., Singleton, M., Adamovicz, J. J., Ding, Y., Davoodi-Semiromi, A., & Daniell, H. (2008). Effective plague vaccination via oral delivery of plant cells expressing F1-V antigens in chloroplasts. Infection and Immunity, 76, 3640–3650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Chebolu, S., & Daniell, H. (2007). Stable expression of Gal/GalNAc lectin of Entamoeba histolytica in transgenic chloroplasts and immunogenicity in mice towards vaccine development for amoebiasis. Plant Biotechnology Journal, 5, 230–239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Koya, V., Moayeri, M., Leppla, S. H., & Daniell, H. (2005). Plant-based vaccine: Mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infection and Immunity, 73, 8266–8274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Lenzi, P., Scotti, N., Alagna, F., Tornesello, M. L., Pompa, A., Vitale, A., De Stradis, A., Monti, L., Grillo, S., Buonaguro, F. M., Maliga, P., & Cardi, T. (2008). Translational fusion of chloroplast-expressed human papillomavirus type 16 L1 capsid protein enhances antigen accumulation in transplastomic tobacco. Transgenic Research, 17, 1091–1102.

    Article  CAS  PubMed  Google Scholar 

  109. 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 Biotechnology Journal, 5, 495–510.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Zhou, F., Badillo-Corona, J. A., Karcher, D., Gonzalez-Rabade, N., Piepenburg, K., Borchers, A. M., Maloney, A. P., Kavanagh, T. A., Gray, J. C., & Bock, R. (2008). High-level expression of human immunodeficiency virus antigens from the tobacco and tomato plastid genomes. Plant Biotechnology Journal, 6, 897–913.

    Article  CAS  PubMed  Google Scholar 

  111. Daniell, H., Rai, V., & Xiao, Y. (2019). Cold chain and virus-free oral polio booster vaccine made in lettuce chloroplasts confers protection against all three poliovirus serotypes. Plant Biotechnology Journal, 17, 1357–1368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Saba, K., Gottschamel, J., Younus, I., Syed, T., Gull, K., Lossl, A. G., Mirza, B., & Waheed, M. T. (2019). Chloroplast-based inducible expression of ESAT-6 antigen for development of a plant-based vaccine against tuberculosis. Journal of Biotechnology, 305, 1–10.

    Article  CAS  PubMed  Google Scholar 

  113. Chotprakaikiat, W., Allen, A., Bui-Minh, D., Harden, E., Jobsri, J., Cavallo, F., Gleba, Y., Stevenson, F. K., Ottensmeier, C., Klimyuk, V., & Savelyeva, N. (2016). A plant-expressed conjugate vaccine breaks CD4(+) tolerance and induces potent immunity against metastatic Her2(+) breast cancer. Oncoimmunology, 5, e1166323.

    Article  PubMed  PubMed Central  Google Scholar 

  114. McCormick, A. A., Reddy, S., Reinl, S. J., Cameron, T. I., Czerwinkski, D. K., Vojdani, F., Hanley, K. M., Garger, S. J., White, E. L., Novak, J., Barrett, J., Holtz, R. B., Tuse, D., & Levy, R. (2008). Plant-produced idiotype vaccines for the treatment of non-Hodgkin’s lymphoma: Safety and immunogenicity in a phase I clinical study. Proc Natl Acad Sci U S A, 105, 10131–10136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Pinkhasov, J., Alvarez, M. L., Rigano, M. M., Piensook, K., Larios, D., Pabst, M., Grass, J., Mukherjee, P., Gendler, S. J., Walmsley, A. M., & Mason, H. S. (2011). Recombinant plant-expressed tumour-associated MUC1 peptide is immunogenic and capable of breaking tolerance in MUC1.Tg mice. Plant Biotechnology Journal, 9, 991–1001.

    Article  CAS  PubMed  Google Scholar 

  116. Plchova, H., Moravec, T., Hoffmeisterova, H., Folwarczna, J., & Cerovska, N. (2011). Expression of Human papillomavirus 16 E7ggg oncoprotein on N- and C-terminus of potato virus X coat protein in bacterial and plant cells. Protein Expression and Purification, 77, 146–152.

    Article  CAS  PubMed  Google Scholar 

  117. Tran, M., Van, C., Barrera, D. J., Pettersson, P. L., Peinado, C. D., Bui, J., & Mayfield, S. P. (2013). Production of unique immunotoxin cancer therapeutics in algal chloroplasts. Proc Natl Acad Sci U S A, 110, E15-22.

    Article  PubMed  Google Scholar 

  118. Wang, X., Brandsma, M., Tremblay, R., Maxwell, D., Jevnikar, A. M., Huner, N., & Ma, S. (2008). A novel expression platform for the production of diabetes-associated autoantigen human glutamic acid decarboxylase (hGAD65). BMC Biotechnology, 8, 87.

    Article  PubMed  PubMed Central  Google Scholar 

  119. Berhanu, S., Ueda, T., & Kuruma, Y. (2019). Artificial photosynthetic cell producing energy for protein synthesis. Nature Communications, 10, 1325.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Schwander, T., Schada von Borzyskowski, L., Burgener, S., Cortina, N. S., & Erb, T. J. (2016). A synthetic pathway for the fixation of carbon dioxide in vitro. Science, 354, 900–904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Miller, T. E., Beneyton, T., Schwander, T., Diehl, C., Girault, M., McLean, R., Chotel, T., Claus, P., Cortina, N. S., Baret, J. C., & Erb, T. J. (2020). Light-powered CO2 fixation in a chloroplast mimic with natural and synthetic parts. Science, 368, 649–654.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Singh, N. D., Li, M., Lee, S. B., Schnell, D., & Daniell, H. (2008). Arabidopsis Tic40 expression in tobacco chloroplasts results in massive proliferation of the inner envelope membrane and upregulation of associated proteins. The Plant Cell, 20, 3405–3417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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R.S and S.D. conceived and designed the review. R.S., R.P., and S.D. wrote and revised the manuscript.

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Singhal, R., Pal, R. & Dutta, S. Chloroplast Engineering: Fundamental Insights and Its Application in Amelioration of Environmental Stress. Appl Biochem Biotechnol 195, 2463–2482 (2023). https://doi.org/10.1007/s12010-022-03930-8

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