Abstract
Although organelle (mitochondria and plastid) genomes have less than 1% of the genes in the nucleus, they encode essential genes, such as those involved in energy production, respiration, and photosynthesis, and genes that control agronomically important characteristics such as cytoplasmic male sterility. Organelle genomes have high copy numbers in each cell (one to two orders of magnitude greater than in the nucleus) and are characterized by maternal inheritance. To know functions of genes encoded in the organelle genomes or to develop new plants adapted to various severe environments, genetic engineering of organelle genomes is one of the promising approaches. However, modifying the mitochondrial or plastid genomes in rice is presently impossible or difficult. Here, we discuss the characteristic features of these genomes and recent attempts at plastid transformation.
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References
Ahmadabadi M, Ruf S, Bock R (2007) A leaf-based regeneration and transformation system for maize (Zea mays L.) Transgenic Res 16:437–448. https://doi.org/10.1007/s11248-006-9046-y
Akagi H, Sakamoto M, Shinjyo C, Shimada H, Fujimura T (1994) A unique sequence located downstream from the rice mitochondrial atp6 may cause male sterility. Curr Genet 25(1):52–58
Asaf S, Khan AL, Khan AR, Waqas M, Kang SM, Khan MA, Shahzad R, Seo CW, Shin JH, Lee IJ (2016) Mitochondrial genome analysis of wild rice (Oryza minuta) and its comparison with other related species. Plos One 11(4):e0152937. https://doi.org/10.1371/journal.pone.0152937
Asaf S, Waqas M, Khan AL, Khan MA, Kang S-M, Imran QM, Shahzad R, Bilal S, Yun B-W, Lee I-J (2017) The complete chloroplast genome of wild Rice (Oryza minuta) and its comparison to related species. Front Plant Sci 8:1–15. https://doi.org/10.3389/fpls.2017.00304
Barone P, Zhang XH, Widholm JM (2009) Tobacco plastid transformation using the feedback-insensitive anthranilate synthase [??]-subunit of tobacco (ASA2) as a new selectable marker. J Exp Bot 60:3195–3202. https://doi.org/10.1093/jxb/erp160
Bellucci M, De Marchis F, Ferradini N, Pompa A, Veronesi F, Rosellini D (2015) A mutant Synechococcus gene encoding glutamate 1-semialdehyde aminotransferase confers gabaculine resistance when expressed in tobacco plastids. Plant Cell Rep 34:2127–2136. https://doi.org/10.1007/s00299-015-1856-z
Bentolila S, Stefanov S (2012) A reevaluation of rice mitochondrial evolution based on the complete sequence of male-fertile and male-sterile mitochondrial genomes. Plant Physiol 158(2):996–1017. https://doi.org/10.1104/pp.111.190231
Bock R (2007) Towards plastid transformation in maize. News Rep 6:2–5
Bogdanove AJ, Voytas DF (2011) TAL effectors: customizable proteins for DNA targeting. Science 333:1843–1846. https://doi.org/10.1126/science.1204094
Brar DS, Khush GS (1997) Alien introgression in rice. Plant Mol Biol 35:35–47. https://doi.org/10.1023/A:1005825519998
Civáň P, Craig H, Cox CJ, Brown TA (2015) Three geographically separate domestications of Asian rice. Nat Plants 1:15164. https://doi.org/10.1038/nplants.2015.164
Clarke JL, Daniell H (2011) Plastid biotechnology for crop production: present status and future perspectives. Plant Mol Biol 76:211–220. https://doi.org/10.1007/s11103-011-9767-z
Daniell H, Khan MS, Allison L (2002) Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology. Trends Plant Sci 7:84–91. https://doi.org/10.1016/S1360-1385(01)02193-8
Daniell H, Lin C-S, Yu M, Chang W-J (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol 17:134. https://doi.org/10.1186/s13059-016-1004-2
Doyle JJ, Davis JI, Soreng RJ, Garvin D, Anderson MJ (1992) Chloroplast DNA inversions and the origin of the grass family (Poaceae). Proc Natl Acad Sci U S A 89:7722–7726. https://doi.org/10.1073/pnas.89.16.7722
Dunne A, Maple-Grødem J, Gargano D, Haslam RP, Napier JA, Chua NH, Russell R, Møller SG (2014) Modifying fatty acid profiles through a new cytokinin-based plastid transformation system. Plant J 80:1131–1138. https://doi.org/10.1111/tpj.12684
Fromm H, Edelman M, Aviv D, Galun E (1987) The molecular basis for rRNA-dependent spectinomycin resistance in Nicotiana chloroplasts. EMBO J 6:3233–3237
Fujii S, Kazama T, Yamada M, Toriyama K (2010) Discovery of global genomic re-organization based on comparison of two newly sequenced rice mitochondrial genomes with cytoplasmic male sterility-related genes. BMC Genomics 11:209. https://doi.org/10.1186/1471-2164-11-209
Ge S, Sang T, Lu BR, Hong DY (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc Natl Acad Sci U S A 96:14400–14405. https://doi.org/10.1073/pnas.96.25.14400
Gonzalez A, Jimenez A, Vazquez D, Davies JE, Schindler D (1978) Studies on the mode of action of hygromycin B, an inhibitor of translocation in eukaryotes. Biochim Biophys Acta 521:459–469
Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16(Suppl):S154–S169. https://doi.org/10.1105/tpc.015966
Hanson MR, Gray BN, Ahner BA (2013) Chloroplast transformation for engineering of photosynthesis. J Exp Bot 64:731–742
Hiei Y, Komari T (2008) Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat Protoc 3:824–834. https://doi.org/10.1038/nprot.2008.46
Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. MGG Mol Gen Genet 217:185–194. https://doi.org/10.1007/BF02464880
Huang X, Han B (2015) Rice domestication occurred through single origin and multiple introgressions. Nat Plants 2:15207. https://doi.org/10.1038/nplants.2015.207
Huang X, Kurata N, Wei X, Wang Z-X, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W, Guo Y, Lu Y, Zhou C, Fan D, Weng Q, Zhu C, Huang T, Zhang L, Wang Y, Feng L, Furuumi H, Kubo T, Miyabayashi T, Yuan X, Xu Q, Dong G, Zhan Q, Li C, Fujiyama A, Toyoda A, Lu T, Feng Q, Qian Q, Li J, Han B (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501. https://doi.org/10.1038/nature11532
Igarashi K, Kazama T, Motomura K, Toriyama K (2013) Whole genomic sequencing of RT98 mitochondria derived from Oryza rufipogon and northern blot analysis to uncover a cytoplasmic male sterility-associated gene. Plant Cell Physiol 54(2):237–243. https://doi.org/10.1093/pcp/pcs177
International Rice Genome Sequencing P (2005) The map-based sequence of the rice genome. Nature 436(7052):793–800. https://doi.org/10.1038/nature03895
Iwabuchi M, Kyozuka J, Shimamoto K (1993) Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J 12(4):1437–1446
Iwahashi M, Nakazono M, Kanno A, Sugino K, Ishibashi T, Hirai A (1992) Genetic and physical maps and a clone bank of mitochondrial DNA from rice. Theor Appl Genet 84(3-4):275–279. https://doi.org/10.1007/BF00229482
Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee S-B, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci U S A 104:19369–19374. https://doi.org/10.1073/pnas.0709121104
Jin S, Daniell H (2015) The engineered chloroplast genome just got smarter. Trends Plant Sci 20:622–640. https://doi.org/10.1016/j.tplants.2015.07.004
Jin S, Singh ND, Li L, Zhang X, Daniell H (2015) 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 Biotechnol J 13:435–446. https://doi.org/10.1111/pbi.12355
Katayama H, Ogihara Y (1996) Phylogenetic affinities of the grasses to other monocots as revealed by molecular analysis of chloroplast DNA. Curr Genet 29:572–581. https://doi.org/10.1007/s002940050087
Kazama T, Toriyama K (2016) Whole mitochondrial genome sequencing and re-examination of a cytoplasmic male sterility-associated gene in Boro-Taichung-type cytoplasmic male sterile Rice. PLoS One 11(7):e0159379. https://doi.org/10.1371/journal.pone.0159379
Khan MS (2012) Plastid genome engineering in plants: present status and future trends. Mol Plant Breed 3:91–102. https://doi.org/10.5376/mpb.2012.03.0009
Khan MS, Maliga P (1999) Fluorescent antibiotic resistance marker for tracking plastid transformation in higher plants. Nat Biotechnol 17:910–915. https://doi.org/10.1038/12907
Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34. https://doi.org/10.1023/A:1005810616885
Kim K, Lee S-C, Lee J, Yu Y, Yang K, Choi B-S, Koh H-J, Waminal NE, Choi H-I, Kim N-H, Jang W, Park H-S, Lee J, Lee HO, Joh HJ, Lee HJ, Park JY, Perumal S, Jayakodi M, Lee YS, Kim B, Copetti D, Kim S, Kim S, Lim K-B, Kim Y-D, Lee J, Cho K-S, Park B-S, Wing RA, Yang T-J (2015) Complete chloroplast and ribosomal sequences for 30 accessions elucidate evolution of Oryza AA genome species. Sci Rep 5:15655. https://doi.org/10.1038/srep15655
Kumar S, Hahn FM, Baidoo E, Kahlon TS, Wood DF, McMahan CM, Cornish K, Keasling JD, Daniell H, Whalen MC (2012) Remodeling the isoprenoid pathway in tobacco by expressing the cytoplasmic mevalonate pathway in chloroplasts. Metab Eng 14:19–28. https://doi.org/10.1016/j.ymben.2011.11.005
Lee SM, Kang K, Chung H, Yoo SH, Xu XM, Lee S-B, Cheong J-J, Daniell H, Kim M (2006) Plastid transformation in the monocotyledonous cereal crop, rice (Oryza sativa) and transmission of transgenes to their progeny. Mol Cell 21:401–410. doi: 987 [pii]
Li Y, Sun B, Su N, Meng X, Zhang Z, Shen G (2009) Establishment of a gene expression system in rice chloroplast and obtainment of PPT-resistant rice plants. Agric Sci China 8:643–651. https://doi.org/10.1016/S1671-2927(08)60259-X
Li W, Ruf S, Bock R (2011a) Chloramphenicol acetyltransferase as selectable marker for plastid transformation. Plant Mol Biol 76:443–451. https://doi.org/10.1007/s11103-010-9678-4
Li ZM, Zheng XM, Ge S (2011b) Genetic diversity and domestication history of African rice (Oryza glaberrima) as inferred from multiple gene sequences. Theor Appl Genet 123:21–31. https://doi.org/10.1007/s00122-011-1563-2
Li D, Tang N, Fang Z, Xia Y, Cao M (2016a) Co-transfer of TALENs construct targeted for chloroplast genome and chloroplast transformation vector into rice using particle bombardment. J Nanosci Nanotechnol 16:12194–12201. https://doi.org/10.1166/jnn.2016.12949
Li D, Tang N, Liu M, Shen C, Hu Y, Xia Y, Cao M (2016b) Using hygromycin phosphotransferase and enhanced green fluorescent protein genes for tracking plastid transformation in Rice (Oryza sativa L.) via gold particle bombardment. Nanosci Nanotechnol Lett 8:409–417. https://doi.org/10.1166/nnl.2016.2153
Liebers M, Grübler B, Chevalier F, Lerbs-Mache S, Merendino L, Blanvillain R, Pfannschmidt T (2017) Regulatory shifts in plastid transcription play a key role in morphological conversions of plastids during plant development. Front Plant Sci 8:23. https://doi.org/10.3389/fpls.2017.00023
Lin MT, Occhialini A, Andralojc PJ, Parry MAJ, Hanson MR (2014) A faster Rubisco with potential to increase photosynthesis in crops. Nature 513:547–550. https://doi.org/10.1038/nature13776
Londo JP, Chiang Y-C, Hung K, Chiang T, Schaal BA (2006) Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc Natl Acad Sci U S A 103:9578–9583. https://doi.org/10.1073/pnas.0603152103
Lutz KA, Azhagiri AK, Tungsuchat-Huang T, Maliga P (2007) A guide to choosing vectors for transformation of the plastid genome of higher plants. Plant Physiol 145:1201–1210. https://doi.org/10.1104/pp.107.106963
Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A 101:12404–12410. https://doi.org/10.1073/pnas.0403715101
Maliga P, Bock R (2011) Plastid biotechnology: food, fuel, and medicine for the 21st century. Plant Physiol 155:1501–1510. https://doi.org/10.1104/pp.110.170969
Molina J, Sikora M, Garud N, Flowers JM, Rubinstein S, Reynolds A, Huang P, Jackson S, Schaal BA, Bustamante CD, Boyko AR, Purugganan MD (2011) Molecular evidence for a single evolutionary origin of domesticated rice. Proc Natl Acad Sci U S A 108:8351–8356. https://doi.org/10.1073/pnas.1104686108
Nock CJ, Waters DLE, Edwards MA, Bowen SG, Rice N, Cordeiro GM, Henry RJ (2011) Chloroplast genome sequences from total DNA for plant identification. Plant Biotechnol J 9:328–333. https://doi.org/10.1111/j.1467-7652.2010.00558.x
Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Gen Genomics 268(4):434–445. https://doi.org/10.1007/s00438-002-0767-1
Okazaki M, Kazama T, Murata H, Motomura K, Toriyama K (2013) Whole mitochondrial genome sequencing and transcriptional analysis to uncover an RT102-type cytoplasmic male sterility-associated candidate gene derived from Oryza rufipogon. Plant Cell Physiol 54(9):1560–1568. https://doi.org/10.1093/pcp/pct102
Pyke K (2007) Plastid biogenesis and differentiation. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Berlin, pp 1–28
Rigano MM, Scotti N, Cardi T (2012) Unsolved problems in plastid transformation © 2012 Landes Bioscience. © 2012 Landes Bioscience. Do not distribute. 1–5
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. https://doi.org/10.1104/pp.109.152017
Sakai A, Suzuki T, Miyazawa Y, Kawano S, Nagata T, Kuroiwa T (1998) Comparative analysis of plastid gene expression in tobacco chloroplasts and proplastids: relationship between transcription and transcript accumulation. Plant Cell Physiol 39:581–589. https://doi.org/10.1093/oxfordjournals.pcp.a029408
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. https://doi.org/10.1007/s00122-007-0567-4
Scotti N, Cardi T (2012) Plastid transformation as an expression tool for plant-derived biopharmaceuticals. In: Dunwell JM, Wetten AC (eds) Transgenic plants: methods and protocols, methods in molecular biology. Humana Press, Totowa, pp 451–466
Shimada H, Sugiura M (1991) Fine-structural features of the chloroplast genome – comparison of the sequenced chloroplast genomes. Nucleic Acids Res 19:983–995. https://doi.org/10.1093/nar/19.5.983
Sikdar SR, Serino G, Chaudhuri S, Maliga P (1998) Plastid transformation in Arabidopsis thaliana. Plant Cell Rep 18:20–24. https://doi.org/10.1007/s002990050525
Silhavy D, Maliga P (1998) Plastid promoter utilization in a rice embryogenic cell culture. Curr Genet 34:67–70. https://doi.org/10.1007/s002940050367
Stupar RM, Lilly JW, Town CD, Cheng Z, Kaul S, Buell CR, Jiang J (2001) Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci U S A 98(9):5099–5103. https://doi.org/10.1073/pnas.091110398
Svab Z, Hajdukiewicz P, Maliga P (1990) Stable transformation of plastids in higher plants. Proc Natl Acad Sci U S A 87:8526–8530. https://doi.org/10.1073/pnas.87.21.8526
Tian X, Zheng J, Hu S, Yu J (2006) The rice mitochondrial genomes and their variations. Plant Physiol 140(2):401–410. https://doi.org/10.1104/pp.105.070060
Tong W, Kim T-S, Park Y-J (2016) Rice chloroplast genome variation architecture and phylogenetic dissection in diverse Oryza species assessed by whole-genome resequencing. Rice (N Y) 9:57. https://doi.org/10.1186/s12284-016-0129-y
Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15(1):57–61. https://doi.org/10.1038/ng0197-57
Vaughan DA, Lu BR, Tomooka N (2008) The evolving story of rice evolution. Plant Sci 174:394–408. https://doi.org/10.1016/j.plantsci.2008.01.016
Vera A, Sugiura M (1995) Chloroplast rRNA transcription from structurally different tandem promoters: an additional novel-type promoter. Curr Genet 27:280–284. https://doi.org/10.1007/BF00326161
Verma D, Daniell H (2007) Chloroplast vector systems for biotechnology applications. Plant Physiol 145:1129–1143. https://doi.org/10.1104/pp.107.106690
Vitte C, Ishii T, Lamy F, Brar D, Panaud O (2004) Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.) Mol Gen Genomics 272:504–511. https://doi.org/10.1007/s00438-004-1069-6
Wambugu PW, Brozynska M, Furtado A, Waters DL, Henry RJ (2015) Relationships of wild and domesticated rices (Oryza AA genome species) based upon whole chloroplast genome sequences. Sci Rep 5:13957. https://doi.org/10.1038/srep13957
Wang M, Yu Y, Haberer G, Marri PR, Fan C, Goicoechea JL, Zuccolo A, Song X, Kudrna D, Ammiraju JSS, Cossu RM, Maldonado C, Chen J, Lee S, Sisneros N, de Baynast K, Golser W, Wissotski M, Kim W, Sanchez P, Ndjiondjop M-N, Sanni K, Long M, Carney J, Panaud O, Wicker T, Machado CA, Chen M, Mayer KFX, Rounsley S, Wing RA (2014) The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nat Genet 46:982–988. https://doi.org/10.1038/ng.3044
Wani SH, Sah SK, Sági L, Solymosi K (2015) Transplastomic plants for innovations in agriculture. A review. Agron Sustain Dev 35:1391–1430. https://doi.org/10.1007/s13593-015-0310-5
Waters DLE, Nock CJ, Ishikawa R, Rice N, Henry RJ (2012) Chloroplast genome sequence confirms distinctness of Australian and Asian wild rice. Ecol Evol 2:211–217. https://doi.org/10.1002/ece3.66
Wyman C, Kanaar R (2006) DNA double-strand break repair: all’s well that ends well. Annu Rev Genet 40:363–383. https://doi.org/10.1146/annurev.genet.40.110405.090451
Xu JH, Liu Q, Hu W, Wang T, Xue Q, Messing J (2015) Dynamics of chloroplast genomes in green plants. Genomics 106:221–231. https://doi.org/10.1016/j.ygeno.2015.07.004
Yang CC, Kawahara Y, Mizuno H, Wu J, Matsumoto T, Itoh T (2012) Independent domestication of Asian rice followed by gene flow from japonica to indica. Mol Biol Evol 29:1471–1479. https://doi.org/10.1093/molbev/msr315
Yu Q, Lutz KA, Maliga P (2017) Efficient plastid transformation in arabidopsis. Plant Physiol 175(1):186–193
Zhang TW, Hu SN, Zhang GY, Pan LL, Zhang XW, Al-Mssallem IS, Yu J (2012) The organelle genomes of hassawi rice (Oryza sativa L.) and its hybrid in Saudi Arabia: genome variation, rearrangement, and origins. Plos One 7(7):e42041. https://doi.org/10.1371/journal.pone.0042041
Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R (2015) Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347:991. LP-994
Zhang B, Shanmugaraj B, Daniell H (2017) Expression and functional evaluation of biopharmaceuticals made in plant chloroplasts. Curr Opin Chem Biol 38:17–23. https://doi.org/10.1016/j.cbpa.2017.02.007
Zhu Q, Ge S (2005) Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol 167:249–265. https://doi.org/10.1111/j.1469-8137.2005.01406.x
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This work is supported by grants, PRESTO-Sakigake from the Japanese Science and Technology Agency (JPMJPR12B2 to SA) and Kakenhi from the Japanese society for the promotion of Science (16H06182 to TK and 16K14827 to SA).
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Kazama, T., Nishimura, A., Arimura, Si. (2018). Rice Organelle Genomics: Approaches to Genetic Engineering and Breeding. In: Sasaki, T., Ashikari, M. (eds) Rice Genomics, Genetics and Breeding. Springer, Singapore. https://doi.org/10.1007/978-981-10-7461-5_4
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