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Comparative Chloroplast Genome Analysis of Single-Cell C4 Bienertia Sinuspersici with Other Amaranthaceae Genomes

Received: 15 August 2018     Accepted: 31 August 2018     Published: 26 September 2018
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Abstract

Bienertia sinuspersici is a single-cell C4 (SCC4) plant species whose photosynthetic mechanisms occur in two cytoplasmic compartments containing central and peripheral chloroplasts. The efficiency of the C4 photosynthetic pathway to suppress photorespiration and enhance carbon gain has led to a growing interest in its research. A comparative analysis of B. sinuspersici chloroplast genome with other genomes of Amaranthaceae was conducted. Results from a 70% cut off sequence identity showed that B. sinuspersici is closely related to Beta vulgaris with slight variations in the arrangement of few genes such ycf1 and ycf15; and, the absence of psbB in Beta vulgaris. B. sinuspersici has the largest 153, 472 bp while Spinacea oleracea has the largest protein-coding sequence 6,754 bp larger than B. sinuspersici. The GC contents of each of the species ranges from 36.3 to 36.9% with B. sinuspersici having the same GC percentage as Haloxylon persicum and H. ammodendron (36.6%). The IR size also varies yet in all six species, the Ira/LSC border is generally located upstream of the trnH-GUG gene. A total of 107 tandem repeats were found in each of the species, most of which are situated in the intergenic space. These results provide basic information that may be valuable for future related studies.

Published in Journal of Plant Sciences (Volume 6, Issue 4)
DOI 10.11648/j.jps.20180604.13
Page(s) 134-143
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2018. Published by Science Publishing Group

Keywords

Bienertia Sinuspersici, Single-Cell C4, Central and Peripheral Chloroplasts, Comparative Anaylysis, Tandem Repeats

References
[1] Sugiura, M. (1992) The chloroplast genome. Plant molecular biology, 19(1), 149-168.
[2] Tiller, N. and Bock, R. (2014). The translational apparatus of plastids and its role in plant development. Molecular plant, 7(7), 1105-1120.
[3] Raman, G. and Park, S. (2015) Analysis of the complete chloroplast genome of a medicinal plant, Dianthus superbus var. longicalyncinus, from a comparative genomics perspective. PLoS One, 10(10), e0141329.
[4] Grabsztunowicz, M., Koskela, M. M. and Mulo, P. (2017) Post-translational modifications in regulation of chloroplast function: Recent advances. Frontiers in plant science, 8, 240.
[5] Bendich, A. J. (1987) Why do chloroplasts and mitochondria contain so many copies of their genome?. BioEssays, 6(6), 279-282.
[6] Yang, Y., Yuanye, D., Qing, L., Jinjian, L., Xiwen, L. and Yitao, W. (2014) Complete chloroplast genome sequence of poisonous and medicinal plant Datura stramonium: organizations and implications for genetic engineering. PLoS One, 9(11), e110656.
[7] Furbank, R. T. and Taylor, W. C. (1995). Regulation of photosynthesis in C3 and C4 plants: a molecular approach. The Plant Cell, 7(7), 797.
[8] Offermann, S., Okita, T. W. and Edwards, G. E. (2011) How do single cell C4 species form dimorphic chloroplasts?. Plant signaling & behavior, 6(5), 762-765.
[9] Voznesenskaya, E. V., Franceschi, V. R., Kiirats, O., Artyusheva, E. G., Freitag, H. and Edwards, G. E. (2002) Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). The Plant Journal, 31(5), 649-662.
[10] Akhani, H., Barroca, J., Koteeva, N., Voznesenskaya, E., Franceschi, V., Edwards, G. … and Ziegler, H. (2005) Bienertia sinuspersici (Chenopodiaceae): a new species from Southwest Asia and discovery of a third terrestrial C4 plant without Kranz anatomy. Systematic Botany, 30(2), 290-301.
[11] Lara, M. V., Offermann, S., Smith, M., Okita, T. W., Andreo, C. S. and Edwards, G. E. (2008) Leaf development in the single-cell C4 system in Bienertia sinuspersici: expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions. Plant physiology, 148(1), 593-610.
[12] Voznesenskaya, E. V., Koteyeva, N. K., Chuong, S. D., Akhani, H., Edwards, G. E. and Franceschi, V. R. (2005) Differentiation of cellular and biochemical features of the single‐cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). American Journal of Botany, 92(11), 1784-1795.
[13] Chuong, S. D., Franceschi, V. R. and Edwards, G. E. (2006) The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. The Plant Cell, 18(9), 2207-2223.
[14] Bräutigam, A. and Gowik, U. (2016) Photorespiration connects C3 and C4 photosynthesis. Journal of experimental botany, 67(10), 2953-2962.
[15] Gowik, U. and Westhoff, P. (2011) The path from C3 to C4 photosynthesis. Plant Physiology, 155(1), 56-63.
[16] Offermann, S., Okita, T. W. and Edwards, G. E. (2011) Resolving the compartmentation and function of C4 photosynthesis in the single-cell C4 species Bienertia sinuspersici. Plant physiology, 155(4), 1612-1628.
[17] Aubry, S., Brown, N. J. and Hibberd, J. M. (2011) The role of proteins in C3 plants prior to their recruitment into the C4 pathway. Journal of experimental botany, 62(9), 3049-3059.
[18] Furbank, R. T. (2011) Evolution of the C4 photosynthetic mechanism: are there really three C4 acid decarboxylation types?. Journal of experimental botany, 62(9), 3103-3108.
[19] Kajala, K., Covshoff, S., Karki, S., Woodfield, H., Tolley, B. J., Dionora, M. J. A., … and Quick, W. P. (2011) Strategies for engineering a two-celled C4 photosynthetic pathway into rice. Journal of experimental botany, 62(9), 3001-3010.
[20] Miyao, M., Masumoto, C., Miyazawa, S. I. and Fukayama, H. (2011) Lessons from engineering a single-cell C4 photosynthetic pathway into rice. Journal of experimental botany, 62(9), 3021-3029.
[21] Nelson, T. (2011) The grass leaf developmental gradient as a platform for a systems understanding of the anatomical specialization of C4 leaves. Journal of experimental botany, 62(9), 3039-3048.
[22] Peterhansel, C. (2011) Best practice procedures for the establishment of a C4 cycle in transgenic C3 plants. Journal of experimental botany, 62(9), 3011-3019.
[23] Sage, R. F. and Zhu, X. G. (2011) Exploiting the engine of C4 photosynthesis. Journal of experimental botany, 62(9), 2989-3000.
[24] Mitchell, P. L. and Sheehy, J. E. (2006) Supercharging rice photosynthesis to increase yield. New Phytologist, 171(4), 688-693.
[25] Hibberd, J. M., Sheehy, J. E. and Langdale, J. A. (2008) Using C4 photosynthesis to increase the yield of rice—rationale and feasibility. Current opinion in plant biology, 11(2), 228-231.
[26] Dawe, D., Pandey, S. and Nelson, A. (2010) Emerging trends and spatial patterns of rice production. Rice in the Global Economy: Strategic Research and Policy Issues for Food Security. Los Baños, Philippines: International Rice Research Institute (IRRI).
[27] Zhu, X. G., Long, S. P. and Ort, D. R. (2010) Improving photosynthetic efficiency for greater yield. Annual review of plant biology, 61, 235-261.
[28] Myers, E. W., Sutton, G. G., Delcher, A. L., Dew, I. M., Fasulo, D. P., Flanigan, M. J., ... and Anson, E. L. (2000) A whole-genome assembly of Drosophila. Science, 287(5461), 2196-2204.
[29] Lohse, M., Drechsel, O. and Bock, R. (2007) OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Current genetics, 52(5-6), 267-274.
[30] Kim, B., Kim, J., Park, H. and Park, J. (2016) The complete chloroplast genome sequence of Bienertia sinuspersici. Mitochondrial DNA Part B, 1(1), 388-389.
[31] Li, H., Cao, H., Cai, Y. F., Wang, J. H., Qu, S. P. and Huang, X. Q. (2014) The complete chloroplast genome sequence of sugar beet (Beta vulgaris ssp. vulgaris).
[32] Dong, W., Xu, C., Li, D., Jin, X., Li, R., Lu, Q. and Suo, Z. (2016) Comparative analysis of the complete chloroplast genome sequences in psammophytic Haloxylon species (Amaranthaceae). PeerJ, 4, e2699.
[33] Schmitz-Linneweber, C., Maier, R. M., Alcaraz, J. P., Cottet, A., Herrmann, R. G. and Mache, R. (2001) The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization. Plant Molecular Biology, 45(3), 307-315.
[34] Benson, G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic acids research, 27(2), 573.
[35] Suzuki, J. Y., Sriraman, P., Svab, Z. and Maliga, P. (2003) Unique architecture of the plastid ribosomal RNA operon promoter recognized by the multisubunit RNA polymerase in tobacco and other higher plants. The Plant Cell, 15(1), 195-205.
[36] Zhang, J. (2003) Evolution by gene duplication: an update. Trends in ecology & evolution, 18(6), 292-298.
[37] Kondrashov, F. A. and Kondrashov, A. S. (2006) Role of selection in fixation of gene duplications. Journal of Theoretical Biology, 239(2), 141-151.
[38] Cotton, J. A. (2008) The impact of gene duplication on human genome evolution. eLS.
[39] Freeling, M. and Subramaniam, S. (2009) Conserved noncoding sequences (CNSs) in higher plants. Current opinion in plant biology, 12(2), 126-132.
[40] Guo, H. and Moose, S. P. (2003) Conserved noncoding sequences among cultivated cereal genomes identify candidate regulatory sequence elements and patterns of promoter evolution. The Plant Cell, 15(5), 1143-1158.
[41] Thomas, B. C., Rapaka, L., Lyons, E., Pedersen, B., and Freeling, M. (2007) Arabidopsis intragenomic conserved noncoding sequence. Proceedings of the National Academy of Sciences, 104(9), 3348-3353.
[42] Bock, R. (2007) Structure, function, and inheritance of plastid genomes. In Cell and molecular biology of plastids (pp. 29-63). Springer Berlin Heidelberg.
[43] Delannoy, E., Fujii, S., Colas des Francs-Small, C., Brundrett, M. and Small, I. (2011) Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Molecular Biology and Evolution, 28(7), 2077-2086.
[44] Keller, J., Rousseau-Gueutin, M., Martin, G. E., Morice, J., Boutte, J., Coissac, E., ... and Aïnouche, A. (2017) The evolutionary fate of the chloroplast and nuclear rps16 genes as revealed through the sequencing and comparative analyses of four novel legume chloroplast genomes from Lupinus. DNA Research, 24(4), 343-358.
[45] Allen, J. F., Puthiyaveetil, S., Ström, J. and Allen, C. A. (2005) Energy transduction anchors genes in organelles. Bioessays, 27(4), 426-435.
[46] Maier, U. G., Zauner, S., Woehle, C., Bolte, K., Hempel, F., Allen, J. F. and Martin, W. F. (2013) Massively convergent evolution for ribosomal protein gene content in plastid and mitochondrial genomes. Genome biology and evolution, 5(12), 2318-2329.
[47] Deno, H. and Sugiura, M. (1984) Chloroplast tRNAGly gene contains a long intron in the D stem: Nucleotide sequences of tobacco chloroplast genes for tRNAGly (UCC) and tRNAArg (UCU). Proceedings of the National Academy of Sciences, 81(2), 405-408.
[48] Downie, S. R., Olmstead, R. G., Zurawski, G., Soltis, D. E., Soltis, P. S., Watson, J. C. and Palmer, J. D. (1991) Six independent losses of the chloroplast DNA rpl2 intron in dicotyledons: molecular and phylogenetic implications. Evolution, 45(5), 1245-1259.
[49] Logacheva, M. D., Samigullin, T. H., Dhingra, A. and Penin, A. A. (2008) Comparative chloroplast genomics and phylogenetics of Fagopyrum esculentum ssp. ancestrale–a wild ancestor of cultivated buckwheat. BMC Plant Biology, 8(1), 59.
[50] Rock, C. D., Barkan, A. and Taylor, W. C. (1987) The maize plastid psbB-psbF-petB-petD gene cluster: spliced and unspliced petB and petD RNAs encode alternative products. Current genetics, 12(1), 69-77.
[51] Jo, B. S. and Choi, S. S. (2015) Introns: the functional benefits of introns in genomes. Genomics & informatics, 13(4), 112-118.
[52] Gruss, P., Lai, C. J., Dhar, R. and Khoury, G. (1979) Splicing as a requirement for biogenesis of functional 16S mRNA of simian virus 40. Proceedings of the National Academy of Sciences, 76(9), 4317-4321.
[53] Callis, J., Fromm, M. and Walbot, V. (1987) Introns increase gene expression in cultured maize cells. Genes & development, 1(10), 1183-1200.
[54] Beaulieu, E., Green, L., Elsby, L., Alourfi, Z., Morand, E. F., Ray, D. W. and Donn, R. (2011) Identification of a novel cell type‐specific intronic enhancer of macrophage migration inhibitory factor (MIF) and its regulation by mithramycin. Clinical & Experimental Immunology, 163(2), 178-188.
[55] Sorek, R. and Ast, G. (2003) Intronic sequences flanking alternatively spliced exons are conserved between human and mouse. Genome Research, 13(7), 1631-1637.
[56] Pan, Q., Shai, O., Lee, L. J., Frey, B. J. and Blencowe, B. J. (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nature genetics, 40(12), 1413.
[57] Roy, M., Kim, N., Xing, Y. and Lee, C. (2008) The effect of intron length on exon creation ratios during the evolution of mammalian genomes. Rna, 14(11), 2261-2273.
[58] Valencia, P., Dias, A. P. and Reed, R. (2008) Splicing promotes rapid and efficient mRNA export in mammalian cells. Proceedings of the National Academy of Sciences, 105(9), 3386-3391.
[59] Schwartz, S., Meshorer, E., & Ast, G. (2009). Chromatin organization marks exon-intron structure. Nature Structural and Molecular Biology, 16(9), 990.
[60] Spies, N., Nielsen, C. B., Padgett, R. A. and Burge, C. B. (2009) Biased chromatin signatures around polyadenylation sites and exons. Molecular cell, 36(2), 245-254.
[61] Tutar, Y. (2012). Pseudogenes. Comparative and functional genomics, 2012.
[62] Dong, W., Xu, C., Cheng, T. and Zhou, S. (2013) Complete chloroplast genome of Sedum sarmentosum and chloroplast genome evolution in Saxifragales. PLoS One, 8(10), e77965.
[63] Millen, R. S., Olmstead, R. G., Adams, K. L., Palmer, J. D., Lao, N. T., Heggie, L., ... and Calie, P. J. (2001) Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. The Plant Cell, 13(3), 645-658.
[64] Christopher, D. A., Cushman, J. C., Price, C. A. and Hallick, R. B. (1988) Organization of ribosomal protein genes rp123, rp12, rps19, rp122 and rps3 on the Euglena gracilis chloroplast genome. Current genetics, 14(3), 275-286.
[65] Thomson, W. W. and Whatley, J. M. (1980) Development of nongreen plastids. Annual Review of Plant Physiology, 31(1), 375-394.
[66] Steane, D. A. (2005) Complete nucleotide sequence of the chloroplast genome from the Tasmanian blue gum, Eucalyptus globulus (Myrtaceae). DNA Research, 12(3), 215-220.
[67] Palmer, J. D. and Thompson, W. F. (1982) Chloroplast DNA rearrangements are more frequent when a large inverted repeat sequence is lost. Cell, 29(2), 537-550.
[68] Perry, A. S. and Wolfe, K. H. (2002) Nucleotide substitution rates in legume chloroplast DNA depend on the presence of the inverted repeat. Journal of Molecular Evolution, 55(5), 501-508.
[69] Liu, X. Q., Gillham, N. W. and Boynton, J. E. (1989) Chloroplast ribosomal protein gene rps12 of Chlamydomonas reinhardtii. Wild-type sequence, mutation to streptomycin resistance and dependence, and function in Escherichia coli. Journal of Biological Chemistry, 264(27), 16100-16108.
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  • APA Style

    Lorrenne Caburatan, Jin Gyu Kim, Joonho Park. (2018). Comparative Chloroplast Genome Analysis of Single-Cell C4 Bienertia Sinuspersici with Other Amaranthaceae Genomes. Journal of Plant Sciences, 6(4), 134-143. https://doi.org/10.11648/j.jps.20180604.13

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    ACS Style

    Lorrenne Caburatan; Jin Gyu Kim; Joonho Park. Comparative Chloroplast Genome Analysis of Single-Cell C4 Bienertia Sinuspersici with Other Amaranthaceae Genomes. J. Plant Sci. 2018, 6(4), 134-143. doi: 10.11648/j.jps.20180604.13

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    AMA Style

    Lorrenne Caburatan, Jin Gyu Kim, Joonho Park. Comparative Chloroplast Genome Analysis of Single-Cell C4 Bienertia Sinuspersici with Other Amaranthaceae Genomes. J Plant Sci. 2018;6(4):134-143. doi: 10.11648/j.jps.20180604.13

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  • @article{10.11648/j.jps.20180604.13,
      author = {Lorrenne Caburatan and Jin Gyu Kim and Joonho Park},
      title = {Comparative Chloroplast Genome Analysis of Single-Cell C4 Bienertia Sinuspersici with Other Amaranthaceae Genomes},
      journal = {Journal of Plant Sciences},
      volume = {6},
      number = {4},
      pages = {134-143},
      doi = {10.11648/j.jps.20180604.13},
      url = {https://doi.org/10.11648/j.jps.20180604.13},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.jps.20180604.13},
      abstract = {Bienertia sinuspersici is a single-cell C4 (SCC4) plant species whose photosynthetic mechanisms occur in two cytoplasmic compartments containing central and peripheral chloroplasts. The efficiency of the C4 photosynthetic pathway to suppress photorespiration and enhance carbon gain has led to a growing interest in its research. A comparative analysis of B. sinuspersici chloroplast genome with other genomes of Amaranthaceae was conducted. Results from a 70% cut off sequence identity showed that B. sinuspersici is closely related to Beta vulgaris with slight variations in the arrangement of few genes such ycf1 and ycf15; and, the absence of psbB in Beta vulgaris. B. sinuspersici has the largest 153, 472 bp while Spinacea oleracea has the largest protein-coding sequence 6,754 bp larger than B. sinuspersici. The GC contents of each of the species ranges from 36.3 to 36.9% with B. sinuspersici having the same GC percentage as Haloxylon persicum and H. ammodendron (36.6%). The IR size also varies yet in all six species, the Ira/LSC border is generally located upstream of the trnH-GUG gene. A total of 107 tandem repeats were found in each of the species, most of which are situated in the intergenic space. These results provide basic information that may be valuable for future related studies.},
     year = {2018}
    }
    

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  • TY  - JOUR
    T1  - Comparative Chloroplast Genome Analysis of Single-Cell C4 Bienertia Sinuspersici with Other Amaranthaceae Genomes
    AU  - Lorrenne Caburatan
    AU  - Jin Gyu Kim
    AU  - Joonho Park
    Y1  - 2018/09/26
    PY  - 2018
    N1  - https://doi.org/10.11648/j.jps.20180604.13
    DO  - 10.11648/j.jps.20180604.13
    T2  - Journal of Plant Sciences
    JF  - Journal of Plant Sciences
    JO  - Journal of Plant Sciences
    SP  - 134
    EP  - 143
    PB  - Science Publishing Group
    SN  - 2331-0731
    UR  - https://doi.org/10.11648/j.jps.20180604.13
    AB  - Bienertia sinuspersici is a single-cell C4 (SCC4) plant species whose photosynthetic mechanisms occur in two cytoplasmic compartments containing central and peripheral chloroplasts. The efficiency of the C4 photosynthetic pathway to suppress photorespiration and enhance carbon gain has led to a growing interest in its research. A comparative analysis of B. sinuspersici chloroplast genome with other genomes of Amaranthaceae was conducted. Results from a 70% cut off sequence identity showed that B. sinuspersici is closely related to Beta vulgaris with slight variations in the arrangement of few genes such ycf1 and ycf15; and, the absence of psbB in Beta vulgaris. B. sinuspersici has the largest 153, 472 bp while Spinacea oleracea has the largest protein-coding sequence 6,754 bp larger than B. sinuspersici. The GC contents of each of the species ranges from 36.3 to 36.9% with B. sinuspersici having the same GC percentage as Haloxylon persicum and H. ammodendron (36.6%). The IR size also varies yet in all six species, the Ira/LSC border is generally located upstream of the trnH-GUG gene. A total of 107 tandem repeats were found in each of the species, most of which are situated in the intergenic space. These results provide basic information that may be valuable for future related studies.
    VL  - 6
    IS  - 4
    ER  - 

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Author Information
  • Department of Fine Chemistry, Seoul National University of Science and Technology, Seoul, South Korea

  • Department of Fine Chemistry, Seoul National University of Science and Technology, Seoul, South Korea

  • Department of Fine Chemistry, Seoul National University of Science and Technology, Seoul, South Korea

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