Journal of Plant Research

, Volume 130, Issue 4, pp 635–645 | Cite as

Diverse origins of enzymes involved in the biosynthesis of chloroplast peptidoglycan

Regular Paper


Chloroplasts are believed to be descendants of ancestral cyanobacteria that had peptidoglycan layer between the outer and the inner membranes. Historically, the glaucophyte Cyanophora paradoxa and the rhizopod Paulinella chromatophora were believed to harbor symbiotic cyanobacteria having peptidoglycan, which were conventionally named “cyanelles”. In addition, the complete set of genes involved in the synthesis of peptidoglycan has been found in the moss Physcomitrella patens and some plants and algae. The presence of peptidoglycan-like structures was demonstrated by a new metabolic labeling technique in P. patens. However, many green algae and all known red algae lack peptidoglycan-related genes. That is the reason why we questioned the origin of peptidoglycan-synthesizing enzymes in the chloroplasts of the green algae and plants. We performed phylogenetic analysis of ten enzymes involved in the synthesis of peptidoglycan exploiting the Gclust homolog clusters and additional genomic data. As expected, all the identified genes encoded in the chromatophore genome of P. chromatophora were closely related to cyanobacterial homologs. In the green algae and plants, only two genes, murA and mraY, were found to be closely related to cyanobacterial homologs. The origins of all other genes were diverse. Unfortunately, the origins of C. paradoxa genes were not clearly determined because of incompleteness of published genomic data. We discuss on the probable evolutionary scenarios to explain the mostly non-cyanobacterial origins of the biosynthetic enzymes of chloroplast peptidoglycan: A plausible one includes extensive multiple horizontal gene transfers during the early evolution of Viridiplantae.


Chloroplast evolution Cyanophora paradoxa Endosymbiosis Paulinella chromatophora Peptidoglycan Viridiplantae 



This work was supported in part by a Grant-in-Aids for Scientific Research (24570043 and 15K12433 to NS and 25440158 to HT) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan. Some large calculations were performed using the Super Computer System of Human Genome Center, University of Tokyo.

Supplementary material

10265_2017_935_MOESM1_ESM.pdf (5.1 mb)
Supplementary material 1 (PDF 5213 KB) (281 kb)
Supplementary material 2 (ZIP 281 KB)


  1. Archibald JM (2015) Endosymbiosis and eukaryotic cell evolution. Curr Biol 25:R911–R921CrossRefPubMedGoogle Scholar
  2. Awai K, Ohta H, Sato N (2014) Oxygenic photosynthesis without galactolipids. Proc Natl Acad Sci USA 111:13571–13575CrossRefPubMedPubMedCentralGoogle Scholar
  3. Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, Ashton NW, Axtell MJ, Barker E, Barker MS, Bennetzen JL, Bonawitz ND, Chapple C, Cheng C, Correa LG, Dacre M, DeBarry J, Dreyer I, Elias M, Engstrom EM, Estelle M, Feng L, Finet C, Floyd SK, Frommer WB, Fujita T, Gramzow L, Gutensohn M, Harholt J, Hattori M, Heyl A, Hirai T, Hiwatashi Y, Ishikawa M, Iwata M, Karol KG, Koehler B, Kolukisaoglu U, Kubo M, Kurata T, Lalonde S, Li K, Li Y, Litt A, Lyons E, Manning G, Maruyama T, Michael TP, Mikami K, Miyazaki S, Morinaga S, Murata T, Mueller-Roeber B, Nelson DR, Obara M, Oguri Y, Olmstead RG, Onodera N, Petersen BL, Pils B, Prigge M, Rensing SA, Riaño-Pachón DM, Roberts AW, Sato Y, Scheller HV, Schulz B, Schulz C, Shakirov EV, Shibagaki N, Shinohara N, Shippen DE, Sørensen I, Sotooka R, Sugimoto N, Sugita M, Sumikawa N, Tanurdzic M, Theissen G, Ulvskov P, Wakazuki S, Weng JK, Willats WW, Wipf D, Wolf PG, Yang L, Zimmer AD, Zhu Q, Mitros T, Hellsten U, Loqué D, Otillar R, Salamov A, Schmutz J, Shapiro H, Lindquist E, Lucas S, Rokhsar D, Grigoriev IV (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–963CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bhattacharya D, Price DC, Chan CX, Gross J, Steiner JM, Löffelhardt W (2014) Analysis of the genome of Cyanophora paradoxa: An algal model for understanding primary endosymbiosis. In: Löffelhardt W (ed) Endosymbiosis. Springer, Heidelberg, pp 135–150CrossRefGoogle Scholar
  5. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  6. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321Google Scholar
  7. Hirano T, Tanidokoroa K, Shimizu Y, Kawarabayasi Y, Ohshima T, Sato M, Tadano S, Ishikawa Y, Takio S, Takechi K, Takano H (2016) Moss chloroplasts are surrounded by a peptidoglycan wall containing d-amino acids. Plant Cell 28:1521–1532PubMedPubMedCentralGoogle Scholar
  8. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, Sato S, Yamada T, Mori H, Tajima N, Moriyama T, Ikeuchi M, Watanabe M, Wada H, Kobayashi K, Saito M, Masuda T, Sasaki-Sekimoto Y, Mashiguchi K, Awai K, Shimojima M, Masuda S, Iwai M, Nobusawa T, Narise T, Kondo S, Saito H, Sato R, Murakawa M, Ihara Y, Oshima-Yamada Y, Ohtaka K, Satoh M, Sonobe K, Ishii M, Ohtani R, Kanamori-Sato M, Honoki R, Miyazaki D, Mochizuki H, Umetsu J, Higashi K, Shibata D, Kamiya Y, Sato N, Nakamura Y, Tabata S, Ida S, Kurokawa K, Ohta H (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun 5:3978CrossRefPubMedPubMedCentralGoogle Scholar
  9. Iino M, Hashimoto H (2003) Intermediate features of cyanelle division of Cyanophora paradoxa (Glaucocystophyta) between cyanobacterial and plastid division. J Phycol 39:561–569CrossRefGoogle Scholar
  10. Kies L (1974) Elektronenmikroskopische Untersuchungen an Paulinella chromatophora lauterborn, einer mit blau-grünen Endosymbionten (Cyanellen). Protoplasma 80:69–89CrossRefPubMedGoogle Scholar
  11. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  12. Lin X, Li N, Kudo H, Zhang Z, Li J, Wang L, Zhang W, Takechi K, Takano H (2017) Genes sufficient for synthesizing peptidoglycan are retained in gymnosperm genomes, and MurE from Larix gmelinii can rescue the albino phenotype of Arabidopsis MurE mutants. Plant Cell Physiol (in press) Google Scholar
  13. Machida M, Takechi K, Sato H, Chung SJ, Kuroiwa H, Takio S, Seki M, Shinozaki K, Fujita T, Hasebe M, Takano H (2006) Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss. Proc Natl Acad Sci USA 103:6753–6758CrossRefPubMedPubMedCentralGoogle Scholar
  14. Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralblatt 25:593–604Google Scholar
  15. Moriyama T, Sato N (2014) Enzymes involved in organellar DNA replication in photosynthetic eukaryotes. Front Plant Sci 5:480CrossRefPubMedPubMedCentralGoogle Scholar
  16. Nowack ECM, Grossman AR (2012) Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci USA 109:5340–5345CrossRefPubMedPubMedCentralGoogle Scholar
  17. Nowack EC, Melkonian M, Glöckner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 25:410–418CrossRefGoogle Scholar
  18. Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM, Schwacke R, Gross J, Blouin NA, Lane C, Reyes-Prieto A, Durnford DG, Neilson JAD, Lang BF, Burger G, Steiner JM, Löffelhardt W, Meuser JE, Posewitz MC, Ball S, Arias MC, Henrissat B, Coutinho PM, Rensing S, Symeonidi A, Doddapaneni H, Green BR, Rajah VD, Boore J, Bhattacharya D (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335:843–847CrossRefPubMedGoogle Scholar
  19. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin-I T, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69CrossRefPubMedGoogle Scholar
  20. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–42Google Scholar
  21. Sapp J (1994) Evolution by association. Oxford University Press, OxfordGoogle Scholar
  22. Sasaki NV, Sato N (2010) CyanoClust: comparative genome resources of cyanobacteria and plastids. Database bap025Google Scholar
  23. Sato N (2000) SISEQ: Manipulation of multiple sequence and large database files for common platforms. Bioinformatics 16:180–181CrossRefPubMedGoogle Scholar
  24. Sato N (2001) Was the evolution of plastid genetic machinery discontinuous? Trends Plant Sci 6:151–156CrossRefPubMedGoogle Scholar
  25. Sato N (2009) Gclust: trans-kingdom classification of proteins using automatic individual threshold setting. Bioinformatics 25:599–605CrossRefPubMedGoogle Scholar
  26. Sato N (2016) Conservation versus discontinuity in the genealogy of cyanobacteria and plastids: Fantasy and reality of the endosymbiogenesis theory of plastid origin. Endocytobiosis. Cell Res 27:33–36Google Scholar
  27. Sato N, Awai K (2016) Diversity in biosynthetic pathways of galactolipids in the light of endosymbiotic origin of chloroplasts. Front Plant Sci 7:117CrossRefPubMedPubMedCentralGoogle Scholar
  28. Sato M, Mogi Y, Nishikawa T, Miyamura S, Nagumo T, Kawano S (2009) The dynamic surface of dividing cyanelles and ultrastructure of the region directly below the surface in Cyanophora paradoxa. Planta 229:781–791CrossRefPubMedGoogle Scholar
  29. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32:234–258CrossRefPubMedGoogle Scholar
  30. Stanier RY, Doudoroff MJ, Adelberg EA (1967) The Microbial World. Prentice-Hall, Eglewood Cliffs, NJGoogle Scholar
  31. Takano H, Takechi K (2010) Plastid peptidoglycan. Biochim Biophys Acta 1800:144–151CrossRefPubMedGoogle Scholar
  32. van Baren MJ, Bachy C, Reistetter EN, Purvine SO, Grimwood J, Sudek S, Yu H, Poirier C, Deerinck TJ, Kuo A, Grigoriev IV, Wong CH, Smith RD, Callister SJ, Wei CL, Schmutz J, Worden AZ (2016) Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants. BMC Genomics 17:267CrossRefPubMedPubMedCentralGoogle Scholar
  33. Vollmer W, Seligman SJ (2009) Architecture of peptidoglycan: more data and more models. Trends Microbiol 18:59–66CrossRefGoogle Scholar
  34. Worden AZ, Lee JH, Mock T, Rouzé P, Simmons MP, Aerts AL, Allen AE, Cuvelier ML, Derelle E, Everett MV, Foulon E, Grimwood J, Gundlach H, Henrissat B, Napoli C, McDonald SM, Parker MS, Rombauts S, Salamov A, von Dassow P, Badger JH, Coutinho PM, Demir E, Dubchak I, Gentemann C, Eikrem W, Gready JE, John U, Lanier W, Lindquist EA, Lucas S, Mayer KFX, Moreau H, Not F, Otillar R, Panaud O, Pangilinan J, Paulsen I, Piegu B, Poliakov A, Robbens S, Schmutz J, Toulza E, Wyss T, Zelensky A, Zhou K, Armbrust EV, Bhattacharya D, Goodenough UW, Van de Peer Y, Grigoriev IV (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  1. 1.Department of Life Sciences, Graduate School of Arts and SciencesUniversity of TokyoTokyoJapan
  2. 2.Faculty of Advanced Science and TechnologyKumamoto UniversityKumamotoJapan
  3. 3.Institute of Pulsed Power ScienceKumamoto UniversityKumamotoJapan

Personalised recommendations