, Volume 254, Issue 5, pp 1879–1885 | Cite as

Three rings for the evolution of plastid shape: a tale of land plant FtsZ

  • Christopher Grosche
  • Stefan A. Rensing
Original Article


Nuclear-encoded plant FtsZ genes are derived from endosymbiotic gene transfer of cyanobacteria-like genes. The green lineage (Chloroplastida) and red lineage (Rhodophyta) feature FtsZ1 and FtsZ2 or FtsZB and FtsZA, respectively, which are involved in plastid division. These two proteins show slight differences and seem to heteropolymerize to build the essential inner plastid division ring. A third gene, encoding FtsZ3, is present in glaucophyte and charophyte algae, as well as in land plants except ferns and angiosperms. This gene was probably present in the last common ancestor of the organisms united by having a primary plastid (Archaeplastida) and was lost during vascular plant evolution as well as in the red and green algae. The presence/absence pattern of FtsZ3 mirrors that of a full set of Mur genes and the peptidoglycan wall encoded by them. Based on these findings, we discuss a role for FtsZ3 in the establishment or maintenance of plastid peptidoglycan shells.


FtsZ Evolution Plant Moss Charophyte Peptidoglycan 



We are grateful to F. Donges for assistance and for funding by ERA-CAPS SeedAdapt (DFG RE 1697/8–1 to S.A.R.).

Compliance with ethical standards

The authors declare that they have no conflict of interest.

Supplementary material

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ESM 1 (XLSX 15 kb)
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  1. Adl SM et al (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451CrossRefPubMedGoogle Scholar
  2. Bi EF, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354:161–164. doi: 10.1038/354161a0 CrossRefPubMedGoogle Scholar
  3. Burki F et al (2016) Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida. Haptophyta and Cryptista Proc Biol Sci 283. doi: 10.1098/rspb.2015.2802
  4. Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD, Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10:507–516CrossRefPubMedGoogle Scholar
  5. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165. doi: 10.1093/bioinformatics/btr088 CrossRefPubMedPubMedCentralGoogle Scholar
  6. de Vries J, Stanton A, Archibald JM, Gould SB (2016) Streptophyte Terrestrialization in light of plastid evolution. Trends Plant Sci 21:467–476. doi: 10.1016/j.tplants.2016.01.021 CrossRefPubMedGoogle Scholar
  7. Frickenhaus S, Beszteri B (2008) Quicktree-SD, Software developed by AWI-Bioinformatics. doi:
  8. Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci U S A 100:4328–4333. doi: 10.1073/pnas.0530206100 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20:2460–2470. doi: 10.1105/tpc.108.061440 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Miyagishima SY, Osteryoung KW (2009) PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J 59:700–711. doi: 10.1111/j.1365-313X.2009.03905.x CrossRefPubMedGoogle Scholar
  11. Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517. doi: 10.1146/annurev.arplant.59.032607.092915 CrossRefPubMedGoogle Scholar
  12. Gremillon L, Kiessling J, Hause B, Decker EL, Reski R, Sarnighausen E (2007) Filamentous temperature-sensitive Z (FtsZ) isoforms specifically interact in the chloroplasts and in the cytosol of Physcomitrella patens. New Phytol 176:299–310CrossRefPubMedGoogle Scholar
  13. Hirano T et al (2016) Moss chloroplasts are surrounded by a Peptidoglycan Wall containing D-amino acids. Plant Cell 28:1521–1532. doi: 10.1105/tpc.16.00104 PubMedPubMedCentralGoogle Scholar
  14. Holtsmark I, Lee S, Lunde KA, Auestad K, Maple-Grodem J, Moller SG (2013) Plastid division control: the PDV proteins regulate DRP5B dynamin activity. Plant Mol Biol 82:255–266. doi: 10.1007/s11103-013-0059-7 CrossRefPubMedGoogle Scholar
  15. Homi S, Takechi K, Tanidokoro K, Sato H, Takio S, Takano H (2009) The peptidoglycan biosynthesis genes MurA and MraY are related to chloroplast division in the moss Physcomitrella patens. Plant Cell Physiol 50:2047–2056. doi: 10.1093/pcp/pcp158 CrossRefPubMedGoogle Scholar
  16. Hong Z et al (2003) A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol Biol 53:261–265CrossRefPubMedGoogle Scholar
  17. Itoh R, Fujiwara M, Nagata N, Yoshida S (2001) A chloroplast protein homologous to the eubacterial topological specificity factor minE plays a role in chloroplast division. Plant Physiol 127:1644–1655CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jarvis P, López-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14:787–802. doi: 10.1038/nrm3702 CrossRefPubMedGoogle Scholar
  19. Kasten B, Reski R (1997) Beta-lactam antibiotics inhibit chloroplast division in a moss (Physcomitrella patens) but not in tomato (Lycopersicon esculentum). J Plant Physiol 150:137–140CrossRefGoogle Scholar
  20. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi: 10.1093/molbev/mst010 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607. doi: 10.1146/annurev-arplant-050312-120144 CrossRefPubMedGoogle Scholar
  22. Kiessling J et al (2004) Dual targeting of plastid division protein FtsZ to chloroplasts and the cytoplasm. EMBO Rep 5:889–894CrossRefPubMedPubMedCentralGoogle Scholar
  23. Leister D (2016) Towards understanding the evolution and functional diversification of DNA-containing plant organelles. F1000Res 5 doi: 10.12688/f1000research.7915.1
  24. Ma X, Margolin W (1999) Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 181:7531–7544PubMedPubMedCentralGoogle Scholar
  25. Machida M et al (2006) Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss. Proc Natl Acad Sci U S A 103:6753–6758CrossRefPubMedPubMedCentralGoogle Scholar
  26. Maier UG, Zauner S, Hempel F (2015) Protein import into complex plastids: cellular organization of higher complexity. Eur J Cell Biol 94:340–348. doi: 10.1016/j.ejcb.2015.05.008 CrossRefPubMedGoogle Scholar
  27. Maple J, Aldridge C, Moller SG (2005) Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J 43:811–823. doi: 10.1111/j.1365-313X.2005.02493.x CrossRefPubMedGoogle Scholar
  28. Martin A, Lang D, Hanke ST, Mueller SJ, Sarnighausen E, Vervliet-Scheebaum M, Reski R (2009a) Targeted Gene knockouts reveal overlapping functions of the five Physcomitrella patens FtsZ isoforms in chloroplast division, chloroplast shaping, cell patterning, plant development, and gravity sensing. Mol Plant 2:1359–1372CrossRefPubMedPubMedCentralGoogle Scholar
  29. Martin A, Lang D, Heckmann J, Zimmer AD, Vervliet-Scheebaum M, Reski R (2009b) A uniquely high number of ftsZ genes in the moss Physcomitrella patens. Plant Biol (Stuttg) 11:744–750. doi: 10.1111/j.1438-8677.2008.00174.x CrossRefGoogle Scholar
  30. Miyagishima SY, Itoh R, Toda K, Takahashi H, Kuroiwa H, Kuroiwa T (1998) Identification of a triple ring structure involved in plastid division in the primitive red alga Cyanidioschyzon merolae. J Electron Microsc 47:269–272Google Scholar
  31. Miyagishima SY, Froehlich JE, Osteryoung KW (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18:2517–2530. doi: 10.1105/tpc.106.045484 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Miyagishima SY, Nakanishi H, Kabeya Y (2011) Structure, regulation, and evolution of the plastid division machinery. Int Rev Cell Mol Biol 291:115–153. doi: 10.1016/b978-0-12-386035-4.00004-5 CrossRefPubMedGoogle Scholar
  33. Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (2003) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15:655–665CrossRefPubMedPubMedCentralGoogle Scholar
  34. Miyagishima SY, Nozaki H, Nishida K, Nishida K, Matsuzaki M, Kuroiwa T (2004) Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 58:291–303. doi: 10.1007/s00239-003-2551-1 CrossRefPubMedGoogle Scholar
  35. Mukherjee A, Lutkenhaus J (1994) Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol 176:2754–2758CrossRefPubMedPubMedCentralGoogle Scholar
  36. Nakanishi H, Suzuki K, Kabeya Y, Miyagishima SY (2009) Plant-specific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr Biol 19:151–156. doi: 10.1016/j.cub.2008.12.018 CrossRefPubMedGoogle Scholar
  37. Okazaki K et al (2009) The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 21:1769–1780. doi: 10.1105/tpc.109.067785 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Oliva MA, Cordell SC, Löwe J (2004) Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11:1243–1250. doi: 10.1038/nsmb855 CrossRefPubMedGoogle Scholar
  39. Osteryoung KW, Pyke KA (2014) Division and dynamic morphology of plastids. Annu Rev Plant Biol 65:443–472. doi: 10.1146/annurev-arplant-050213-035748 CrossRefPubMedGoogle Scholar
  40. Rensing SA, Kiessling J, Reski R, Decker EL (2004) Diversification of ftsZ during early land plant evolution. J Mol Evol 58:154–162CrossRefPubMedGoogle Scholar
  41. Reski R (2009) Challenges to our current view on chloroplasts. Biol Chem 390:731–738. doi: 10.1515/BC.2009.089 CrossRefPubMedGoogle Scholar
  42. Ronquist F et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi: 10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Schmitz AJ, Glynn JM, Olson BJ, Stokes KD, Osteryoung KW (2009) Arabidopsis FtsZ2-1 and FtsZ2-2 are functionally redundant, but FtsZ-based plastid division is not essential for chloroplast partitioning or plant growth and development. Mol Plant 2:1211–1222CrossRefPubMedGoogle Scholar
  44. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi: 10.1093/bioinformatics/btu033 CrossRefPubMedPubMedCentralGoogle Scholar
  45. TerBush AD, Yoshida Y, Osteryoung KW (2013) FtsZ in chloroplast division: structure, function and evolution. Curr Opin Cell Biol 25:461–470. doi: 10.1016/ CrossRefPubMedGoogle Scholar
  46. Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15:1918–1933CrossRefPubMedPubMedCentralGoogle Scholar
  47. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191. doi: 10.1093/bioinformatics/btp033 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Whatley JM, Gunning BES (1981) Chloroplast development in AZOLLA roots. New Phytol 89:129–138. doi: 10.1111/j.1469-8137.1981.tb04755.x CrossRefGoogle Scholar
  49. Wickett NJ et al (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci U S A 111:E4859–E4868. doi: 10.1073/pnas.1323926111 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Yoshida Y et al (2006) Isolated chloroplast division machinery can actively constrict after stretching. Science 313:1435–1438. doi: 10.1126/science.1129689 CrossRefPubMedGoogle Scholar
  51. Yoshida Y et al (2010) Chloroplasts divide by contraction of a bundle of nanofilaments consisting of polyglucan. Science 329:949–953. doi: 10.1126/science.1190791 CrossRefPubMedGoogle Scholar
  52. Yoshida Y, Mogi Y, TerBush AD, Osteryoung KW (2016) Chloroplast FtsZ assembles into a contractible ring via tubulin-like heteropolymerization. Nat Plants 2:16095. doi: 10.1038/nplants.2016.95 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2017

Authors and Affiliations

  1. 1.Plant Cell Biology, Faculty of BiologyUniversity of MarburgMarburgGermany

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