Skip to main content
Log in

Evolution of the Inner Light-Harvesting Antenna Protein Family of Cyanobacteria, Algae, and Plants

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Two hypotheses account for the evolution of the inner antenna light-harvesting proteins of oxygenic photosynthesis in cyanobacteria, algae, and plants: one in which the CP43 protein of photosytem II gave rise to the extrinsic CP43-like antennas of cyanobacteria (i.e. IsiA and Pcb proteins), as a late development, and the other in which CP43 and CP43-like proteins derive from an ancestral protein. In order to determine which of these hypotheses is most likely, we analyzed the family of antenna proteins by a variety of phylogenetic techniques, using alignments of the six common membrane-spanning helices, constructed using information on the antenna proteins’ three-dimensional structure, and surveyed for evidence of factors that might confound inference of a correct phylogeny. The first hypothesis was strongly supported. As a consequence, we conclude that the ancestral photosynthetic apparatus, with 11 membrane-spanning helices, split at an early stage during evolution to form, on the one hand, the reaction center of photosystem II and, on the other hand, the ancestor of inner antenna proteins, CP43 (PsbC) and CP47 (PsbB). Only much later in evolution did the CP43 lineage give rise to the CP43’ proteins (IsiA and Pcb) of cyanobacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

References

  • Ababneh F, Jermiin LS, Robinson J (2006) Generation of the exact distribution and simulation of matched nucleotide sequences on a phylogenetic tree. J Math Model Algorithm 5:291–308

    Article  Google Scholar 

  • Baymann F, Brugna M, Muhlenhoff U, Nitschke W (2001) Daddy, where did (PS)I come from? Biochim Biophys Acta 1507:291–310

    Article  PubMed  CAS  Google Scholar 

  • Bibby TS, Nield J, Barber J (2001a) A photosystem II-like protein, induced under iron–stress, forms an antenna ring around the photosystem I trimer in cyanobacteria. Nature 412:743–745

    Article  CAS  Google Scholar 

  • Bibby TS, Nield J, Partensky F, Barber J (2001b) Oxyphotobacteria: antenna ring around photosystem I. Nature 413:590–590

    Article  CAS  Google Scholar 

  • Bibby TS, Mary I, Nield J, Partensky F, Barber J (2003a) Low-light-adapted prochlorococcus species possess specific antennae for each photosystem. Nature 424:1051–1054

    Article  CAS  Google Scholar 

  • Bibby TS, Nield J, Chen M, Larkum AWD, Barber J (2003b) Structure of a PSII supercomplex isolated from of Prochloron didemni retaining its chlorophll a/b light harvesting system. Proc Natl Acad Sci USA 100:9050–9054

    Article  CAS  Google Scholar 

  • Blankenship RE (2001) Molecular evidence for the evolution of photosynthesis. Trends Plant Sci 6:4–6

    Article  PubMed  CAS  Google Scholar 

  • Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science, Oxford, UK/Malden, MA

    Google Scholar 

  • Bowker AH (1948) A test for symmetry in contingency tables. J Am Stat Assoc 43:572–574

    Article  Google Scholar 

  • Chen M, Bibby TS (2005) photosynthetic apparatus of antenna-reaction centres supercomplexes in oxyphotobacteria: Insight through significance of Pcb/IsiA Proteins. Photosynth Res 86:165–173

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Quinnell RG, Larkum AWD (2002) The major light-harvesting pigment protein of Acaryochloris marina. FEBS Lett 514:149–152

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Bibby TS, Nield J, Larkum AWD, Barber J (2005a) Iron deficiency induces a chlorophyll d-binding Pcb antenna system around Photosystem I in Acaryochloris marina. Biochim Biophys Acta 1708:367–374

    Article  CAS  Google Scholar 

  • Chen M, Bibby TS, Nield J, Larkum AWD, Barber J (2005b) Structure of a large photosystem II supercomplex from Acaryochloris marina. FEBS Lett 579:1306–1310

    Article  CAS  Google Scholar 

  • Drummond AJ, Rambaut A (2005) BEAST v1.3. Distributed by the author. Department of Zoology, University of Oxford, Oxford

  • Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320

    PubMed  CAS  Google Scholar 

  • Felsenstein J (2005) PHYLIP—Phylogeny inference package, version 3.6 Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosyntheic oxygen-evolving center. Science 303:1831–1833

    Article  PubMed  CAS  Google Scholar 

  • Fromme P, Jordan P, Kraub N (2001) Structure of photosystem I. Biochim Biophys Acta 1507:5–31

    Article  PubMed  CAS  Google Scholar 

  • Fyfe PK, Jones MR, Heathcote P (2002) Insights into the evolution of the antenna domains of Type-I and Type-II photosynthetic reaction centres through homology modelling. FEBS Lett 530:117–123

    Article  PubMed  CAS  Google Scholar 

  • Green BR (2003) The evolution of light-harvesting antennas. In: Green BR, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic, Dordrecht, pp 129–168

    Google Scholar 

  • Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379

    Article  PubMed  CAS  Google Scholar 

  • Ho SYW, Jermiin LS (2004) Tracing the decay of the historical signal in biological sequence data. Syst Biol 53:623–637

    Article  PubMed  Google Scholar 

  • Hofmann K, Stoffel W (1993) TMbase—a database of membrane spanning proteins segments. Biol Chem H-S 374:166

    Google Scholar 

  • Jakobsen IB, Easteal S (1996) A program for calculating and displaying compatibility matrices as an aid in determining reticulate evolution in molecular sequences. Comput Appl Biosci 12:291–295

    PubMed  CAS  Google Scholar 

  • Jayaswal V, Jermiin LS, Robinson J (2005) Estimation of phylogeny using a general markov model. Evol Bioinformatics Online 1:62–80

    Google Scholar 

  • Jermiin LS, Olsen GJ, Mengersen KL, Easteal S (1997) Majority-rule consensus of phylogenetic trees obtained by maximum-likelihood analysis. Mol Bio Evol 14:1296–1302

    CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    PubMed  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Kraub N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917

    Article  PubMed  CAS  Google Scholar 

  • Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29:170–179

    Article  PubMed  CAS  Google Scholar 

  • Kolber ZS, Van Dover CL, Niederman RA, Falkowski PG (2000) Bacterial photosynthesis in surface water of the open ocean. Nature 407:177–179

    Article  PubMed  CAS  Google Scholar 

  • Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  PubMed  CAS  Google Scholar 

  • La Roche J, Van der Staay GWM, Partensky F, Ducret A, Aebersold R, Li R, Golden SS, Hiller RG, Wrench PM, Larkum AWD, Green BR (1996) Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvestiong proteins. Proc Natl Acad Sci USA 93:15244–15248

    Article  PubMed  CAS  Google Scholar 

  • Larkum AWD (2006) Evolution of reaction centers and photosystems. In: Grimm B, Porra RJ, Rudiger W, Scheer H (eds) Chlorophylls and Bacteriocholorophylls. Vol 25. Advances in Photosynthesis and Respiration, Springer Verlag, Berlin, pp 261–282

    Google Scholar 

  • Larkum AWD, Howe CJ (1997) Molecular aspects of light-harvesting processes in algae. Advances in Botanical Research, Vol 27. Academic Press, London, pp 257–330

    Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0Å resolution structure of photosystem II. Nature 438:1040–1044

    Article  PubMed  CAS  Google Scholar 

  • Robert B, Cogdell RJ, Van Grondelle R (2003) The light harvesting system of purple bacteria. Kluwer Academic, Dordrecht

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Sarcina M, Mullineaux C (2004) Mobility of the isiA chlorophyll-binding protein in cyanobacterial thylakoid membranes. J Biol Chem 279: 36514–36518

    Article  PubMed  CAS  Google Scholar 

  • Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504

    Article  PubMed  CAS  Google Scholar 

  • Schubert WD, Klukas O, Saenger W, Witt HT, Fromme P, Krauss N (1998) A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. J Mol Biol 280:297–314

    Article  PubMed  CAS  Google Scholar 

  • Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Bio Evol 16:1114–1116

    CAS  Google Scholar 

  • Smith SW, Overbeek R, Woese CR, Gilbert W, Gillevet PM (1994) The genetic data environment: an expandable GUI for multiple-sequence analysis. Comput Appl Biosci 10:671–675

    PubMed  CAS  Google Scholar 

  • Summons RE, Janhke LL, Hope JM, Logan GA (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400:1554–1557

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, MA

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Thorne JL, Kishino H, Painter IS (2002) Estimating the rate of evolution of rate of molecular evolution. Mol Biol Evol 15:1647–1657

    Google Scholar 

  • Ting CS, Rocap G, King J, Chisholm SW (2002) Cyanobacterial photosynthesis in the oceans: the origin and significance of divergent light-harvesting strategies. Trends Microbiol 10:134–142

    Article  PubMed  CAS  Google Scholar 

  • Van der Staay GWM, Yurkova N, Green BR (1988) The 38 KDa chlorophyll a/b protein of the prokaryote Prochlorothrix hollandica is encoded by a divergent pcb gene. Plant Mol Biol 36:709–716

    Article  Google Scholar 

  • Vasil’ev S, Bruce D (2004) Optimization and evolution of light harvesting in photosynthesis: The role of antenna chlorophyll conserved between photosystem II and photosystem I. Plant Cell 16:3059–3068

    Article  PubMed  CAS  Google Scholar 

  • Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Bio Evol 18:691–699

    CAS  Google Scholar 

  • Yang ZH (1996) Among-site rate variation and its impact on phylogenetic analysis. Trends Ecol Evol 11:367–372

    Article  Google Scholar 

  • Zhang Y, Jermiin LS, Larkum AWD (2003) Phylogenetic analysis of light-harvesting antenna peptides from plants and bacteria. Foundermental aspects to global perspectives. In: Vander E, Bruce D (eds) Proceedings of the 13th International Conference on Photosynthesis. Alliance Communication Group, Kansas, Montreal, pp 745–746

    Google Scholar 

Download references

Acknowledgments

This work was partially supported by grants to A.W.D.L., B.B.Z., L.S.J., and M.C., from the Australian Research Council. Y.Z. also wishes to acknowledge the receipt of a travel scholarship from the University of Sydney.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anthony W. D. Larkum.

Additional information

[Reviewing Editor: Dr. Patrick Keeling]

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Y., Chen, M., Zhou, B.B. et al. Evolution of the Inner Light-Harvesting Antenna Protein Family of Cyanobacteria, Algae, and Plants. J Mol Evol 64, 321–331 (2007). https://doi.org/10.1007/s00239-006-0058-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-006-0058-2

Keywords

Navigation