Skip to main content
SpringerLink
Log in

A Multistep Process Gave Rise to RNA Polymerase IV of Land Plants

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

Abstract

Since their discovery in Metazoa, the three nuclear RNA polymerases (RNAPs) have been found in fungi, plants, and diverse protists. In all eukaryotes studied to date, RNAPs I, II, and III collectively transcribe all major RNAs made in the nucleus. We have found genes for the largest subunit (RPD1/RPE1) of a new DNA-dependent RNAP, RNAP IV, in all major land plant taxa and in closely related green algae. Genes for the second-largest subunit (RPD2) of this enzyme were found in all land plants. Phylogenetic study indicates that RNAP IV genes are sister to the corresponding RNAP II genes. Our results show the genesis of RNAP IV to be a multistep process in which the largest and second-largest subunit genes evolved by independent duplication events in the ancestors of Charales and land plants. These findings provide insights into evolutionary mechanisms that can explain the origin of multiple RNAPs in the eukaryotic nucleus.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adman R, Schultz LD, Hall BD (1972) Transcription in yeast: separation and properties of multiple RNA polymerases. Proc Natl Acad Sci USA 69:1702–1706

    Article  PubMed  CAS  Google Scholar 

  • AGI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Bell SD, Jackson SP (1998) Transcription and translation in Archaea: a mosaic of eukaryal and bacterial features. Trends Microbiol 6:222–228

    Article  PubMed  CAS  Google Scholar 

  • Bellaoui M, Gruissem W (2004) Altered expression of the Arabidopsis ortholog of DCL affects normal plant development. Planta 219:819–826

    Article  PubMed  CAS  Google Scholar 

  • Cramer P, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292:1863–1876

    Article  PubMed  CAS  Google Scholar 

  • Dacks JB, Marinets A, Ford Doolittle W, Cavalier-Smith T, Logsdon JM, Jr. (2002) Analyses of RNA Polymerase II genes from free-living protists: phylogeny, long branch attraction, and the eukaryotic big bang. Mol Biol Evol 19:830–840

    PubMed  CAS  Google Scholar 

  • Dequard-Chablat M, Riva M, Carles C, Sentenac A (1991) RPC19, the gene for a subunit common to yeast RNA polymerases A (I) and C (III). J Biol Chem 266:15300–15307

    PubMed  CAS  Google Scholar 

  • Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, Deng LT, Wu X, Reith M, CavalierSmith T, Maier UG (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410:1091–1096

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (2004) PHYLIP. Available at: http://evolution.genetics.washington.edu/phylip.html; accessed October 20, 2006

  • Gnatt AL, Cramer P, Fu J, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 A resolution. Science 292:1876–1882

    Article  PubMed  CAS  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  PubMed  CAS  Google Scholar 

  • Golding GB, Gupta RS (1995) Protein-based phylogenies support a chimeric origin for the eukaryotic genome. Mol Biol Evol 12:1–6

    PubMed  CAS  Google Scholar 

  • Greenleaf AL, Bautz EK (1975) RNA polymerase B from Drosophila melanogaster larvae. Purification and partial characterization. Eur J Biochem 60:169–179

    Article  PubMed  CAS  Google Scholar 

  • Grishin NV (1995) Estimation of the number of amino acid substitution per site when the substitution rate varies among sites. J Mol Evol 41:675–679

    Article  CAS  PubMed  Google Scholar 

  • Guilfoyle TJ, Lin CY, Chen YM, Key JL (1976) Purification and characterization of RNA polymerase I from a higher plant. Biochim Biophys Acta 418:344–357

    PubMed  CAS  Google Scholar 

  • Hedtke B, Borner T, Weihe A (1997) Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 277:809–811

    Article  PubMed  CAS  Google Scholar 

  • Hess WR, Borner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59

    Article  PubMed  CAS  Google Scholar 

  • Hu P, Wu S, Sun Y, Yuan CC, Kobayashi R, Myers MP, Hernandez N (2002) Characterization of human RNA polymerase III identifies orthologues for Saccharomyces cerevisiae RNA polymerase III subunits. Mol Cell Biol 22:8044–8055

    Article  PubMed  CAS  Google Scholar 

  • Hudson GS, Holton TA, Whitfield PR, Bottomley W (1988) Spinach chloroplast rpoBC genes encode three subunits of the chloroplast RNA polymerase. J Mol Biol 200:639–654

    Article  PubMed  CAS  Google Scholar 

  • Iwabe N, Kuma K, Kishino H, Hasegawa M, Miyata T (1991) Evolution of RNA polymerases and branching patterns of the three major groups of Archaebacteria. J Mol Evol 32:70–78

    Article  PubMed  CAS  Google Scholar 

  • Jendrisak JJ, Burgess RR (1975) A new method for the large-scale purification of wheat germ DNA-dependent RNA polymerase II. Biochemistry 14:4639–4645

    Article  PubMed  CAS  Google Scholar 

  • Jokerst RS, Weeks JR, Zehring WA, Greenleaf AL (1989) Analysis of the gene encoding the largest subunit of RNA polymerase II in Drosophila. Mol Gen Genet 215:266–275

    Article  PubMed  CAS  Google Scholar 

  • Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E, Daxinger L, Kreil DP, Matzke M, Matzke AJ (2005) Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37:761–765

    Article  PubMed  CAS  Google Scholar 

  • Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Ishiguro A, Ishihama A (1997) RNA polymerase II subunits 2, 3, and 11 form a core subassembly with DNA binding activity. J Biol Chem 272:25851–25855

    Article  PubMed  CAS  Google Scholar 

  • Klenk HP, Zillig W, Lanzendorfer M, Brampp B, Palm P (1995) Location of protist lineages in a phylogenetic tree inferred from sequences of DNA-dependent RNA polymerases. Arch Protistenkd 145:221–230

    Google Scholar 

  • 2Korzheva N, Mustaev A, Kozlov M, Malhotra A, Nikiforov V, Goldfarb A, Darst SA (2000) A structural model of transcription elongation. Science 289:619–625

    Article  PubMed  CAS  Google Scholar 

  • Langer D, Hain J, Thuriaux P, Zillig W (1995) Transcription in archaea: similarity to that in eucarya. Proc Natl Acad Sci USA 92:5768–5772

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Hall BD (2004) Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Natl Acad Sci USA 101:4507–4512

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol 16:1799–1808

    PubMed  CAS  Google Scholar 

  • McCourt RM, Delwiche CF, Karol KG (2004) Charophyte algae and land plant origins. Trends Ecol Evol 19:661–666

    Article  PubMed  Google Scholar 

  • Memet S, Saurin W, Sentenac A (1988) RNA polymerases B and C are more closely related to each other than to RNA polymerase A. J Biol Chem 263:10048–10051

    PubMed  CAS  Google Scholar 

  • Mooney RA, Landick R (1999) RNA polymerase unveiled. Cell 98:687–690

    Article  PubMed  CAS  Google Scholar 

  • Ohta N, Matsuzaki M, Misumi O, Miyagishima SY, Nozaki H, Tanaka K, Shin IT, Kohara Y, Kuroiwa T (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10:67–77

    Article  PubMed  CAS  Google Scholar 

  • Pong SS, Loomis WF, Jr. (1973) Multiple nuclear ribonucleic acid polymerases during development of Dictyostelium discoideum. J Biol Chem 248:3933–3939

    PubMed  CAS  Google Scholar 

  • Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618–622

    Article  PubMed  CAS  Google Scholar 

  • Puhler G, Leffers H, Gropp F, Palm P, Klenk HP, Lottspeich F, Garrett RA, Zillig W (1989a) Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci USA 86:4569–4573

    Article  CAS  Google Scholar 

  • Puhler G, Lottspeich F, Zillig W (1989b) Organization and nucleotide sequence of the genes encoding the large subunits A, B and C of the DNA-dependent RNA polymerase of the archaebacterium Sulfolobus acidocaldarius. Nucleic Acids Res 17:4517–4534

    CAS  Google Scholar 

  • Rambaut A (1996) Se-Al: Sequence Alignment Editor. Available at: http://evolve.zoo.ox.ac.uk/software.html?id=seal

  • Roeder RG, Rutter WJ (1969) Multiple forms of DNA-dependent RNA polymerase in eukaryotic organisms. Nature 224:234–237

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sentenac A (1985) Eukaryotic RNA polymerases. CRC Crit Rev Biochem 18:31–90

    PubMed  CAS  Google Scholar 

  • Sklar VE, Jaehning JA, Gage LP, Roeder RG (1976) Purification and subunit structure of deoxyribonucleic acid-dependent ribonucleic acid polymerase III from the posterior silk gland of Bombyx mori. J Biol Chem 251:3794–3800

    PubMed  CAS  Google Scholar 

  • Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci USA 94:4520–4525

    Article  PubMed  CAS  Google Scholar 

  • Stiller JW, Duffield EC, Hall BD (1998) Amitochondriate amoebae and the evolution of DNA-dependent RNA polymerase II. Proc Natl Acad Sci USA 95:11769–11774

    Article  PubMed  CAS  Google Scholar 

  • Sweetser D, Nonet M, Young RA (1987) Prokaryotic and eukaryotic RNA polymerases have homologous core subunits. Proc Natl Acad Sci USA 84:1192–1196

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Larkin RM, Guilfoyle TJ (1995) Arabidopsis expresses two genes that encode polypeptides similar to the yeast RNA polymerase I and III AC40 subunit. Gene 167:203–207

    Article  PubMed  CAS  Google Scholar 

  • Vassylyev DG, Sekine S, Laptenko O, Lee J, Vassylyeva MN, Borukhov S, Yokoyama S (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 A resolution. Nature 417:712–719

    Article  PubMed  CAS  Google Scholar 

  • Young HA, Whiteley HR (1975) Deoxyribonucleic acid-dependent ribonucleic acid polymerases in the dimorphic fungus Mucor rouxii. J Biol Chem 250:479–487

    PubMed  CAS  Google Scholar 

  • Young RA , (1991) RNA polymerase II. Annu Rev Biochem 60:689–715

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Li J, Liu Z, Qi Q, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Zhao W, Li P, Chen W, Zhang Y, Hu J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Tao M, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Campbell EA, Minakhin L, Richter C, Severinov K, Darst SA (1999) Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 A resolution. Cell 98:811–824

    Article  PubMed  CAS  Google Scholar 

  • Zillig W, Klenk HP, Palm P, Puhler G, Gropp F, Garrett RA, Leffers H (1989) The phylogenetic relations of DNA-dependent RNA polymerases of archaebacteria, eukaryotes, and eubacteria. Can J Microbiol 35:73–80

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank John Stiller and Yajuan Liu for stimulating and helpful discussions and Ken Karol for providing green algal cultures.

Author information

Authors and Affiliations

  1. Department of Biology, University of Washington, Seattle, WA, 98195, USA

    Jie Luo & Benjamin D. Hall

Authors
  1. Jie Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benjamin D. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamin D. Hall.

Additional information

[Reviewing Editor: Dr. Patrick Keeling]

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Luo, J., Hall, B.D. A Multistep Process Gave Rise to RNA Polymerase IV of Land Plants. J Mol Evol 64, 101–112 (2007). https://doi.org/10.1007/s00239-006-0093-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-006-0093-z

Keywords

Search

Navigation